Scandinavian Journal of Gastroenterology. 2015; 50: 832–840

ORIGINAL ARTICLE

Manifestations of inflammatory bowel disease in patients of Haitian and Cape Verdean descent CHRISTOPHER STALLWOOD1, KARENPREET SHERGILL2, JOSEPH WU3, FRANCIS A FARRAYE1, HANNAH L MILLER1 1

Section of Gastroenterology, Boston Medical Center, Boston University School of Medicine, Boston, MA, USA, Department of Epidemiology, School of Public Health, Boston University, Boston, MA, USA, and 3 Department of Biostatistics, School of Public Health, Boston University, Boston, MA, USA 2

Abstract Objective. Several studies have reported unique ethnic phenotypes of inflammatory bowel disease (IBD). An appreciation of disease manifestations in different populations may improve clinical outcomes. There are no studies examining IBD in patients of Haitian or Cape Verdean descent. We sought to define the IBD phenotype in these populations. Materials and methods. This was a retrospective review comparing Haitian and Cape Verdean immigrant IBD patients to Caucasians, all receiving care at Boston Medical Center in Boston, Massachusetts, USA. The following variables were analyzed: family history, smoking history, vaccinations/cancer screening, age of diagnosis, disease duration, disease location, medication use, and complications. Results. Thirty-one Haitians and 21 Cape Verdeans were matched to Caucasian controls. Haitians (mean age 42 years) and Cape Verdeans (mean age 47 years) with Crohn’s disease were diagnosed with IBD later than Caucasians (mean age 31 years, p = 0.04 and 0.02, respectively). Haitians with Crohn’s were less likely to have a history of tobacco use compared to Caucasians (13% vs. 51%, p = 0.02). Cape Verdeans with Crohn’s were less likely to have perianal involvement (0% vs. 50%, p = 0.01). Haitians with IBD were less likely to have ever used glucocorticoids (48% vs. 76%, p = 0.02). There was no difference in vaccination rates, cancer screening, or disease complications. Conclusions. This study demonstrates differences in IBD presentation and disease course among Haitians and Cape Verdeans. Our results suggest a more mild disease in these ethnic groups. Future studies are needed to identify the influence of environmental factors.

Key Words: Cape Verde, Crohn’s, ethnicity, Haiti, inflammatory bowel disease, ulcerative colitis

Introduction Inflammatory bowel disease (IBD) is a chronic disease of the gastrointestinal tract that affects approximately 1.4 million people in the United States [1,2]. Genetic and environmental factors, as well as host immune system responses, likely all play a role in the pathogenesis. There are large variations in the incidence and prevalence of IBD among different populations [3]. Most epidemiologic studies are from Western countries, where the incidence of IBD is highest, and comprehensive databases exist [2].

The global incidence of IBD, however, is rising [4], and a recent study using a large national database in the United States demonstrated an increasing rate of hospitalizations in Asian and African-American patients with Crohn’s disease (CD) and ulcerative colitis (U C) over the last few decades [5]. Another recent study from Canada suggested ethnic disparities in the clinical features of IBD [6]. Taken together, such observations have fueled an interest in the differing manifestations of IBD in various ethnic populations living in North America.

Correspondence: Christopher Stallwood, MD, Internal Medicine Resident, Department of Medicine, Section of Gastroenterology, Boston Medical Center, Boston University School of Medicine, 85 East Newton Street, Boston, MA, USA. Tel: +1 905 975 7993. Fax: +1 888 980 6391. E-mail: [email protected] This article was originally published with errors. This version has been corrected. Please see Erratum (http://dx.doi.org/10.3109/00365521.2015.1017333)

(Received 23 October 2014; revised 20 December 2014; accepted 11 January 2015) ISSN 0036-5521 print/ISSN 1502-7708 online  2015 Informa Healthcare DOI: 10.3109/00365521.2015.1008034

IBD in Haitians and Cape Verdeans Over the last few years, several studies have reported unique clinical phenotypes of IBD in certain ethnicities [7–11]. It has been estimated that there are greater than 600,000 individuals of Haitian or Cape Verdean descent living in the United States [12,13], though there are currently no studies examining the clinical features of IBD in these patients. A better understanding of the disease manifestations in these populations may improve clinical outcomes. We sought to define the clinical characteristics of IBD in these ethnic groups treated at Boston Medical Center, a safety net hospital in Boston, MA. Methods Study design and patient population Data were collected with the approval of the Institutional Review Board at Boston University/Boston Medical Center. This was a retrospective review of adult patients, age 18–89, with IBD seen in the Center for Digestive Disorders from June 1, 2003 to May 31, 2013. Records were electronically queried for the International Classification of Diseases, 9th Revision codes 555.x (enteritis) and 556.x (colitis) as well as a documented ethnicity of Haitian or Cape Verdean (study populations) or Caucasian (control group). All patients were living in the United States at the time of the office visit. The diagnosis of IBD was confirmed by chart review. Thirty-one Haitian patients and 21 Cape Verdean patients were included in the study (52 total). They were randomly matched by sex and age with 52 Caucasian controls. Ethnicity was selfreported by the patients upon registration. The electronic medical record, including clinical notes, laboratory data, procedure reports, pathology reports, and hospitalization summaries, was reviewed by two independent authors. Patients were excluded if the diagnosis of IBD could not be confirmed by chart review. Outcomes Patient characteristics of sex, age, ethnicity, and smoking history were recorded. Clinical data of health maintenance were also recorded, specifically purified protein derivative (PPD) status, hepatitis A and B vaccine (or evidence of immunity), and dermatology referral for skin exam in appropriate patients. Characteristics regarding the patient’s IBD were also recorded, specifically, age at diagnosis/duration of disease, family history of IBD, medication use, extraintestinal manifestations (EIM) of IBD, the presence of fistulizing disease, location of disease (CD – gastroduodenal, small bowel, ileocecal, colonic,

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perianal; UC – proctitis, left-sided, pancolitis), surgeries and time to first surgery, hospitalizations and time to first hospitalization. EIM was defined as having at least one of the following: episcleritis, uveitis, iritis, primary sclerosing cholangitis, erythema nodosum, pyoderma gangrenosum, IBD arthropathy, ankylosing spondylitis, or sacroiliitis. For CD patients, surgeries were grouped as follows: small bowel resection/stricturoplasty, ileocolonic resection, colonic resection, or perianal surgery (Seton’s/fistula surgery). For UC patients, proctocolectomy with IPAA or ileostomy was recorded. Medications were recorded from office notes and discharge summaries, and reported as lifetime medication use. Glucocorticoids, 5-ASA (aminosalicylic acid), thiopurines, methotrexate, and anti-tumor necrosis factor (TNF) medications were recorded. Statistical analysis All statistical analyses were performed using SAS version 9.3 (SAS Institute, Inc., Cary, NC, USA). For all dependent variables, comparisons were made between the Caucasian group and each of the two ethnic groups (Haitian and Cape Verdean). For continuous dependent variables, Student’s t-test was used to compare the two-group means. The Folded F-test was used to assess the equality of variances between groups. If variances were equal, the Student’s t-test using pooled variance was used; otherwise, the Satterthwaite t-test was used. For categorical dependent variables, Fisher’s exact test or Pearson Chi-square test of proportions was used. To characterize the differences in disease manifestation between the two IBD disease subtypes, CD and UC, subgroup analysis was performed on selected demographic variables such as smoking status, age of diagnosis, duration of disease, disease locations, and surgery types. Odds ratio and its 95% confidence interval were used to evaluate the direction and strength of the association between the occurrence of IBD-related surgeries or hospitalizations and ethnic groups. This association was tested using the Fisher’s exact test of proportion. Hazard ratio and its 95% confidence interval were used to evaluate the direction and strength of the association between the time from diagnosis to first occurrence of IBD-related surgeries or hospitalizations (in years) and ethnic groups. HRs were estimated using the Cox proportional hazard model. In addition, Kaplan–Meier (or ProductLimit) survival curves were produced to characterize the distribution of time from diagnosis to first surgery or hospitalization. These associations were tested using nonparametric log-rank test. Since subjects were matched on age and sex, associations between

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Table I. Patient demographics. Haitian (n = 31) Sex Male: n (%) Female: n (%) Age (years) Mean (SD) Median Family history of IBD Yes: n (%) IBD classification Crohn’s disease: n (%) Ulcerative colitis: n (%) Smoking history (ever smoker) All: n (%) Crohn’s disease: n (%) Ulcerative colitis: n (%) Age at diagnosis (years) All: Mean (SD, Median) Crohn’s disease: Mean (SD, median) Ulcerative colitis: mean (SD, median) Duration of disease (years) All: mean (SD, median) Crohn’s disease: Mean (SD, median) Ulcerative colitis: Mean (SD, median)

p-Value

Cape Verdean (n = 21)

p-Value

Caucasian (n = 52)

8 (25.8) 23 (74.2)

0.8056

7 (33.3) 14 (66.7)

0.7807

15 (28.8) 37 (71.2)

50.3 (14.7) 52.0

0.4280

44.0 (14.9) 39.0

0.3820

47.5 (15.7) 50.5

2 (6.5)

0.1176

4 (19.1)

1.0000

11 (21.1)

16 (51.6) 15 (48.4)

1.0000

8 (38.1) 13 (61.9)

0.3024

28 (53.8) 24 (46.2)

6 (28.6) 3 (37.5) 3 (23.8)

0.2913 0.6906 0.7082

22 (44.0) 14 (51.1) 8 (34.8)

3 (10.0) 2 (12.5) 1 (7.1)

0.0013 [1] 0.0206 [1] 0.1120

44.1 (17.1, 46.0) 42.2 (14.0, 39.0) 45.8 (20.0, 47.0)

0.0170 [1] 0.0366 [1] 0.1469

38.1 (16.2, 39.5) 47.1 (17.7, 45.0) 32.4 (12.8, 28.0)

0.3047 0.0169 [1] 0.4415

33.7 (15.3, 28.5) 31.2 (14.3, 28.0) 36.7 (16.1, 37.0)

8.2 (5.1, 8.0) 9.7 (5.9, 9.0) 6.8 (3.8, 5.5)

0.0024 [1] 0.0360 [1] 0.0386 [1]

7.2 (5.2, 5.5) 4.6 (3.7, 4.0) 8.9 (5.4, 9.0)

0.0010 [1] 0.0001 [1] 0.3950

13.8 (10.4, 11.0) 15.7 (10.9, 12.5) 11.6 (9.6, 8.5)

Abbreviations: IBD = Inflammatory bowel disease; SD = Standard deviation. Note: [1] p-value < 0.05 comparing to Caucasian group. For categorical variables, p-value is based on Fisher’s exact test, while for continuous variables, it is based on two-sample Student’s t-test.

these IBD-related study outcomes and ethnic groups were considered adjusted for age and sex. Results Demographics There were 31 Haitian patients (16 with CD, 15 with UC) and 21 Cape Verdean patients (8 with CD, 13 with UC) in the study, each randomly matched by age and sex to a Caucasian control (28 with CD, 24 with UC). The study populations were successfully matched by age and sex (Table I). There was no significant difference in IBD classification of CD versus UC (Table I). There was also no difference in family history of IBD (Table I). Regarding tobacco use, Haitians with CD were less likely to have ever smoked tobacco in their lifetime when compared to Caucasians (13% vs. 51%, p = 0.02; Table I). There was no significant difference in smoking history between the Cape Verdean and Caucasian groups. Haitians were diagnosed with IBD at a later age than Caucasian patients (44 years vs. 34 years, p = 0.02; Table I). There was no significant difference in age of diagnosis when comparing Cape Verdeans to Caucasians (38 years vs. 34 years, p = 0.30; Table I). However, when analyzed by disease subtype, we found significant

differences in age of diagnosis only in the CD groups; Haitians with CD were diagnosed at 42 years of age, Cape Verdeans with CD were diagnosed at 47 years of age, and Caucasians with CD were diagnosed at 31 years of age (p = 0.04 and p = 0.02, respectively; Table I). There was no difference between the groups in patients with UC. Haitians and Cape Verdeans with IBD had a shorter duration of disease compared to Caucasians (8 years, 7 years, and 14 years, p = 0.002 and p = 0.001, respectively; Table I). When further analyzed based on disease subtype, we found significant differences in duration of disease only in the CD group (Table I). Routine health-care maintenance for IBD patients There was no significant difference between Haitians or Cape Verdean and Caucasian IBD patients in vaccination rates or documented immunity against hepatitis A or B (Table II). There was also no difference in tuberculosis screening or referral to dermatology for a screening skin exam (Table II). IBD phenotype There was no difference in EIM of disease. There was also no difference in fistulizing disease. Regarding

IBD in Haitians and Cape Verdeans

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Table II. Routine health-care maintenance in inflammatory bowel disease. Haitian (n = 31) Purified protein derivative status Obtained: n (%) 9 (30.0) Hepatitis A Vaccinated: n (%) 7 (22.6) Hepatitis B Vaccinated: n (%) 10 (32.3) Dermatology evaluation Received: n (%) 4 (12.9)

p-Value

Cape Verdean (n = 21)

p-Value

Caucasian (n = 52)

0.2689

7 (33.3)

0.2114

9 (17.6)

0.0908

9 (42.9)

1.0000

21 (43.8)

0.2520

7 (33.3)

0.4317

23 (46.0)

0.7583

3 (14.3)

1.0000

9 (17.3)

Note: None of the comparisons between Cape Verdean/Haitian and Caucasian groups has p-value

Manifestations of inflammatory bowel disease in patients of Haitian and Cape Verdean descent.

Several studies have reported unique ethnic phenotypes of inflammatory bowel disease (IBD). An appreciation of disease manifestations in different pop...
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