Mucosal Healing Among Black and White Patients With Inflammatory Bowel Disease

Abstract

INTRODUCTION:

Crohn's disease and ulcerative colitis are characterized by chronic inflammation of the gastrointestinal tract. Mucosal healing (MH) is a therapeutic goal in patients with inflammatory bowel disease (IBD). Current data suggest that Black patients may experience worse clinical outcomes than White patients with IBD. This study assessed MH between Black and White patients with IBD.

METHODS:

Retrospective analysis was performed on Black and White adults with IBD who were hospitalized for an active flare. The presence of MH was assessed at 6–18 months after hospitalization. IBD treatments received before and during hospitalization, within 6 months, and 6–18 months after discharge were recorded. C-reactive protein (CRP) levels were collected at hospitalization and 6–18 months after discharge; the difference was reported as delta CRP.

RESULTS:

One hundred nine patients were followed up after hospitalization. Of those 88 (80.7%) were White patients, and 21 (19.3%) were Black patients. White and Black patients received similar proportions of IBD treatment before (P = 0.2) and during (P = 0.6) hospitalization, within 6 months (P = 0.1), and 6–18 months (P = 0.1) after discharge. Black patients achieved numerically higher rates of MH (15/21 = 71.4% vs 53/88 = 60.2%, P = 0.3) and delta CRP (P = 0.2) than White patients, however, not statistically significant.

DISCUSSION:

In patients admitted to the hospital with an IBD flare with similar treatment and care, there was a trend toward higher rates of MH in Black patients compared with White patients. These data suggest that MH is likely not the only factor that is associated with Black patients experiencing worse clinical outcomes when compared with White patients.

INTRODUCTION

Crohn's disease (CD) and ulcerative colitis (UC) are chronic idiopathic diseases of the gastrointestinal tract that are grouped under the term inflammatory bowel disease (IBD). Patients with IBD experience burdensome symptoms, some of which are life-changing, and these patients endure invasive testing as part of their longitudinal care. The therapy for IBD includes immunosuppressive medications that are costly and often have serious risk profiles. Modern therapies are judged based on their ability to improve patient symptoms and quality of life, as well as their ability to heal the lining of the gut.

Racial disparities exist in the care of patients with IBD that can affect disease outcomes. One study examined IBD treatment utilization as their outcomes and found that Black patients were less likely than White patients to be under the care of a gastroenterologist, and among patients with CD, Black patients were less likely to have been on infliximab (1). A large systematic review reported no major differences in IBD medication utilization as well as disease location, disease behavior, involvement of upper GI tract and perianal region, and extraintestinal manifestations across races and ethnic groups (2).

Mucosal healing (MH) has emerged as the most rigorous target endpoint of clinical efficacy for IBD therapies. MH is typically determined by endoscopic assessment of intestinal inflammation and is referred to as the absence of mucosal ulcerations in CD (3). In UC, an international consensus defined MH as the absence of friability, blood, erosions, and ulcers of the gut mucosa (4). Numerous studies have demonstrated that MH is associated with better patient outcomes such as reduced risk of disease relapse, more effective steroid tapering responses, fewer hospitalizations and surgeries, lower rates of colectomies, and improved ability to work (5,6). In addition to MH, other empiric measures for assessing disease activity are commonly used, including findings on cross-sectional imaging and laboratory markers such as fecal calprotectin and C-reactive protein (CRP) (7).

MH in different racial and ethnic populations of patients with IBD has not been well studied. Specifically, previous studies have not examined MH across racial groups (8). Our study investigates Black and White patients hospitalized at a university tertiary care medical center for an IBD flare. These patients had similar medical therapy and access to care before hospitalization and were followed for MH in the subsequent 6–18 months. Our aim was to compare rates of MH in Black and White patients who had similar access to care and IBD therapy utilization.

METHODS

Study population

Between 2013 and 2017, 1,101 adults (>18 years old) with a diagnosis of CD or UC or mixed disease (disease exhibiting features of both CD and UC) were hospitalized for a suspected IBD flare at the University of Florida Shands Hospital and were screened for inclusion in this study (Figure 1). Patients who were pregnant or incarcerated were excluded. Patients who were included in the study were those with an IBD flare which we defined as active disease confirmed by presence of inflammation seen on endoscopy, histology, or cross-sectional imaging. These patients also had to have follow-up within 6–18 months of initial hospitalization to assess MH through endoscopy, histology, or cross-sectional imaging such as computed tomography (CT) and magnetic resonance imaging (MRI). To assess disease activity or MH, endoscopy was the preferred method of evaluation followed by histology and, lastly, cross-sectional imaging. Endoscopy was not performed in all patients for a variety of reasons, either because the prep could not be tolerated, the patient refused, or because patients were too ill to go under endoscopic evaluation. In those cases, evaluation of MH was performed through CT or MRI. The study was approved by the Institutional Review Board (IRB#: 201701678).

[Figure omitted. See PDF]

Data collection

Data were extracted from the electronic medical record. Race was self-reported, and the choices for race in our electronic medical record were the following: Black or African American, White, American Indian or Alaska Native, Asian or Pacific Islander, other, or unknown. IBD treatments received by the patients before and during hospitalization as well as within 6 months and 6–18 months after discharge were collected. IBD treatments were documented as “none,” “steroids,” “biologics,” “immunomodulators,” or “combination therapy” (biologics together with immunomodulators). Steroids included oral or IV prednisone or budesonide. Biologic included infliximab, adalimumab, certolizumab, golimumab, and ustekinumab. Immunomodulator includes azathioprine and methotrexate. IBD treatments received within 6 months and 6–18 months after discharge were collected at the first gastrointestinal follow-up visit within 6 months and 6–18 months after hospitalization. CRP was also collected at hospitalization and 6–18 months after discharge, and delta CRP was calculated by subtracting the 2 values. The presence of MH, defined as resolution of inflammation, was evaluated with the first endoscopy or cross-sectional imaging study 6–18 months after discharge.

Statistical analysis

Categorical variables are reported as N (%), whereas continuous variables are reported as mean ± SD. Group comparisons were performed using χ² tests for categorical variables and t-tests for continuous variables. Primary interest was in assessing evidence of racial disparities in a cohort with equal access to care. With N = 88 White patients and N = 21 Black patients, the study had only 13% power to detect a difference of 10 percentage points on the primary outcome (MH); hence, P > 0.05 does not suggest a lack of group differences. However, the magnitude and direction of group differences are valuable in assessing whether results in this cohort conform with reported racial disparities in other patient populations. All analyses were performed using JMP software (SAS v 16; SAS Institute, Cary, NC).

RESULTS

Demographic information is shown in Table 1. We included 109 adult patients with IBD hospitalized for an active IBD flare who had a follow-up to assess for MH within 6–18 months after hospitalization. Among the 109 patients, the mean age was 38.8 ± 16.7 years, mean weight (kg) was 71.0 ± 21.1, 58% were females, and 87.2% had CD. In terms of racial composition, the majority of the patients with IBD were White patients at 80.7% (88/109), followed by Black patients at 19.3% (21/109). Compared with White patients, Black patients had similar demographics except for a higher proportion of females (73.7% vs 51.2%) and a diagnosis of CD (100.0% vs 84.1%). In terms of treatment, similar proportions of Black and White patients received every type of IBD treatment (none, steroids, biologics, immunomodulators, and combination therapy) before hospitalization (P = 0.2) (Table 1).

Table 1.

Patient characteristics at time of hospitalization

Baseline patient characteristics	Total population (n = 109)	Black patients (n = 21)	White patients (n = 88)	P value
Age (yr)	38.83 ± 16.67	42 ± 14.46	38.07 ± 17.14	0.3
Female, n (%)	63 (57.8%)	17 (80.95%)	46 (52.27%)	0.0129
Weight (mean ± SD)	70.97 ± 21.13	73.17 ± 21.62	70.44 ± 21.10	0.6
Initial CRP (mean ± SD)	64.86 ± 65.79	95.5 ± 77.56	55.14 ± 59.40	0.1
IBD type, n (%)
CD, n (%)	95 (87.16%)	21 (100%)	74 (84.09%)	0.0394
UC, n (%)	13 (11.93%)	0 (0.00%)	13 (14.77%)
Mixed, n (%)	1 (0.92%)	0 (0.00%)	1 (1.14%)
Treatment before hospitalization
Biologic before hospitalization, n (%)	20 (18.35%)	5 (23.81%)	15 (17.05%)	0.2
Immunomodulator before hospitalization, n (%)	6 (5.50%)	0 (0.00%)	6 (6.82%)
Combination biologic and immunomodulator before hospitalization, n (%)	29 (26.61%)	4 (19.05%)	25 (28.41%)
Steroid before hospitalization, n (%)	13 (11.93%)	5 (23.81%)	8(9.09%)
None before hospitalization, n (%)	41 (37.61%)	7 (33.33%)	34 (38.64%)

Steroids includes oral or IV prednisone or budesonide. Biologic includes infliximab, adalimumab, certolizumab, golimumab, and ustekinumab. Immunomodulator includes azathioprine and methotrexate. Combination therapy is a biologic and an immunomodulator.

CD, Crohn's disease; CRP, C-reactive protein; IBD, inflammatory bowel disease; UC, ulcerative colitis.

MH and delta CRP

Within 6–18 months after discharge, MH was achieved in 62.4% (68/109) of all patients. The proportion of Black patients who achieved MH was higher than White patients who achieved MH. MH was achieved in 71.4% (15/21) of Black patients compared with 60.2% of White patients (53/88) within 6–18 months after discharge (P = 0.3) (Figures 2 and 3). Black patients were also found to have numerically higher CRP values at hospitalization and 6–18 months after discharge, but this was not statistically significant; P = 0.1 and P = 0.2, respectively. Delta CRP was calculated by subtracting CRP values at 6–18 months after discharge from CRP during hospitalization. Black patients were found to have the highest delta CRP at 79.3 ± 69.8, but this was not statistically significant (P = 0.2) (Table 2).

[Figure omitted. See PDF]

[Figure omitted. See PDF]

Table 2.

Mean CRP levels at hospitalization and 6–18 months after discharge among White and Black patients who achieved mucosal healing

Characteristic CRP mean ± SD	Total population (n = 26)	Black patients (n = 9)	White patients (n = 17)	P value
CRP at hospitalization	77.22 ± 73.73	111.19 ± 85.02	59.24 ± 62.35	0.1
CRP level 6–18 months after discharge	21.7 ± 30.60	34.07 ± 41.30	15.15 ± 21.88	0.2
Delta CRP	56.64 ± 62.61	79.32 ± 69.81	44.63 ± 58.67	0.2

CRP, C-reactive protein.

MH and subgroups

We also decided to analyze MH among Black and White patients with CD (Table 3), Black and White female patients in the entire patient study population (Table 4), and Black and White female patients with CD (Table 5). For patients with CD, the rates of MH for Black and White patients were 71% vs 61% (Table 3). Among Black and White female patients in the entire patient study population, the rates of MH were 71% and 65% (Table 4). Among only females with CD, the rates were 71% vs 65% (Table 5). Because the rates for these subgrouping are comparable with the rates for the overall cohort, there is little evidence in our data that our findings are associated with gender or having CD.

Table 3.

Percentage of Black and White patients with CD who achieved mucosal healing at follow-up

	Black patients (N = 21)	White patients (N = 74)	P value
Mucosal healing achieved	71.43% (15/21)	60.81% (45/74)	0.4

CD, Crohn's disease.

Table 4.

Percentage of Black and White female patients who achieved mucosal healing at follow-up

	Black patients (N = 17)	White patients (N = 46)	P value
Mucosal healing achieved	70.59% (12/17)	65.22% (30/46)	0.7

Table 5.

Percentage of Black and White female patients with Crohn's disease who achieved mucosal healing at follow-up

	Black patients (N = 17)	White patients (N = 40)	P value
Mucosal healing achieved	70.59% (12/17)	65.00% (26/40)	0.7

Treatment utilization

As mentioned, similar proportions of Black and White patients received IBD treatment before hospitalization (P = 0.2). Both groups were similarly exposed to biologic therapies, an indicator of advanced care in IBD (Table 1).

Likewise, similar proportions of Black and White patients received treatment during hospitalization, within 6 months, and 6–18 months after discharge. The majority of the Black and White patients received combination therapy. A higher proportion of White patients received biologics during hospitalization (2.3% vs 0%), within 6 months (14.7% vs 0%), and 6–18 months (21.6% vs 14.3%) after discharge than Black patients. A higher proportion of Black patients received combination therapy during hospitalization (23.8% vs 20.5%), within 6 months (71.4% vs 55.7%), and 6–18 months (52.4% vs 44.3%) after discharge than White patients; however, neither were statistically significant (Table 6).

Table 6.

Inflammatory bowel disease treatments used during hospitalization, within 6 months, and 6–18 months after discharge among Black and White patients

	White patients (N = 88)	Black patients (N = 21)	P value
Treatment during hospitalization
None	29 (29/88 = 33.0%)	4 (4/21 = 19.0%)	0.6
Steroids	34 (34/88 = 38.6%)	10 (10/21 = 47.6%)
Biologic	2 (2/88 = 2.3%)	0 (0/21 = 0%)
Immunomodulator	5 (5/88 = 5.7%)	2 (2/21 = 9.5%)
Combination	18 (18/88 = 20.5%)	5 (5/21 = 23.8%)
Treatment within 6 months after discharge
None	5 (5/88 = 5.7%)	2 (2/21 = 9.5%)	0.1
Steroids	7 (7/88 = 8.0%)	2 (2/21 = 9.5%)
Biologic	13 (13/88 = 14.7%)	0 (0/21 = 0%)
Immunomodulator	14 (14/88 = 15.9%)	2 (2/21 = 9.5%)
Combination	49 (49/88 = 55.7%)	15 (15/21 = 71.4%)
Treatment within 6–18 months after discharge
None	19 (19/88 = 21.6%)	3 (3/21 = 14.3%)	0.2
Steroids	5 (5/88 = 5.7%)	1 (1/21 = 4.8%)
Biologic	19 (19/88 = 21.6%)	3 (3/21 = 14.3%)
Immunomodulator	6 (6/88 = 6.82%)	3 (3/21 = 14.3%)
Combination	39 (39/88 = 44.3%)	11 (11/21 = 52.4%)

Steroids include oral or IV prednisone or budesonide. Biologic includes infliximab, adalimumab, certolizumab, golimumab, and ustekinumab. Immunomodulator includes azathioprine, methotrexate. Combination therapy is a biologic and an immunomodulator.

Among patients who achieved MH, there were no differences between racial groups in utilization of treatments before and during hospitalization, within 6 months, and 6–18 months after discharge (Table 7).

Table 7.

Inflammatory bowel disease treatments used before and during hospitalization and within 6 months and 6–18 months after discharge among Black and White patients who had achieved mucosal healing

	White patients (N = 53)	Black patients (N = 15)	P value
Treatment before hospitalization
None	18 (18/53 = 34.0%)	6 (6/15 = 40.0%)	0.3
Steroids	5 (5/53 = 9.4%)	3 (3/15 = 20.0%)
Biologic	11 (11/53 = 20.8%)	2 (2/15 = 13.3%)
Immunomodulator	6 (6/53 = 11.3%)	0 (0/15 = 0.0%)
Combination	13 (13/53 = 24.5%)	4 (4/15 = 26.7%)
Treatment during hospitalization
None	18 (18/53 = 34.0%)	4 (4/15 = 26.7%)	0.8
Steroids	20 (20/53 = 37.7%)	6 (6/15 = 40.0%)
Biologic	2 (2/53 = 3.8%)	0 (0/15 = 0%)
Immunomodulator	4 (4/53 = 7.6%)	22 (2/15 = 13.3%)
Combination	9 (9/53 = 17.0%)	3 (3/15 = 20.0%)
Treatment within 6 months after discharge
None	4 (4/53 = 7.6%)	2 (2/15 = 13.3%)	0.2
Steroids	3 (3/53 = 5.7%)	2 (2/15 = 13.3%)
Biologic	9 (9/53 = 17.0%)	0 (0/15 = 0.00%)
Immunomodulator	10 (10/53 = 18.9%)	2 (2/15 = 13.3%)
Combination	27 (27/53 = 51.0%)	9 (9/15 = 60.0%)
Treatment within 6–18 months after discharge
None	12 (12/53 = 22.6%)	3 (3/15 = 20.0%)	0.9
Steroids	2 (2/53 = 3.7%)	1 (1/15 = 6.7%)
Biologic	14 (14/53 = 26.4%)	3 (3/15 = 20.0%)
Immunomodulator	3 (3/53 = 5.6%)	2 (2/15 = 13.3%)
Combination	22 (22/53 = 41.5%)	6 (6/15 = 40.0%)

Steroids include oral or IV prednisone or budesonide. Biologic includes infliximab, adalimumab, certolizumab, golimumab, and ustekinumab. Immunomodulator includes azathioprine and methotrexate. Combination therapy is a biologic and an immunomodulator.

DISCUSSION

MH has emerged as an important targeted endpoint for therapy in IBD. MH is associated with better patient outcomes such as reduced risk of disease relapse, increased ability to attain steroid-free remission, fewer hospitalization and surgeries, lower rates of colectomies, and improved ability to work (5,6). Our data demonstrates that Black patients have higher rates of MH after hospitalization than White patients. The MH changes parallel changes in CRP values among both Black and White patients within 6–18 months after hospitalization.

There is a large body of data across a variety of clinical settings that explores racial disparities in many facets related to IBD treatment and outcomes. Previous data have looked at overall disease severity, disease location and phenotype, treatment differences, variations in medical management, rates of surgery and surgical outcomes, as well as other factors such as resource use and markers of care. To the best of our knowledge, our study is the first to assess the impact of race on MH. Our findings demonstrate no statistically significant difference between Black and White patients with respect to MH.

Overall, racial disparities in IBD outcomes have been heterogeneous. However, a large number of studies suggest that Black patients have increased rates of perianal disease/IBD complications, are less likely to have isolated ileal disease, and are more likely to have penetrating disease (9–16). Black patients are also less likely to get treatment with biological agents and are more likely to be treated with steroids (1). They have an increased need for CD-related surgery and a higher rate of surgical complications (10,17–19).

On the other hand, other studies have demonstrated contradictory findings. For instance, no racial differences have been seen in other studies regarding disease extent, location, and IBD-related surgery (17,20). Various studies found that Black and White patients have similar rates of perianal disease (1,9,21). Studies have also found no significant difference in disease location among racial groups (22–24). Also, multiple studies found no difference in need for IBD-related surgery or surgical management across different races (13,21,25,26). Therefore, consistent findings of racial disparities in IBD location, severity, and complications are not present.

Similarly, no differences in medication utilization and adherence were found among patients with IBD of different racial groups. In a study of data from more than 26 million patient visits, no difference was found in the use of immunomodulators or anti-TNF therapies among patients of different races or ethnicities (13). In addition, a retrospective study conducted in an urban healthcare system found similar use patterns of biologics among Hispanic, Black, and White patients with IBD (25). In a large study of more than 1,000 patients with CD treated with infliximab, no association between race and adherence was found (27). In addition, another recent study of patients receiving injectable biologic therapy reported no significant difference in adherence between White vs non-White patients with IBD (28).

Disparities in access to care is another IBD outcome that has been investigated. Nguyen et al found that Black patients were significantly less likely to see a gastroenterologist or an IBD specialist regularly. Access to specialist care can substantially affect healthcare outcomes, which is evident from other studies of race disparities in outcomes of other diseases, including non–small cell lung cancer and stroke (29,30). One study that analyzed data from the Medicaid Analytic eXtract from 4 states where access to gastroenterologists and IBD-specific medications was uniform found no significant disparities in the use of biologic or immunomodulator therapies between Black and White patients with CD or UC (13).

Our study utilized a population of patients with IBD with similar access to care and medication use and evaluated the primary outcome of MH at follow-up. In our study, Black patients had a higher rate of MH and delta CRP after hospitalization than White patients. This may be related to equal access to care and similar utilization of treatment. Our study design was to investigate MH after hospitalization for a flare of IBD. The requirement for hospitalization effectively minimizes bias associated with access to care because all patients had access to hospitalization, an important access point for patients with IBD. Even before hospitalization, both Black and White patients had similar therapies and received similar therapies during hospitalization, within 6 months, and within 6–18 months after discharge. One additional factor highlighted by our data is the importance of initiating therapy during hospitalization rather than deferring to the outpatient setting. Transition of care from inpatient to outpatient IBD is fraught with uncertainties and has been noted to be an important point associated with high-quality care (31). In the past several years, transitions of care from the inpatient to the outpatient setting have markedly improved at our center and nationwide, although challenges with respect to insurance coverage for advanced therapies and clinic access issues still remain.

Limitations

This was a retrospective cohort study at a single tertiary care center that may have led to inherent selection bias, which would limit generalizability as patients at a tertiary medical center may differ from those in the community. Also, we were not able to gather data on the disease status before hospitalization because most of the patients who were hospitalized were not established within our hospital system before arrival. In addition, because our hospital system is a large tertiary referral medical center with a vast catchment area of the Southeast United States, we receive a large number of patients with no previous establishment or data in our hospital system. The sample size of the study was small, and the relative number of patients demonstrating MH in each racial and gender group was even less. As a result, our study was not adequately powered to detect if the differences in MH among Blacks and Whites are statistically significant. Future studies would benefit from a larger sample size as it would provide more patients in each IBD group (Crohn's and UC), gender, and racial subgroup. There is also the possibility that a degree of survivorship bias is present because severe cases of IBD carry the risk of mortality during admissions for flares and other related complications, thus decreasing likelihood of outpatient follow-up for mucosal surveillance. Strengths of the current study include granular IBD endpoint data to assess for clinical flare and MH by using multiple modalities such as endoscopic findings, biopsies, or cross-sectional imaging (CT or MRI). In the future, it may be beneficial to establish multicenter cohort studies to increase patient sample size and diversity.

Existing literature reports worse clinical outcomes among Black patients than White patients who have IBD. Our data, which compared MH in Black and White patients experiencing an IBD flare requiring hospitalization, demonstrate no statistical difference in healing rates, with a trend toward Black patients experiencing more MH. The patients in this study all had equal access to care and treatment utilization was equivalent. Therefore, our research suggests that lack of MH may not be the sole factor involved in poor clinical outcomes among Black patients with IBD. Instead, other factors may play a significant role.

Study Highlights

WHAT IS KNOWN

• ✓ Black patients have worse clinical outcomes than White patients in IBD.

WHAT IS NEW HERE

• ✓ Mucosal healing rates were similar among Black and White patients with IBD.

CONFLICTS OF INTEREST

Guarantor of the article: Devika Dixit, MD.

Specific author contributions: D.D.: planned and conducted the study, collected and interpreted data, and drafted and edited the manuscript. N.C.R.: planned and conducted the study and collected and interpreted data. S.S., A.D., and V.I.R.: drafted and edited the manuscript. S.Q.: collected the data and edited the manuscript. D.N.: interpreted data. S.D.R.: planned the study and edited the manuscript. E.M.Z.: performed interpretation and manuscript review. A.Y.K.: oversaw the project and performed manuscript preparation.

Financial support: None to report.

Potential competing interests: None to report.

Author Notes

Correspondence: Devika Dixit, MD. E-mail: [email protected].

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