Celiac Disease in African-Americans

Abstract

Celiac disease is generally under diagnosed in the United States and it is unclear whether the disease is encountered in ethnic minorities. Our purpose is to describe a case series of African-American patients with celiac disease. Nine (1.3%) African-American patients with celiac disease were identified from a prospectively generated database of 700 patients with biopsy proven celiac disease and seen between 1981 and 2004. Females predominated, with seven, compared to two males. Diarrhea was the presentation in only two patients, while three presented with iron deficiency anemia. One third had at least one autoimmune disease. Compliance with a gluten-free diet, the only medical therapy of this disease, was poor. Only four patients adhered strictly to the diet. Celiac disease occurs in African-Americans and may well be underdiagnosed. Special attention needs to be given to methods that encourage adherence to the diet in minority groups.

Full text

Dig Dis Sci (2006)
DOI 10.1007/s10620-005-9000-5
ORIGINAL PAPER
Celiac Disease in African-Americans
Pardeep Brar · Ann R. Lee · Suzanne K. Lewis ·
Govind Bhagat · Peter H. R. Green
Received: 11 August 2005 / Accepted: 17 August 2005
C

Springer Science+Business Media, Inc. 2006
Abstract Celiac disease is generally under diagnosed in
the United States and it is unclear whether the disease is en-
countered in ethnic minorities. Our purpose is to describe a
case series of African-American patients with celiac disease.
Nine (1.3%) African-American patients with celiac disease
were identified from a prospectively generated database of
700 patients with biopsy proven celiac disease and seen be-
tween 1981 and 2004. Females predominated, with seven,
compared to two males. Diarrhea wasthepresentationinonly
two patients, while three presented with iron deficiency ane-
mia. One third had at least one autoimmune disease. Compli-
ance with a gluten-free diet, the only medical therapy of this
disease, was poor. Only four patients adhered strictly to the
diet. Celiac disease occurs in African-Americans and may
well be underdiagnosed. Special attention needs to be given
to methods that encourage adherence to the diet in minority
groups.
Keywords: African-American
.
Celiac disease
.
Compliance
.
Gluten-free diet
.
HLA DQ typing
Introduction
Celiac disease is an autoimmune enteropathy that occurs in
genetically predisposed individuals and is precipitated by
the ingestion of gluten containing grains [1]. The disease is
P. Br ar · A. Lee · S. Lewis · G. Bhagat · P. H. R. Green
Department of Medicine, Columbia University
College of Physicians and Surgeons,
New York, New York, USA
P. H. R. Green (

)
Herbert Irving Pavilion, Room 645, 161 Fort Washington Avenue,
New York, New York 10032
e-mail: pg11@columbia.edu
multigenetic, however, there is a requirement that an individ-
ual must possess the HLA alleles that encode for DQ2 and/or
DQ8 [2]. These molecules are involved in the presenta-
tion of pathogenic deamidated gliadins to antigen presenting
cells [3].
Formerly, celiac disease was considered rare in the United
States; however, it is now estimated to occur in about 1% of
the population [4, 5]. The prevalence of this disease in mi-
nority populations within the United States is not known.
It is, however, considered rare in African-Americans, partly
because HLA DQ2 and DQ8 are regarded as primarily Cau-
casian genetic traits. We have, however, detected celiac dis-
ease in African-Americans at our institution and present
these findings in the current report. This is especially impor-
tant because celiac disease, an eminently treatable condition,
is considered to be underrecognized in the United States.
Methods
African-American patients who were treated for celiac dis-
ease at the Celiac Disease Center of Columbia University
were identified from an anonymized database of 700 celiac
disease patients (65% females and 35% males). We defined
African-American patients as those Black patients who re-
ported their ethnicity as African-American. Only biopsy-
proven celiac disease patients were included in this study.
Data regarding age, sex, age at diagnosis, mode of presen-
tation, serologic profiles, and response to a gluten-free diet
were prospectively recorded.
Small bowel histology was reviewed for all patients. The
study was approved by our institutional review board. All pa-
tients had intraepithelial lymphocytosis and villous atrophy
corresponding to Marsh stage III [6]. We classified the degree
of villous atrophy as partial villous atrophy (PVA), subtotal
villous atrophy (STVA), or total villous atrophy (TVA).
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Dig Dis Sci (2006)
Table 1. Demographics, presentation mode, serology, and histopathology.
Age at Mode of
No Sex diagnosis (yr) presentation Associated conditions IgA/G EMA or tTG Villous atrophy HLA DQ2/8
1M64 Anemia ++ Subtotal DQ2
2F37 Edema + NA Subtotal DQ2
3 F 54 Incidental at EGD Rheumatoid arthritis, SLE +− Partial NA
4 F 30 Anemia Myasthenia gravis, DH + NA Partial NA
5 F 59 Anemia IDDM + NA Subtotal NA
6 F 83 Diarrhea MC, osteo-porosis ++ Partial NA
7 F 28 Diarrhea DH + NA Partial DQ2
8 F 15 Abdominal pain −− Partial DQ2/8
9 M 15 Growth failure −+ Partial NA
Note. EGD, esophagogastroduodenoscopy; +, present; −, absent; NA, not assessed; EMA, endomysial antibody; tTG, transglutaminase antibody;
M, male;F, female; SLE, systemic lupus erythematosus; DH, dermatitis herpetiformis; IDDM, insulin-dependent diabetes mellitus; MC, microscopic
colitis.
Results
A total of nine African-American patients, two males and
seven females (Table 1), were identified from the database
of 700 patients, representing 1.3% of all patients. Their mean
age at time of diagnosis was 42 years. Two were children,
aged 15 years.
Only two (22%) patients presented with the classi-
cal presentation of diarrhea. The other seven patients had
“silent” celiac disease, presenting with iron deficiency ane-
mia (n =3), abdominal plain (n =1), growth failure (n =1),
edema because of hypoalbuminemia (n =1), and one as
an incidental finding during endoscopy for gastrointesti-
nal bleeding. Two had already been diagnosed with biopsy-
proven dermatitis herpetiformis, though they had not been
advised about a gluten-free diet. Two had osteoporosis and
three patients had autoimmune diseases, including myasthe-
nia gravis, systemic lupus erythematosus, rheumatoid arthri-
tis, and insulin-dependant diabetes mellitus. One patient had
concomitant microscopic (lymphocytic) colitis.
Serology, HLA, and pathology (Table 1)
All patients had at least one serologic test performed at the
time of diagnosis and all except one had at least one positive
serologic result. Three of five patients had either a posi-
tive endomysial (EMA) or a positive tissue transglutaminase
(tTG) antibody present. Four patients were assessed for the
presence of HLA DQ2 or DQ8 and had positive results.
One patient (No. 8) had a negative serologic profile but was
both DQ2 and DQ8 positive. All patients had villous atrophy
(subtotal n =3, PVA n=6), at presentation.
Follow-up on gluten-free diet (Table 2)
All patients were advised a gluten-free diet. They were seen
by a dietician experienced in the gluten-free diet and were
referred to a celiac support group. The mean duration of
follow-up was 39 months. Four patients adhered to the diet
strictly; two did not attempt the diet, despite counseling from
the physician, the dietician, and a local support group, while
three had poor compliance, admitting to only intermittent ad-
herence to the diet. Despite poor compliance in three patients,
all those on the diet showed an improvement in symptoms.
Antibodies persisted in three of five patients with available
follow-up antibodies, as did villous atrophy, though it was
less marked in three patients.
Discussion
We identified nine African-American patients with celiac
disease, representing 1.3% of all patients seen at our special-
ist referral center. The demographic profile of the African-
American patients was similar to that of the other patients
seen at our center, in that females predominated, and at least
one associated autoimmune disease was present in a third
of the patients [7]. The majority of the patients presented
with “silent” celiac disease, a trend noted by us and others
[8, 9], and iron deficiency anemia was the most frequent
presentation [10].
Celiac disease is being increasingly diagnosed throughout
the world. While it is recognized throughout Europe and in
countries populated by those of European origin such as
South Africa, Australia, New Zealand, and South America,
it is now being diagnosed in populations where celiac disease
was traditionally not thought to occur. The disease appears
to be common in North Africa [11, 12], as well as in the
Middle East [13, 14] and northern India [15, 16]. Celiac
disease has also been documented in Cuba [17] and in West
Indian children living in England [18].
Celiac disease is considered rare in individuals of central
African descent [19], however, the blood donor screening
study by Not et al., in Baltimore, Maryland, in the United
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Dig Dis Sci (2006)
States, revealed that 1 of 250 African-Americans had pos-
itive endomysial antibodies, a frequency similar to that of
entire group [20]. There have been no systematic screen-
ing studies of celiac disease among African-Americans, so
we are not aware of just how common this disease may
be. African-Americans make up 12% of the U.S. popula-
tion, yet only 1% of the patients with celiac disease that
we have seen were African-Americans. The low prevalence
of disease may be due to a lower frequency of the DQ2 or
DQ8 alleles in the African-American population or it may
be the consequence of other factors such as referral bias or
socioeconomic factors affecting access to health care. We
are not aware of studies of the frequency of DQ2 or DQ8
among African-Americans. Future research should include
studies of HLA DQ2/8 frequency among African-American
patients from different geographic locations in the United
States.
One striking feature observed in our series of patients is
the poor dietary compliance among five patients, with two
not attempting the diet at all. Compliance with a gluten-free
diet is often a problem. In France and Belgium, less than half
of all adult patients studied adhered strictly to the diet for
more than 1 year postdiagnosis [21]. In the United Kingdom
a low compliance has been reported for both teenagers and
adults [22]. Reasons for poor dietary compliance include
expense, availability, and palatability of gluten-free food.
Other factors associated with poor compliance with the diet
include lack of symptoms at diagnosis [23], inadequate initial
dietary counseling [24], inadequate medical or nutritional
follow-up [25], and inaccurate dietary information provided
by resources such as the Internet [26]. Minority populations
have been noted to have compliance difficulties. One study
from the United Kingdom, comparing dietary compliance
between members of a minority population (South Asians)
and Caucasians, all with celiac disease, reported a higher
compliance rate among the Caucasians [27]. South Asians
were less likely to attend dietetic clinics, join a support group,
and be satisfied with information provided by doctors and
dieticians. Compliance with diet in those with celiac disease
should be encouraged because it is associated with a good
quality of life [28].
In conclusion, we have identified celiac disease in only
nine African-Americans. The true prevalence of celiac dis-
ease among this population in the United States needs to
be determined. In addition, when celiac disease is identified
in minority groups, special attention needs to be placed on
factors that increase dietary compliance.
References
1. Alaedini A, Green PH (2005) Narrative review: celiac disease:
understanding a complex autoimmune disorder. Ann Intern Med
142(4):289–298
2. Louka AS, Sollid LM (2003) HLA in coeliac disease: unravel-
ling the complex genetics of a complex disorder. Tissue Antigens
61(2):105–117
3. Green PH, Jabri B (2003) Coeliac disease. Lancet 362(9381):383–
391
4. Fasano A, Berti I, Gerarduzzi T, Not T, Colletti RB, Drago S,
Elitsur Y, Green PH, Guandalini S, Hill ID, Pietzak M, Ventura
A, Thorpe M, Kryszak D, Fornaroli F, Wasserman SS, Murray JA,
Horvath K (2003) Prevalence of celiac disease in at-risk and not-
at-risk groups in the United States: a large multicenter study. Arch
Intern Med 163(3):286–292
5. James SP (2005) National Institutes of Health consensus develop-
ment conference statement on celiac disease, June 28–30, 2004.
Gastroenterology 128(4, Pt 2):S1–S9
6. Green PH, Rostami K, Marsh MN (2005) Diagnosis of coeliac
disease. Best Pract Res Clin Gastroenterol 19(3):389–400
7. Bai D, Brar P, Holleran S, Ramakrishnan R, Green PH (2005) Effect
of gender on the manifestations of celiac disease: evidence for
greater malabsorption in men. Scand J Gastroenterol 40(2):183–
187
8. Lo W, Sano K, Lebwohl B, Diamond B, Green PH (2003) Chang-
ing presentation of adult celiac disease. Dig Dis Sci 48(2):395–
398
9. Murray JA, Van Dyke C, Plevak MF, Dierkhising RA, Zinsmeister
AR, Melton LJ3rd (2003) Trends in the identification and clinical
features of celiac disease in a North American community, 1950–
2001. Clin Gastroenterol Hepatol 1(1):19–27
10. Karnam US, Felder LR, Raskin JB (2004) Prevalence of occult
celiac disease in patients with iron-deficiencyanemia: a prospective
study. South Med J 97(1):30–34
11. Lionetti P, Favilli T, Chiaravalloti G, Ughi C, Maggiore G (1999)
Coeliac disease in Saharawi children in Algerian refugee camps.
Lancet 353(9159):1189–1190
12. al-Tawaty AI, Elbargathy SM (1998) Coeliac disease in north-
eastern Libya. Ann Trop Paediatr 18(1):27–30
13. Tatar G, Elsurer R, Simsek H, Balaban YH, Hascelik G, Ozcebe
OI, Buyukasik Y, Sokmensuer C (2004) Screening of tissue trans-
glutaminase antibody in healthy blood donors for celiac dis-
ease screening in the Turkish population. Dig Dis Sci 49(9):
1479–1484
14. al-Hassany M (1975) Coeliac disease in Iraqi children. J Trop
Pediatr Environ Child Health 21(4):178–179
15. Puri AS, Garg S, Monga R, Tyagi P, Saraswat MK (2004) Spectrum
of atypical celiac disease in North Indian children. Indian Pediatr
41(8):822–827
16. Sood A, Midha V, Sood N, Malhotra V (2003) Adult celiac disease
in northern India. Indian J Gastroenterol 22(4):124–126
17. Sagaro E, Jimenez N (1981) Family studies of coeliac disease in
Cuba. Arch Dis Child 56(2):132–133
18. Hung JC, Phillips AD, Walker-Smith JA (1995) Coeliac disease in
children of West Indian origin. Arch Dis Child 73(2):166–167
19. Ciclitira PJ, King AL, Fraser JS (2001) AGA technical review
on celiac sprue. American Gastroenterological Association. Gas-
troenterology 120(6):1526–1540
20. Not T, Horvath K, Hill ID, Partanen J, Hammed A, Magazzu G,
Fasano A (1998) Celiac disease risk in the USA: high prevalence
of antiendomysium antibodies in healthy blood donors. Scand J
Gastroenterol 33(5):494–498
21. Vahedi K, Mascart F, Mary JY, Laberenne JE, Bouhnik Y, Morin
MC, Ocmant A, Velly C, Colombel JF, Matuchansky C (2003) Re-
liability of antitransglutaminase antibodies as predictors of gluten-
free diet compliance in adult celiac disease. Am J Gastroenterol
98(5):1079–1087
22. Kumar PJ, Walker-Smith J, Milla P, Harris G, Colyer J, Halliday R
(1988) The teenage coeliac: follow up study of 102 patients. Arch
Dis Child 63(8):916–920
Springer

Dig Dis Sci (2006)
23. Fabiani E, Taccari LM, Ratsch IM, Di Giuseppe S, Coppa GV,
Catassi C (2000) Compliance with gluten-free diet in adolescents
with screening-detected celiac disease: a 5-year follow-up study. J
Pediatr 136(6):841–843
24. Ciacci C, Cirillo M, Cavallaro R, Mazzacca G (2002) Long-
term follow-up of celiac adults on gluten-free diet: preva-
lence and correlates of intestinal damage. Digestion 66(3):178–
185
25. Bardella MT, Molteni N, Prampolini L, Giunta AM, Baldassarri
AR, Morganti D, Bianchi PA (1994) Need for follow up in coeliac
disease. Arch Dis Child 70(3):211–213
26. England CY, Nicholls AM (2004) Advice available on the Internet
for people with coeliac disease: an evaluation of the quality of
websites. J Hum Nutr Diet 17(6):547–559
27. Butterworth JR, Banfield LM, Iqbal TH, Cooper BT (2004) Fac-
tors relating to compliance with a gluten-free diet in patients with
coeliac disease: comparison of white Caucasian and South Asian
patients. Clin Nutr Oct 23(5):1127–1134
28. Vilamaa M, Collin P, Huhtala H, Sievanen H, Maki M, Kaukinen
K (2005) Is coeliac disease screening in risk groups justified?
A fourteen-year follow-up with special focus on compliance and
quality of life. Aliment Pharmacol Ther 22(4):317–324
Springer