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. Author manuscript; available in PMC: 2021 Aug 1.
Published in final edited form as: J Genet Couns. 2020 Mar 30;29(4):616–624. doi: 10.1002/jgc4.1254

Associations of sociodemographic and clinical factors with gastrointestinal cancer risk assessment appointment completion

Jessica E Ebrahimzadeh 1, Jessica M Long 1, Louise Wang 2, John T Nathanson 3, Shazia Mehmood Siddique 2, Anil K Rustgi 4, David S Goldberg 5, Bryson W Katona 2
PMCID: PMC7415544  NIHMSID: NIHMS1573712  PMID: 32227561

Abstract

Cancer risk assessment services are important for patient care; effective use requires appropriate provider referral, accurate scheduling processes, and completed attendance at booked appointments. Sociodemographic and clinical factors associated with gastrointestinal cancer (GIC) specific risk assessment appointments remain unstudied; therefore, we aimed to identify factors associated with appointment completion in a GIC risk assessment program at a tertiary academic center. Retrospective chart review was conducted on all patients scheduled for an appointment in the Gastrointestinal Cancer Risk Evaluation Program (GI-CREP) between January 2016 and December 2017. Data collected included demographic and clinical factors. Chi-square and Wilcoxon rank-sum tests compared variables among patients based on the study outcome of whether a GI-CREP appointment was completed; marginal standardization was used to predict the standardized percentage of patients that had appointment completion. A total of 676 patients had a scheduled GI-CREP appointment; 32 individuals were excluded due to incomplete information or scheduling error, resulting in 644 patients available for final analysis. Our study population was predominantly female (61%), White (77%), married (64%), had private healthcare insurance (76%) and lacked a personal history of cancer (60%). Referrals internal to the healthcare system were most common (77%), with gastroenterologists as the most frequent referring provider (42%). Seventy-five percent of scheduled individuals had appointment completion, while 25% of individuals did not. Independent predictors for GI-CREP appointment incompletion included Medicaid insurance (OR 2.45, 95% CI 1.21-4.28, p=0.01), self-identified Black race (OR 1.97, 95% CI: 1.20-3.25, p=0.008), and personal history of cancer (OR 1.60, 95% CI 1.11-2.31, p=0.01). These data highlight existing disparities in GIC risk assessment appointment completion associated with race, health insurance coverage, and medical status. Further studies of these areas are necessary to ensure equitable access to important GIC risk assessment services.

Keywords: disparities, gastrointestinal cancer, risk assessment, genetics services, access

Introduction

Approximately 5-10% of cancers are thought to be caused by pathogenic variants in high-risk cancer susceptibility genes (Foulkes, 2008; Lichtenstein et al., 2000; Susswein et al., 2016). This has led to development of cancer risk assessment programs which enables both identification of at-risk individuals and implementation of personalized evidenced-based approaches for increased surveillance and risk-reduction interventions (Riley et al., 2012). Over the past few decades, there has been an expansion in knowledge and gene discovery linked to gastrointestinal cancer (GIC) risk (Valle et al., 2019). Relatedly, an increasing number of individuals have been referred to and/or completed genetic counseling and testing associated with hereditary GIC risk and polyposis-related conditions (Slavin et al., 2015).

Referrals for GIC risk assessment and genetic testing may be prompted by personal and/or family history of: multiple gastrointestinal (GI) polyps, GI polyps at a young age, GIC at a young age (e.g., colorectal cancer diagnosed before age 50), multiple cancers in one individual, multiple relatives with related cancers, known pathogenic variant in a cancer risk gene, somatic genetic testing suggestive of germline risk, or tumor pathology (i.e. colon or uterine) with loss of mismatch repair (MMR) protein expression (NCCN, 2019). Multiple professional groups have published guidelines addressing which individuals should be referred for a hereditary GIC risk evaluation (NCCN, 2019; Syngal et al., 2015; van der Post et al., 2015; Weissman et al., 2012). Despite existing criteria, some healthcare providers still have limited knowledge regarding general indications for referral, resulting in low rates of referral among individuals who could benefit from a cancer risk assessment (Rolnick et al., 2011; Wood, Flynn, & Stockdale, 2013). Additional reasons for low referral rates include limited provider time, incomplete family history collection by the provider and incomplete patient knowledge of family history (Delikurt, Williamson, Anastasiadou, & Skirton, 2015; Wood et al., 2014).

One prominent indication for referral to a GIC risk assessment program is abnormal immunohistochemistry (IHC) staining of the MMR genes which is a test becoming increasingly common as standard practice for all colorectal tumors resected at many facilities. Abnormal MMR IHC results (unless attributed to somatic BRAF mutation or MLH1 gene promoter hypermethylation) should prompt referral for hereditary cancer risk assessment due to concern for Lynch syndrome, the most common cause of hereditary colorectal cancer (Yurgelun et al., 2015). Two recent publications identified the rates of provider referral among individuals with abnormal MMR IHC on colorectal tumor tissue at 34% and 49%, illustrating that a significant portion of individuals were not appropriately referred for genetic evaluation for potential Lynch syndrome (Han & Spigelman, 2019; Muller et al., 2018). Factors associated with lower referral rates included older age and advanced tumor stage, and there were significant disparities noted for racial and ethnic minority groups (Han & Spigelman, 2019; Muller et al., 2018). These studies reflect the significant need for improvement in appropriate referral of patients.

Although proper provider referral is imperative, it is also important that patients are scheduled for and attend the GIC risk assessment appointment subsequent to the referral. Understanding factors that are associated with appointment completion is critical, since cancer risk evaluations can be valuable for both the referred individuals as well as their families. Furthermore, cancer risk assessment involves highly trained and specialized physicians and genetic counselors, who are limited in number relative to the expected number of prospective individuals seeking and/or requiring such services (Hoskovec et al., 2018). Unattended appointments result in reduced clinical productivity, vacant clinical spaces that could benefit other healthcare clients, and lost financial revenue. (Dantas, Fleck, Oliveira, & Hamacher, 2018). Thus, low rates of appointment attendance can be a major source of inefficiency for clinics, given the scarcity of genetic resources.

Uptake of hereditary cancer risk assessment appointments has been most well-studied in the context of Hereditary Breast and Ovarian Cancer (HBOC) syndrome, associated with pathogenic variants in the BRCA1 and BRCA2 genes. Characteristics and factors previously correlated with lower uptake of genetics appointments include limited information provided by referring healthcare provider, low socioeconomic status, racial and ethnic minority status, non-private medical insurance coverage, concerns regarding genetic discrimination and long scheduling wait times (Anderson et al., 2012; Forman & Hall, 2009; Humphreys et al., 2000; Nikolaidis et al., 2019; J. Shaw et al., 2018; T. Shaw et al., 2018). However, HBOC data related to attendance are not necessarily generalizable to GIC risk groups given differences between the cohorts. For example, unlike HBOC, some GIC risk syndromes have clinical diagnostic criteria or tumor assays that can be used to determine medical management in lieu of germline molecular testing; this may alter motivations to attend a genetic counseling/testing appointment. Other potential differences may include specialty of referring providers, awareness of reason for referral, and increased representation of men in GIC risk assessment cohorts (Childers, Maggard-Gibbons, Macinko, & Childers, 2018). Given that attendance of appointments in a dedicated GIC-specific risk assessment program remains unstudied, we analyzed sociodemographic and clinical factors of individuals scheduled in a GIC-specific risk assessment program to determine whether sociodemographic and/or clinical factors were significantly associated with appointment completion.

Methods

Participants

All study activities were approved by the University of Pennsylvania Institutional Review Board. Retrospective chart review was conducted over a 2-year period, between January 2016 and December 2017, for all patients who had been scheduled for an appointment in the Gastrointestinal Cancer Risk Evaluation Program (GI-CREP) at the Hospital of the University of Pennsylvania, a tertiary academic center. Reasons for exclusion were incomplete information (e.g., unknown health insurance coverage, unidentified race) or documentation showing incorrect scheduling of a patient in the GI-CREP.

Procedures

Data were collected from the electronic medical record (EMR). Covariates of interest included sociodemographic factors, clinical factors related to the reason for referral to GI-CREP, and referring provider specialty. Demographic data included age at date of scheduled appointment, patient-reported race, sex, marital status (married/not married), health insurance type (private, Medicare, Medicaid, other), and zip code of residence. Personal history of cancer was determined by available chart notes. Referring doctor specialty and institutional affiliation (internal versus external provider) were determined by EMR referral documentation or patient-reported physician listed on a standardized intake form. Median zip code level income was obtained using the U.S. Census Bureau, 2013-2017 American Community Survey 5-Year Estimates (United States Census Bureau, 2017). Distance to clinic was calculated via documented patient home address to hospital address, using shortest driving travel time. Appointment status, including completed appointments, cancellations and no shows, were determined by the EMR. Individuals who had record of a finalized GI-CREP office visit in the EMR were categorized as having appointment completion, whereas individuals who had a cancelled appointment ahead of time, and/or had a no-show for the scheduled appointment were categorized as having appointment incompletion. Patients who had a cancelled and/or no-show for initial appointment but subsequently attended a GI-CREP appointment were categorized as having a complete appointment.

Data Analysis

We used chi-square tests to compare categorical variables among patients based on the study outcome (appointment completion versus appointment incompletion), and Wilcoxon rank-sum tests for continuous variables due to the non-normal distribution of the data. We fit multivariable logistic regression models, and tested covariates with a p-value <0.1 for inclusion in the final multivariable model. We used a backwards variable selection process, whereby we included any covariate that was significant in multivariable models (p<0.05). We tested for a potential interaction between insurance type and race to determine whether the probability of attending a clinic appointment differed by race as a function of insurance. We used marginal standardization to predict the standardized percentage of patients that had appointment completion based on insurance type, race and personal history of cancer. All statistics and calculations were performed using Stata Version 15.0 (StataCorp, College Station, TX).

Results

Over the study period, 676 individuals had at least one GI-CREP appointment scheduled (Figure 1). Thirty-two individuals were excluded due to incomplete information, leaving 644 individuals for the final analysis. The majority of individuals with a scheduled GI-CREP appointment were female (61%), married (64%), had private healthcare insurance (76%), were White (77%), and did not have a personal history of cancer (60%) (Table 1). The median zip-code level income was $77,292, and the median distance between home address and clinic address was 20 miles. Referrals made internally within the healthcare system (77%) were more common than external referrals. Across specialties, gastroenterologists were the most frequent referring provider (42%).

Figure 1: Individuals scheduled in GI-CREP.

Figure 1:

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Inclusion process of individuals scheduled in GI-CREP between January 2016 and December 2018, as well as the outcomes of whether an appointment was completed.

Table 1:

Demographic and clinical characteristics of individuals scheduled for an appointment in GI-CREP

Characteristic Full Cohort
(N=644)		 Completed Appointment
(N=480)		 No Completed Appointment
(N=164)
Sex, Female 390 (61%) 294 (61%) 96 (59%)
Married 411 (64%) 318 (66%) 93 (57%)
Insurance
 Private 489 (76%) 376 (78%) 113 (69%)
 Medicare 108 (17%) 80 (17%) 28 (17%)
 Medicaid 37 (6%) 19 (4%) 18 (11%)
 Other 10 (2%) 5 (1%) 5 (3%)
Race
 White 495 (77%) 382 (80%) 113 (69%)
 Black 88 (14%) 53 (11%) 35 (21%)
 Asian 24 (4%) 19 (4%) 5 (3%)
 Other 37 (6%) 26 (5%) 11 (7%)
Median zip-code level income, dollars, median 77,292 (56,590, 96,250) 78,483 (58,401, 97,617) 71,179 (50,524, 95,847)
Specialty of referring provider
 Gastroenterology 273(42%) 207 (43%) 66 (40%)
 Oncology 184 (29%) 125 (26%) 59 (36%)
 Primary care provider 67 (10%) 51 (11%) 16 (10%)
 Other 120 (19%) 97 (20%) 23 (14%)
Internal Referral 497 (77%) 361 (75%) 136 (83%)
Distance to clinic, miles, median 20 (10, 35) 20 (10, 35) 19 (10, 35)
Personal history of cancer 263 (41%) 182 (38%) 81 (49%)
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Overall, 75% of individuals scheduled in GI-CREP had appointment completion (Figure 1). Of individuals who had appointment completion, 10% had at least one prior no-show or cancelled visit prior to appointment completion. The remaining 25% of individuals did not have a completed visit as determined by appointment cancellation or no-show, with 15% of these individuals having more than one appointment that was not attended.

Several variables were found to be independently associated with incomplete GI-CREP appointments in multivariable models (Table 2). Insurance status was found to be associated with GI-CREP appointment completion; specifically, individuals with Medicaid had over twice the likelihood of incomplete appointments compared to those with private insurance (OR 2.45, 95% CI 1.21-4.28, p=0.01). Race was also identified as a statistically significant variable associated with rate of appointment completion; specifically, Black patients were more likely to have an incomplete GI-CREP appointment compared to White patients (OR 1.97, 95% CI: 1.20-3.25, p=0.008). Lastly, individuals with a personal history of cancer also had an increased likelihood of having an incomplete GI-CREP appointment compared to those without a cancer history (OR 1.60, 95% CI 1.11-2.31, p=0.01). All other variables evaluated were not significant in multivariable models (p>0.1) including sex, marital status, median zip-code level income, referring doctor specialty, referral type (internal versus external provider), and distance in miles from home to the site of the GI-CREP clinic. The interaction of race and insurance was not significant (p>0.1).

Table 2:

Variables associated with a significant likelihood of an incomplete GI-CREP appointment

Variable* Multivariable OR P-value
Insurance 0.034
 Private Reference
 Medicare 1.03 (0.63-1.68) 0.90
 Medicaid 2.45 (1.21-4.98) 0.01
 Other 3.11 (0.83-11.58) 0.09
Race 0.046
 White Reference
 Black 1.97 (1.20-3.25) 0.008
 Asian 0.74 (0.26-2.12) 0.58
 Other 1.32 (0.61-2.82) 0.48
Personal history of cancer 1.60 (1.11-2.31) 0.01
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*

Other variables evaluated but found not to be significant in multivariable models (p>0.1) included: gender, marital status, median zip-code income, specialty of referring provider, referral type (internal or external), and distance in miles from home to GI-CREP clinic.

Marginal standardization was used to help examine the three significant variables (insurance type, race and personal history of cancer) to predict the standardized percentage of patients with a completed GI-CREP appointment (Figure 2). Fifty one percent of individuals with Medicaid had appointment completion, which was significantly lower than the 77% and 74% of people with private insurance and/or Medicare, respectively (p<0.05). Black patients had GI-CREP appointment completion 60% of the time, which was significantly lower than the 77% and 79% of White and Asian patients, respectively (p<0.05). Lastly, individuals without a personal history of cancer had appointment completion 78% of the time, significantly more than the 69% individuals with a personal history of cancer (p<0.05).

Figure 2: Rate of successful completion of a GI-CREP appointment.

Figure 2:

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Marginal standardization was performed to determine the rate of GI-CREP appointment completion by reported insurance type (A), race (B), and personal history of cancer (C). *p<0.05

Discussion

Cancer risk assessment programs play an important role in identifying individuals at increased risk of developing cancer, which is critical for providing surveillance and risk reduction interventions for the individual, and also for providing appropriate recommendations and risk-stratification for family members. We examined sociodemographic and clinical variables of individuals scheduled in a high volume, GIC risk assessment program at a tertiary academic center. Data analysis demonstrated that lower rates of appointment completion occurred among individuals with Medicaid insurance, Black race and personal history of cancer suggesting disparities exist related to access to GIC risk assessment services.

In our cohort, individuals with Medicaid had a lower rate of GI-CREP appointment completion compared to those with private insurance. In the medical and genetic literature, Medicaid insurance is often considered a surrogate for lower socioeconomic status when household income is unknown (Casey et al., 2018). Conversely, there were no significant differences in the rates of GI-CREP appointment completion based on median zip code level income. This discordance is likely representative of the different types of information characterized by these factors; zip code level income is an indicator of area-based socioeconomic status, whereas Medicaid status is an indicator of individual-based socioeconomic status (Berkowitz et al., 2015). Lower rates of appointment completion among individuals with lower socioeconomic status may be in part due to the perception of genetic testing as expensive, which has been previously identified as a barrier to service delivery (Hann et al., 2017). Other studies have found that concern regarding cost and insurance coverage for genetic counseling and/or testing can impede uptake of HBOC risk assessment (Anderson et al., 2012; Forman & Hall, 2009). However, patient out-of-pocket costs for cancer genetic testing have decreased significantly in the last five years, and currently many individuals with Medicaid are eligible for free or low cost genetic testing through financial assistance programs at commercial laboratories. Consequently, it is important for referring providers to be educated on and to inform patients about the often low out-of-pocket cost of genetic testing if patients raise the concern of cost.

Our data also identified racial disparities among individuals scheduled for GIC risk evaluation, which are consistent with previously reported studies in the HBOC population (Armstrong, Micco, Carney, Stopfer, & Putt, 2005; Forman & Hall, 2009; Halbert, Kessler, Stopfer, Domchek, & Wileyto, 2006). Specifically among individuals with a scheduled GI-CREP appointment, Black individuals had a significantly increased likelihood of appointment incompletion compared to White individuals (Table 2, OR 1.97, CI = 1.20-3.25). Previous studies in HBOC cohorts have attempted to clarify other potential variables that could reduce completion of genetic testing among Black women meeting criteria for such consultation (Armstrong et al., 2005; Mays et al., 2012). Possible impacting factors may include lack of awareness of genetic services, concerns regarding genetic information, cultural perceptions, values and quality of relationship with the healthcare provider (Alsan & Wanamaker, 2017; Armstrong et al., 2005; Canedo, Miller, Myers, & Sanderson, 2019; Halbert et al., 2012; Mays et al., 2012).

Notably, the majority of the population in our study self-identified as White (77%) which is not representative of the racially diverse population our healthcare system strives to serve. The paucity of racial and ethnic minorities, including Black and Hispanic individuals in our cohort suggests that the healthcare system itself may not have a patient demographic reflective of the community’s racial demographic, that racial/ethnic minorities are not being referred by their healthcare providers at equal rates to White patients, or appointments were not scheduled for GIC risk assessment despite referral being made. Given that hereditary GIC syndromes affect individuals across all races and ethnic groups, it is important for healthcare providers to uniformly make appropriate referrals of individuals to cancer risk assessment programs, regardless of race/ethnicity (Plummer et al., 2012). Furthermore, providers should ensure they discuss patient-centered rationale and benefits of the service when explaining the reason for the referral to bolster patient understanding and uptake of cancer risk assessment (Shaw et al., 2018).

Multiple studies, mostly focused on HBOC risk assessment, have demonstrated individuals with a personal history of cancer are more likely or equally likely to attend a genetic counseling appointment compared to those without a cancer diagnosis (Willis et al., 2017). In contrast, our results demonstrated individuals with a diagnosis of cancer were less likely to attend a GIC risk assessment visit, raising the possibility of potential distinctions of the GIC cohort. Potential differences between GIC and HBOC cohorts may include: cancer stage at diagnosis, prognosis, the impact of germline genetic test results on surgical decisions, and awareness of hereditary risk factors. Lower rates of appointment completion among individuals with a personal history of cancer may also be related to an increasing number of individuals with advanced metastatic cancer being referred for germline genetic testing due to potential therapeutic implications (Le et al., 2015; Tempero, 2019). Despite the value of completing germline genetic testing, scheduling and attending another in-person visit can be challenging for individuals with advanced cancer given the high morbidity and psychological burden associated with disease (Bauer et al., 2018; Pickard et al., 2016). The recent shift of individuals with advanced cancer being referred for genetic testing not only impacts GIC, but also many other cancer types, such as breast, ovarian and prostate; this may provide an alternative explanation for the lower rates of appointment completion of affected individuals in our study when compared to older literature. There are ongoing studies assessing alternative service delivery models, including a point of care model integrating genetic testing into the standard oncology appointment along with standardized pre-test educational materials; increased physician referrals and patient uptake of genetic testing have both been demonstrated through a point of care approach for individuals with metastatic pancreatic and prostate cancer (Symecko et al, 2019).

Study Limtations

A limitation of our standardized retrospective review of the EMR is that despite identifying characteristics associated with appointment completion, it did not capture motivators or barriers specific to individual patients. Therefore, we cannot know why and how some patients were able to complete their GIC risk assessment appointment and why others could not. Additionally, our study did not include data regarding individuals that may have been referred for a risk evaluation, but never had a scheduled appointment. Furthermore, it is possible that some of the individuals that did not attend an appointment at our center, could have completed a cancer risk assessment outside of our health system. Lastly, there is a possibility the Medicaid population which was used a proxy for low socioeconomic status, may be confounded by other variables, such as disability.

Practice Implications

Our study identified sociodemographic disparities in GIC risk assessment appointment completion. Further understanding of whether specific motivators or barriers may exist could allow for relevant interventions to increase equitable access to these services. One practice implication for referring providers is to provide patient-centered rationale regarding the potential utility and impact of the cancer risk assessment, which may require utilization of multiple communication modalities and repeated articulation. The degree of information provided at the time of referral has been shown to influence whether patients elect to pursue genetic counseling and testing (Hann et al., 2017; Shaw et al., 2018). Furthermore, a designated employee (e.g., intake coordinator, patient liaison, genetic counselor assistant) could provide additional information to improve patient understanding and address concerns, such as cost, in advance of a scheduled appointment.

Research Recommendations

Our study identified disparities among individuals having appointment completion in GI-CREP and also suggests potential disparities in individuals scheduled in GI-CREP. The study design did not allow for characterization of barriers specific to individual patients. Therefore, future directions could include a qualitative prospective study querying individuals regarding specific barriers or motivating factors to better understand appointment completion of GIC risk assessment appointments. For example, structured interviews with patients scheduled for GIC risk assessment could be used to assess competing life stressors and understanding of referral reason. If there are significant variables, this data could then be used to design, implement, and evaluate strategies intended to increase access and utilization of these services. Additionally, our study cohort included fewer racial and ethnic minorities than expected given the racial and ethnic diversity represented in the community our hospital strives to serve. Further studies could be performed to characterize provider referral patterns to add to the understanding of appointment scheduling patterns and attendance in the GI-CREP clinic.

Conclusion

Our study provides a characterization of sociodemographic and clinical factors associated with GIC risk assessment appointment completion. Some of the correlations found in this study population were consistent with previous studies, specifically that lower rates of appointment completion were observed among individuals with Medicaid insurance and Black race with no significant interaction between these two variables. One unique finding of our cohort was that individuals with a personal history of cancer were significantly less likely to have appointment completion compared to those without a personal history of cancer. In summary, these data demonstrate disparities in those who completed a GIC risk assessment appointment and also suggest potential disparities in those who were scheduled in a dedicated GIC risk assessment program. Given the vital role cancer genetics services can provide, further studies are needed to investigate provider referral patterns, scheduling patterns, individual motivators and potential barriers to appointment completion, and strategy implementation aiming to promote equitable access to cancer risk evaluation regardless of race, ethnicity, insurance coverage, health status, or other features that may currently impede equitable care.

Acknowledgements

The study received support from NIH/NIDDK grants K08DK106489 and R03DK120946 (BWK), The Lustgarten Family Colon Cancer Research Fund (AKR, BWK), and The Jason and Julie Borrelli Lynch Syndrome Research Fund (BWK).

Footnotes

Conflict of Interest Statement

Jessica E. Ebrahimzadeh, Jessica M. Long, Louise Wang, John T. Nathanson, Shazia Mehmood Siddique, Anil K. Rustgi, and David S. Goldberg declare they have no conflict of interest.

Bryson Katona reports grants from NIH/NIDDK, paid travel related to a clinical trial from Janssen, and being a consultant for Exact Sciences.

Human Studies and Informed Consent

This study was approved by and conducted according to the ethical standards of the University of Pennsylvania Institutional Review Board (IRB). All applicable international, national, and/or institutional guidelines were followed. The IRB approved this study without requiring informed consent from the participants.

Animal Studies

No non-human animal studies were carried out by the authors for this article.

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