INFLAMMATORY BOWEL DISEASE IN UNDERSERVED POPULATIONS: LESSONS FOR PRACTICE

Abstract

Purpose of review:

The incidence of inflammatory bowel disease (IBD) is increasing in minority groups across the United States. There are racial and ethnic disparities in IBD care and outcomes that are rooted in historical injustice and inequities in the social determinants of health.

Recent findings:

Current literature has identified racial, ethnic, and sociodemographic disparities in therapeutics and outcomes for IBD including disease severity, morbidity and mortality.

Summary:

Strategies to achieve equity in IBD include tackling structural racism as a driver of health disparities and making actionable changes against multi-level barriers to care.

Introduction

Inflammatory bowel disease (IBD), which encompasses Crohn’s disease (CD) and ulcerative colitis (UC), is a disorder characterized by chronic inflammation of the gastrointestinal tract, and can be associated with significant morbidity and frequent healthcare utilization. An estimated 3 million individuals in the United States (US) are living with IBD, and the prevalence continues to increase both nationally and globally (1). While IBD has historically affected White populations at a greater prevalence compared to other groups, there is a rising incidence in minority populations, and it is imperative to recognize this trend to reduce disparate health outcomes (2, 3).

This review provides an overview of current data on IBD in underrepresented racial and ethnic minority groups in the US, defined as any group other than non-Hispanic White, with an emphasis on Black and Hispanic populations, the two largest minority groups in the US. The scope of this review first addresses the changing epidemiology of IBD and differences in disease phenotype by race and ethnicity, and second is followed by an overview of structural inequities for historically marginalized groups, evaluation of barriers to care resulting in disparate outcomes for minority patients with IBD, and third and lastly lessons for practice to achieve equity in IBD across all racial and ethnic groups.

A Changing Landscape: Differences in Phenotype and Presentation

The incidence of IBD is increasing in racial and ethnic minorities across the US. A population-based cohort study from 1970 and 2010 demonstrated increases in IBD incidence for Whites and minorities by 39% and 134% respectively (3). While IBD was historically understood to affect predominantly White populations of European descent, the increased incidence in minority groups is reflective of changes in the racial and ethnic profile of the US population (1–3).

In this context, it is important to recognize variations in clinical phenotypes based on race and ethnicity to ensure timely diagnosis and management. A recent systematic review and meta-analysis of 198 population-based cohort studies of adult IBD patients compared CD and UC in White (337,670), Black (1,528), Hispanic (8,37), and Asian (156,127) patients (4). Black patients with CD were found to have a higher proportion of penetrating disease and a smaller proportion of ileal and non-penetrating, non-stricturing disease compared to other groups (4). Black patients were also found to have higher incidence of perianal disease compared to White patients (0.31 vs. 0.14, p=.02) (4). There is similar data for pediatric IBD patients – one study found higher rates of stricturing and penetrating CD in Black children compared to White (51.3% vs 27.4%; P=0.006) (5). Studies comparing IBD phenotypes in Hispanics to non-Hispanic White patients found similar disease behavior in both groups, except for reduced upper gastrointestinal Crohn’s in Hispanics (6, 7). Data on Asian CD patients found a larger proportion of isolated upper GI involvement in this group compared to White patients (Table 1) (4).

Table 1:

Overview of variations in clinical phenotypes for non-White Race and Ethnicity, as compared to White patients, based on available data.

Overview of Variations Clinical Phenotypes by Race and Ethnicity
Black	Hispanic	Asian
Crohn’s Disease
• Higher proportion of penetrating disease4,5  • Smaller proportion of ileal and nonpenetrating, non- stricturing disease4  • Higher incidence of perianal disease compared to White patients4	• Similar disease behavior, except for reduced upper gastrointestinal disease6,7	• Larger proportion of isolated upper GI involvement4
Ulcerative Colitis
• Lower rates of proctitis4*
Extraintestinal Manifestations
•Higher prevalence of uveitis10  • Increased rate of arthralgias in CD patients11  • Increased ankylosing spondylitis and/or sacroiliitis in UC11	• Higher prevalence of erythema nodosum10

^*Mixed evidence, as one small study found no significant difference in extent or location of colitis based on race (8).

Data on racial differences in UC are variable. Shi et al. identified significantly lower rates of proctitis in Black and Hispanic patients compared to White patients (4). However, a small retrospective cohort study examining disease extent and severity in UC by race concluded no significant differences in extent of colitis, i.e. proctitis vs left sided vs pancolitis, based on race (Table 1) (7, 8).

In addition to disease location and behavior, there is data to suggest racial differences in incidence of extraintestinal manifestations (EIMs) (9). Nguyen et al. found that Black patients had significantly greater prevalence of uveitis compared to White patients (8.1%vs 1.6%, p < 0.001), and Hispanic patients had significantly higher prevalence of erythema nodosum than White patients (10.7%vs 3.4%, p < 0.001) (10). Sofia et al. found an increased rate of arthralgias in Black CD patients (36.5 vs. 23.9 %, p<0.01) and ankylosing spondylitis and/or sacroiliitis in Black UC patients (7.1 vs. 1.6 %, p = 0.035) compared to White patients (Table 1) (11).

Alongside differences in phenotype, there may be variations in disease presentation, namely age of diagnosis and severity of disease at diagnosis. Some data report minorities with IBD present at older age compared to White groups ((12, 13), which may be related to barriers to care. It is important to recognize the rising incidence of IBD in minority patients and differences in phenotype by race and ethnicity to minimize delays in diagnosis, treatment, and complications for this patient population.

Overview of Structural Inequities

In underserved minority groups, the etiology of poor outcomes across several chronic medical conditions is multilayered and often stems from the intersection of structural inequities and social determinants of health (SDOH).

Structural inequities are personal, interpersonal, institutional, and systemic drivers, such as racism, sexism, and homophobia, which impact the distribution of healthcare resources and outcomes (14). Policies often foster disparities at all levels with long-term effects on adverse outcomes (14).

The intersection of structural inequities and health disparities are not unique to IBD. An example of a policy that underlies structural inequities is historic “redlining.” This term refers to lending and/or insurance discrimination that bases credit decisions on “desirability (15).” Although now banned in the US, “redlining” is an example of a historical, structural inequity with implications on health today. A majority of areas “redlined” remain low-to-moderate income and communities of color. A recent study found residents of historically redlined neighborhoods were nearly twice as likely to have poor health compared to non-redlined areas (15). A study examining 8 cities in California demonstrated a link between historically redlined communities and a significant increase in ED visits for individuals with asthma (16). These communities were predominantly Hispanic and Black and reflect those who are frequently affected by discriminatory housing policies (16). In IBD, understanding structural inequities helps provide insight into disparities and provides a potential lead point to improve care.

Barriers to Care for Marginalized IBD Populations

Structural inequities create barriers to delivering equitable care in IBD. One confounder when understanding disparate outcomes in underrepresented groups is the role of diagnostic delays. A large cohort study of pediatric IBD patients revealed that Black children were more likely to be older than 12 years of age when diagnosed with IBD than non-Black children(13). These findings raise concerns that the older age of IBD diagnosis observed in Black children may be in part due to a low index of suspicion for IBD in minority children among medical providers. Additionally, evidence suggests that Black patients with IBD are less likely than White patients to be under the regular medical care of a gastroenterologist or IBD specialist (17). In the same study, Black patients more often than White patients reported difficulty with obtaining specialist referrals and greater concerns over healthcare-related costs (17). Delays in diagnosis and specialist referral illustrate the potential knowledge gap in healthcare providers about IBD in minority groups and highlight a complex contributor to disparities in this population.

Patient factors that contribute to barriers to care are often linked to socioeconomic status (18). Older Black patients with IBD are at the highest risk of having low health literacy (19). Health literacy is important for adherence to therapies and establishing trust with providers. This was supported by a qualitative analysis of Black and White patients undergoing IBD surgery that cited barriers to a positive surgical experience included inadequate personal knowledge of IBD, ineffective written and verbal communication, lack of a support system and complications after surgery (20).

Racism in medicine is a deep-rooted systemic problem that continues to undermine equitable care among minorities. The history of medical experimentation, abuse, lack of consent and lack of trust, expose that racism is embedded in SDOH and impacts outcomes across several disease states (21). A single-center study of IBD patients demonstrated that trust-in-physician, race, and age remained predictors of adherence to medical management (22). Differences in therapeutic practice also raise concern of treatment bias. A study from the University of North Carolina reported Black patients with CD had 3 times the risk of treatment with steroids when compared to Whites (23). Retrospective data suggests Black and Hispanic patients received fewer prescriptions for immunomodulators and biologics despite adjustments for disease severity (7, 24). A systematic review identified, race-based differences in medical therapy, and found lower rates of potentially disease-modifying drug use among minority patients (18). Furthermore, despite the increase in IBD clinical trials and the importance of clinical trials to advance care and outcomes for IBD patients, participation is low amongst Black and Hispanic patients (25). Collectively, the presentation, treatment, and outcomes of underrepresented minority patients with IBD are directly linked to both structural and systemic barriers in health care.

Disparities in Clinical Outcomes

Healthcare Utilization

Racial and ethnic differences in ED utilization, hospitalization, readmission and length of stay have been reported. At a single university ED, Black IBD patients were noted to have ED admission rates up to three times that of White IBD patients (26). Similar findings have been demonstrated in the pediatric population, where one study found Black CD children to have a higher percentage of ED visits compared to White children (33% vs 22%)(27).

Disparate outcomes have also been noted in hospitalizations, length of stay and readmissions. A single-center retrospective study assessed rates of CD hospitalizations by race and ethnicity and found hospitalizations were four times higher for those in the lowest income group compared to the highest income group on unadjusted analysis, and twice as high in an adjusted analysis (28). In addition, Black patients in the study were twice as likely to have a CD-related hospitalization in comparison to White patients, illustrating the separate yet distinct disparities due to poverty and race/racism. In contrast, a multicenter study of 145 CD patients found no difference in the number of GI-related hospitalizations between Black and White patients (23). A study in the pediatric population found 37% increased odds of increased hospital length-of-stay (LOS) in Black and Hispanic children with CD in comparison to White children with CD (29). Similarly, a study looking at readmission in pediatric CD patients found 16% increased risk of readmission 1 year after the first admission and a slightly increased LOS in Black CD patients (5 vs 4 days) in comparison to White CD patients (30).

Disparities in Surgical Outcomes

Racial and ethnic disparities in IBD-related surgeries and outcomes have also been noted. One study found that Black and Hispanic patients with UC had lower colectomy rates in comparison to White patients (0.46, p<0.001 and 0.74, p = 0.009) after adjustment for multiple confounders (31), however, Black patients in the study had longer time to surgery in comparison to White patients (8.8 vs 5.6 days, p 0.02). While there was no difference in in-hospital mortality rates by race, Medicaid patients had in-hospital mortality rates that were 3.3 times higher than privately insured patients (31). A study of CD patients found lower incidence rate ratios for bowel resection for Black patients (0.68, CI 0.61–0.76), Hispanic (0.70, 95% CI 0.60–0.83) and Asian/Pacific Islanders (0.31, CI 0.16–0.59) in comparison to White patients on multivariate analysis (32). In contrast, a systematic review describing the phenotypes of 525,425 patients from 198 unique studies found that Black and Hispanic patients with UC had higher rates of cumulative surgery compared to White and Asian patients respectively (0.18 and 0.29 vs 0.11 and 0.07, p<0.01). Similar findings were seen in CD with Black and Hispanic patients again showing higher cumulative surgery rates compared to White and Asian patients (0.41 and 0.49 vs 0.32 and 0.29) (4). Furthermore, a study including 9513 patients who underwent bowel surgery for CD noted that Black patients were more likely to undergo ostomy creation and were more likely to be smokers (33, 34). Observed differences in surgery rates between studies may be attributed to differences in sample size or other geographic, cultural or practice-based differences between the study samples.

Poor outcomes after IBD surgery have also been noted. One study found that Black patients had a higher proportion of death or serious morbidity within 30 days of IBD surgery compared to White patients (27% vs 19.3%, p< 0.001) (35). Another study found that Black, Hispanic, and Asian IBD patients had a longer length of stay after IBD surgery compared to White IBD patients. In the study, Black patients had an increased likelihood of bleeding requiring transfusion, sepsis and renal insufficiency compared to White patients (35). Similar findings were noted in another study where Black patients were noted to have 38% increased odds of major complication after IBD surgery compared to other racial and ethnic groups (33). No racial differences in postoperative mortality were noted similar to what was seen in other studies (31, 33, 35).

Identifying Potential Solutions

Our review shows evidence of disparities for racial and ethnic minorities with IBD in the US. An overarching theme is the challenge with Access to Care (Figure 1). With the incidence of IBD in minorities on the rise, it is important for providers to acknowledge this challenge in order to provide equitable care for all patients. Furthermore, to tackle structural inequities we must recognize structural racism as the underlying driver of health disparities. This can be strengthened by Critical Race Theory (CRT), the analysis of the intersection of racism, marginalization and structural inequities that impact disparities among racial groups today. The use of CRT in education, research and patient care can provide an approach to measure and address racism-related factors that can affect IBD outcomes (36).

Figure 1:

Barriers underrepresented ethnic minorities challenge with accessing equitable specialty care in IBD and potential solutions.

At the patient facing level, healthcare providers are well-positioned to act as catalysts of change (Figure 1). Within IBD clinics there are several actionable solutions that can be put in place to advance equity for all IBD patients. First, is the incorporation of SDOH screening tools into clinical practice (37). There are several validated tools to assess the social determinants of health at the point of care, such as the Protocol for Responding to and Assessing Patients’ Assets, Risks and Experiences (PRAPARE) measure or the Health-Related Social Needs Screening Tool (38, 39). Once social needs have been identified, it is important to connect patients to resources that are appropriate to their needs. Second, the incorporation of patient navigators into regular outpatient IBD care is an important intervention for the reduction of health disparities (40). Patient navigation has been found to be successful in multiple clinical settings including primary care (41), the cancer screening continuum (40, 42, 43), and HIV care (44, 45). Third, IBD clinics should work to understand the unique experiences and potential barriers faced by marginalized patient groups using patient experience surveys or focus groups (37). Much can be learned directly from the patient regarding strategies to improve care and address barriers. From qualitative IBD studies examining experiences by race, effective communication in varying platforms in a way that resonates with patients and in a way that the patient understands, remains pivotal in improving experiences in underserved groups (20). Lastly, other measures that IBD clinics can take to address patient barriers to care include ensuring availability of language services, expanding clinic hours to increase accessibility (e.g. evening and weekend clinics), providing access to transportation fare and childcare services during appointments, incentivizing benchmarks for providers, and partnering with local community organizations (37).

Conclusion

As the demographic profile of the US population continues to change, and traditionally racial/ethnic minority groups increase in number, there will be parallel changes in the epidemiology of health conditions such as IBD. Data has shown minority patients with IBD experience disparate outcomes at multiple levels, due to longstanding barriers to care in marginalized groups. These include structural inequities that shape social determinants of health and lack of patient and provider knowledge about IBD in minority patients. Achieving health equity will require recognition of these complex forces, advocacy for change, and action by providers and larger healthcare systems.

KEY POINTS.

• Race and socioeconomic-based disparities impact IBD outcomes, including diagnostic delays, in-hospital mortality rates and health-related quality of life.

• Delays in diagnosis may be due to limited access to specialists, but can also result from disease perceptions or decreased knowledge about CD and UC in non-White populations

• Achieving health equity in IBD involves targeting modifiable risk factors in a multilevel context: structural inequities, social determinants of health, gaps in knowledge, and at the patient-provider level.