ISSN 1007-9327 (print)

ISSN 2219-2840 (online)

World Journal of
Gastroenterology
World J Gastroenterol 2014 November 14; 20(42): 15467-15942

Published by Baishideng Publishing Group Inc

S

Contents Weekly Volume 20 Number 42 November 14, 2014

TOPIC HIGHLIGHT 15467 Hepatitis C virus-mediated angiogenesis: Molecular mechanisms and

therapeutic strategies
Hassan M, Selimovic D, El-Khattouti A, Soell M, Ghozlan H, Haikel Y, Abdelkader O,

Megahed M

15476 Diagnostic tests for hepatitis C: Recent trends in electrochemical

immunosensor and genosensor analysis

Uliana CV, Riccardi CS, Yamanaka H

15492 Cirrhotic cardiomyopathy: A cardiologist's perspective

Gassanov N, Caglayan E, Semmo N, Massenkeil G, Er F

15499 Extrahepatic complications to cirrhosis and portal hypertension:

Haemodynamic and homeostatic aspects

Møller S, Henriksen JH, Bendtsen F

15518 Gut-liver axis and probiotics: Their role in non-alcoholic fatty liver disease
Paolella G, Mandato C, Pierri L, Poeta M, Di Stasi M, Vajro P

15532 Liver transplantation and non-alcoholic fatty liver disease

Zezos P, Renner EL

15539 Histopathology of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis

Takahashi Y, Fukusato T

15549 Contrast-enhanced harmonic endoscopic ultrasound imaging: Basic principles,

present situation and future perspectives

Alvarez-Sánchez MV, Napoléon B

15564 Neoadjuvant therapy for pancreas cancer: Past lessons and future therapies
Sutton JM, Abbott DE

15580 Utility of PET/CT in diagnosis, staging, assessment of resectability and

metabolic response of pancreatic cancer

Wang XY, Yang F, Jin C, Fu DL

WJG|www.wjgnet.com I November 14, 2014|Volume 20|Issue 42|

 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

15590 Laparoscopic liver resection for living donation: Where do we stand?

Cauchy F, Schwarz L, Scatton O, Soubrane O

15599 Single port laparoscopy in gastroenterology and hepatology: A ine step

forward
Mittermair C, Schirnhofer J, Brunner E, Pimpl K, Obrist C, Weiss M, Weiss HG

15608 Laparoscopic resection of gastrointestinal neuroendocrine tumors with special

contribution of radionuclide imaging
Shamiyeh A, Gabriel M

15616 Bowel endometriosis: Colorectal surgeon's perspective in a multidisciplinary

surgical team
Wolthuis AM, Meuleman C, Tomassetti C, D'Hooghe T, de Buck van Overstraeten A,

D'Hoore A

15624 Gut microbiota-related complications in cirrhosis

Gómez-Hurtado I, Such J, Sanz Y, Francés R

15632 Modulation of immunity and inlammatory gene expression in the gut, in

inlammatory diseases of the gut and in the liver by probiotics
Plaza-Diaz J, Gomez-Llorente C, Fontana L, Gil A

15650 Interplay between intestinal alkaline phosphatase, diet, gut microbes and
immunity
Estaki M, DeCoffe D, Gibson DL

15657 Enteric microbiota leads to new therapeutic strategies for ulcerative colitis
Chen WX, Ren LH, Shi RH

15664 Wireless capsule endoscopy: Perspectives beyond gastrointestinal bleeding

Redondo-Cerezo E, Sánchez-Capilla AD, De La Torre-Rubio P, De Teresa J

15674 Central pancreatectomy: The Dagradi Serio Iacono operation. Evolution of a

surgical technique from the pioneers to the robotic approach
Iacono C, Ruzzenente A, Bortolasi L, Guglielmi A

REVIEW 15682 Recent studies of 5-luorouracil resistance in pancreatic cancer

Wang WB, Yang Y, Zhao YP, Zhang TP, Liao Q, Shu H

WJG|www.wjgnet.com II November 14, 2014|Volume 20|Issue 42|

 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

ORIGINAL ARTICLE 15691 Mechanism of gastrointestinal abnormal motor activity induced by cisplatin in
conscious dogs
Ando H, Mochiki E, Ohno T, Yanai M, Toyomasu Y, Ogata K, Tabe Y, Aihara R,

Nakabayashi T, Asao T, Kuwano H

15703 Chunggan extract, a traditional herbal formula, ameliorated alcohol-induced

hepatic injury in rat model
Kim HG, Kim JM, Han JM, Lee JS, Choi MK, Lee DS, Park YH, Son CG

15715 Esophageal Helicobacter pylori colonization aggravates esophageal injury

caused by relux
Chu YX, Wang WH, Dai Y, Teng GG, Wang SJ

RESEARCH REPORT 15727 GW4064, a farnesoid X receptor agonist, upregulates adipokine expression in
preadipocytes and HepG2 cells
Xin XM, Zhong MX, Yang GL, Peng Y, Zhang YL, Zhu W

15736 Increased expression and possible role of chitinase 3-like-1 in a

colitis-associated carcinoma model
Ma JY, Li RH, Huang K, Tan G, Li C, Zhi FC

CASE CONTROL STUDY 15745 Could JC virus provoke metastasis in colon cancer?
Sinagra E, Raimondo D, Gallo E, Stella M, Cottone M, Orlando A, Rossi F, Orlando E,

Messina M, Tomasello G, Lo Monte AI, La Rocca E, Rizzo AG

RETROSPECTIVE STUDY 15750 Metformin does not improve survival in patients with hepatocellular
carcinoma
Bhat M, Chaiteerakij R, Harmsen WS, Schleck CD, Yang JD, Giama NH, Therneau TM,

Gores GJ, Roberts LR

CLINICAL TRIALS STUDY 15756 Covert hepatic encephalopathy: Agreement and predictive validity of different
indices
Montagnese S, Balistreri E, Schiff S, De Rui M, Angeli P, Zanus G, Cillo U, Bombonato G,

Bolognesi M, Sacerdoti D, Gatta A, Merkel C, Amodio P

15763 Reduction effect of bacterial counts by preoperative saline lavage of the

stomach in performing laparoscopic and endoscopic cooperative surgery
Mori H, Kobara H, Tsushimi T, Fujihara S, Nishiyama N, Matsunaga T, Ayaki M, Yachida T,

Tani J, Miyoshi H, Morishita A, Masaki T

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 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

15771 Magnifying endoscopy of gastric epithelial dysplasia based on the

morphologic characteristics
Kang HM, Kim GH, Park DY, Cheong HR, Baek DH, Lee BE, Song GA

OBSERVATIONAL STUDY 15780 Autoimmune gastritis presenting as iron deiciency anemia in childhood
Gonçalves C, Oliveira ME, Palha AM, Ferrão A, Morais A, Lopes AI

15787 Higher vitamin D serum concentration increases health related quality of life
in patients with inlammatory bowel diseases
Hlavaty T, Krajcovicova A, Koller T, Toth J, Nevidanska M, Huorka M, Payer J

15797 Immediate detection of endoscopic retrograde cholangiopancreatography-

related periampullary perforation: Fluoroscopy or endoscopy?
Motomura Y, Akahoshi K, Gibo J, Kanayama K, Fukuda S, Hamada S, Otsuka Y,

Kubokawa M, Kajiyama K, Nakamura K

15805 Can composite performance measures predict survival of patients with

colorectal cancer?
Chung KP, Chen LJ, Chang YJ, Chang YJ

15815 Healing time of incision infection after hepatobiliary surgery treated by

needle-free incision suture closure
Ma WJ, Zhou Y, Mao H, Xu RH, Shrestha A, Li FY, Lorance A, Yang Q, Zhang YQ, Jiang T,

Feng H, Zhang W, Cheng NS

PROSPECTIVE STUDY 15820 Adjuvant therapy sparing in rectal cancer achieving complete response after
chemoradiation
García-Albéniz X, Gallego R, Hofheinz RD, Fernández-Esparrach G, Ayuso-Colella JR,

Bombí JA, Conill C, Cuatrecasas M, Delgado S, Ginés A, Miquel R, Pagés M, Pineda E,

Pereira V, Sosa A, Reig O, Victoria I, Feliz L, María de Lacy A, Castells A, Burkholder I,

Hochhaus A, Maurel J

15830 Seroprevalence of celiac disease among United Arab Emirates healthy adult
nationals: A gender disparity
Abu-Zeid YA, Jasem WS, Lebwohl B, Green PH, ElGhazali G

RANDOMIZED 15837 Commercially available probiotic drinks containing Lactobacillus casei

CONTROLLED TRIAL DN-114001 reduce antibiotic-associated diarrhea

Dietrich CG, Kottmann T, Alavi M

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 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

15845 Randomized controlled trial of sodium phosphate tablets vs polyethylene

glycol solution for colonoscopy bowel cleansing
Jung YS, Lee CK, Kim HJ, Eun CS, Han DS, Park DI

RANDOMIZED CLINICAL 15852 Perioperative restricted luid therapy preserves immunological function in
TRIAL patients with colorectal cancer
Jie HY, Ye JL, Zhou HH, Li YX

SYSTEMATIC REVIEWS 15860 Spontaneous and antiviral-induced cutaneous lesions in chronic hepatitis B
virus infection
Grigorescu I, Dumitrascu DL

META-ANALYSIS 15867 Totally laparoscopic gastrectomy for gastric cancer: A systematic review and
meta-analysis of outcomes compared with open surgery
Chen K, Pan Y, Cai JQ, Xu XW, Wu D, Mou YP

15879 Dairy product consumption and gastric cancer risk: A meta-analysis

Sun Y, Lin LJ, Sang LX, Dai C, Jiang M, Zheng CQ

15899 Interleukin-17 SNPs and serum levels increase ulcerative colitis risk: A meta-
analysis
Li J, Tian H, Jiang HJ, Han B

CASE REPORT 15910 Embolization of splenorenal shunt associated to portal vein thrombosis and
hepatic encephalopathy
Franzoni LC, Carvalho FC, Garzon RGA, Yamashiro FS, Augusti L, Santos LAA,

Dorna MS, Baima JP, Lima TB, Caramori CA, Silva GF, Romeiro FG

15916 Interesting rendezvous location in a liver transplantation patient with

anastomosis stricture
Odemis B, Oztas E, Yurdakul M, Torun S, Suna N, Kayacetin E

15920 Amenorrhea as a rare drug-related adverse event associated with everolimus

for pancreatic neuroendocrine tumors
Kawaguchi Y, Maruno A, Kawashima Y, Ito H, Ogawa M, Mine T

15925 Intraductal papillary neoplasm of the bile duct developing in a patient with
primary sclerosing cholangitis: A case report
Hachiya H, Kita J, Shiraki T, Iso Y, Shimoda M, Kubota K

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 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

15931 Delayed hypersensitivity reaction resulting in maculopapular-type eruption

due to entecavir in the treatment of chronic hepatitis B
Kim JT, Jeong HW, Choi KH, Yoon TY, Sung N, Choi YK, Kim EH, Chai HB

15937 Endoscopic variceal ligation caused massive bleeding due to laceration of an

esophageal varicose vein with tissue glue emboli
Wei XQ, Gu HY, Wu ZE, Miao HB, Wang PQ, Wen ZF, Wu B

LETTERS TO THE EDITOR 15941 Clinical importance of serum procalcitonin in ulcerative colitis patients
Karagoz E, Tanoglu A

WJG|www.wjgnet.com VI November 14, 2014|Volume 20|Issue 42|

 World Journal of Gastroenterology
Contents
Volume 20 Number 42 November 14, 2014

APPENDIX I-VI Instructions to authors

ABOUT COVER Editorial Board Member of World Journal of Gastroenterology , C. Mel Wilcox,
MD, Doctor, Professor, Medicine, Division of Gastroenterology and Hepatology ,
University of Alabama at Birmingham, Birmingham, AL 35294, United States

AIMS AND SCOPE World Journal of Gastroenterology (World J Gastroenterol, WJG, print ISSN 1007-9327, online
ISSN 2219-2840, DOI: 10.3748) is a peer-reviewed open access journal. WJG was estab-
lished on October 1, 1995. It is published weekly on the 7th, 14th, 21st, and 28th each month.
The WJG Editorial Board consists of 1362 experts in gastroenterology and hepatology
from 67 countries.
The primary task of WJG is to rapidly publish high-quality original articles, reviews,
and commentaries in the ields of gastroenterology, hepatology, gastrointestinal endos-
copy, gastrointestinal surgery, hepatobiliary surgery, gastrointestinal oncology, gastroin-
testinal radiation oncology, gastrointestinal imaging, gastrointestinal interventional ther-
apy, gastrointestinal infectious diseases, gastrointestinal pharmacology, gastrointestinal
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therapeutics. WJG is dedicated to become an inluential and prestigious journal in gas-
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Citation Index Expanded (also known as SciSearch®), Journal Citation Reports®, Index Medi-
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FLYLEAF I-IX Editorial Board

Responsible Assistant Editor: Xiang Li Responsible Science Editor: Ya-Juan Ma

EDITORS FOR Responsible Electronic Editor: Shuai Ma Prooing Editorial Ofice Director: Xiu-Xia Song
THIS ISSUE Prooing Editor-in-Chief: Lian-Sheng Ma

NAME OF JOURNAL Andrzej S Tarnawski, MD, PhD, DSc (Med), Pro-
World Journal of Gastroenterology
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ISSN 1007-9327 (print)
ISSN 2219-2840 (online)
LAUNCH DATE
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gery, Fundacion Jimenez Diaz University Hospital,
Madrid 28040, Spain
Saleh A Naser, PhD, Professor, Burnett School of
Biomedical Sciences, College of Medicine, University
of Central Florida, Orlando, FL 32816, United States
Stephen C Strom, PhD, Professor, Department of
Laboratory Medicine, Division of Pathology, Karo-
linska Institutet, Stockholm 141-86, Sweden
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 Submit a Manuscript: http://www.wjgnet.com/esps/ World J Gastroenterol 2014 November 14; 20(42): 15830-15836
Help Desk: http://www.wjgnet.com/esps/helpdesk.aspx ISSN 1007-9327 (print) ISSN 2219-2840 (online)
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PROSPECTIVE STUDY

Seroprevalence of celiac disease among United Arab

Emirates healthy adult nationals: A gender disparity

Yousif A Abu-Zeid, Waheeba S Jasem, Benjamin Lebwohl, Peter H Green, Gehad ElGhazali

Yousif A Abu-Zeid, Department of Biology, College of Sci-
ence, United Arab Emirates University, Al Ain, Abu Dhabi AE-
AZ, United Arab Emirates
Waheeba S Jasem, Ambulatory Healthcare Services, Abu
Dhabi Health Services Company, Abu Dhabi AE-AZ, United
Arab Emirates
Benjamin Lebwohl, Celiac Disease Center at Columbia Uni-
versity, New York, NY 10032, United States
Peter H Green, Department of Medicine, Columbia University
College of Physicians and Surgeons, New York, NY 10032,
United States
Gehad ElGhazali, Mafraq Hospital and Sheikh Khalifa Medi-
cal City, Abu Dhabi AE-AZ, United Arab Emirates
Author contributions: Abu-Zeid YA designed the study, per-
formed the statistical analyses, interpreted the data and wrote
the manuscript; Jasem WS did the sampling, data collection
and the laboratory analysis and contributed in data analysis and
writing; Green PH critically revised the article and contributed
in interpretation of data; Lebwohl B reviewed the article and
critically evaluated the employed statistical methods; ElGhazali
G contributed in the design and provided critical insights in the
writing of the manuscript.
Supported by Research Affairs at the United Arab Emirates
University, grant No. 03-04-2-11/08
Correspondence to: Yousif A Abu-Zeid, Associate Professor
of Immunology, Department of Biology, College of Science,
United Arab Emirates University, P O Box 15551 Al Ain, Abu
Dhabi AE-AZ, United Arab Emirates. youssefa@uaeu.ac.ae
Telephone: +971-3-7136517 Fax: +971-3-7134927
Received: February 24, 2014 Revised: May 10, 2014
Accepted: May 25, 2014
Published online: November 14, 2014
among those who went to Al Ain Hospital to under-
take the prenuptial examination. Test for anti-tissue
transglutaminase (tTG) IgA antibodies was used for CD
diagnosis. Subjects with positive results in the anti tTG
antibodies assay were also tested for anti-endomysial
(EMA) IgA antibodies. A structured interview was used
to collect basic demographic and clinical recall data
including: information on name, contact address, age,
gender, education status, previous diagnosis of CD,
st
diagnosis of CD in 1 degree relatives and history of
“chronic diarrhea, anemia, headache, hepatitis, diabe-
tes, tumor, and thyroid disorder”.
RESULTS: Fourteen blood samples (1.17%; 14/1197)
were seropositive for CD. The latent CD seropositive pa-
tients were 13 women and 1 man and therefore the se-
roprevalence of CD was 1:86 (14/1197) for adult Emira-
tis: 1:44 (13/573) for women and 1:624 for men. Binary
logistic regression revealed that history of chronic ane-
mia (crude OR = 7.09; 95%CI: 2.32-21.61; P = 0.003)
and being a woman (OR = 14.46; 95%CI: 1.89-110.91;
P = 0.001) were associated with CD seropositivity.
Whereas, the thyroid disorder showed a positive as-
sociation with CD seropositivity that approach statisti-
cal signiicance (OR = 11.30; 95%CI: 1.32-96.95; P =
0.09) and therefore was included in the multiple logistic
regression analysis, which showed that CD seropositivity
is independently associated only with history of chronic
anemia (OR = 4.58; 95%CI: 1.45-14.48; P = 0.01) and
being a woman person (OR = 10.47; 95%CI: 1.33-82.14;
P = 0.026).

CONCLUSION: Compared to men the CD seropreva-

Abstract lence among women was remarkably higher. The CD
AIM: To determine celiac disease (CD) prevalence and association with women and chronic anemia is of im-
associated manifestations or risk factors in healthy portance from a public health perspective.
adult Emiratis.
© 2014 Baishideng Publishing Group Inc. All rights reserved.
METHODS: It is a cross-sectional prospective study,
recruiting 1197 (573 women and 624 men) healthy Key words: Celiac disease; Epidemiology; Serology;
Emiratis between September 2007 and April 2008 Prevalence; Gender; United Arab Emirates

WJG|www.wjgnet.com 15830 November 14, 2014|Volume 20|Issue 42|

 Abu-Zeid YA et al . Seroprevalence of CD among Emiratis

Core tip: Celiac disease (CD) prevalence is unknown in anti-endomysial antibody (EMA) test[7]. The tTG test is
United Arab Emirates. Screening for CD among adult based on ELISA which is from a cost and time perspec-
Emiratis was done by using anti TtG antibodies and tive superior to EMA test[8].
anti-endomysial antibodies (EMA) confirmed those CD affects all ages and races worldwide and its
positive. A structured interview was used to collect prevalence varies from 0.5%-3%. Initially the disease was
demographic data and clinical history. Eleven hundred thought to be largely conined to northern Europe and
ninety seven subjects were included in the study; Australasia and not common in North America and the
the seroprevalence was 1:86 for all adults; 1:44 for Middle East, but CD is now known to be prevalent in all
women; 1:624 for men. Chronic anemia and being a those regions[9]. The published prevalence for CD varies
woman independently associated signiicantly with CD between 1:150-1:300 in UK and 1:80-1:122 in Ireland[4],
seropositivity. To our knowledge, this is the irst study while it was 1:200 among Italian school children which
on CD prevalence among Emiratis; reporting the high- is much more than earlier prevalence based on clinical
est gender difference in CD seroprevalence worldwide. findings[10]. Hotmeier and Caspary reported that; for
each diagnosed CD patient there are approximately 7-10
undiagnosed patients[11]. The above-mentioned indings
Abu-Zeid YA, Jasem WS, Lebwohl B, Green PH, ElGhazali G. suggested an analogy to what is called CD iceberg. A
Seroprevalence of celiac disease among United Arab Emirates study reported a prevalence of 1:96 in north India and
healthy adult nationals: A gender disparity. World J Gastroenterol
the study concluded that CD is more common than ex-
2014; 20(42): 15830-15836 Available from: URL: http://www.
pected[12], while the prevalence was 1:50 in Shiraz, Iran[13].
wjgnet.com/1007-9327/full/v20/i42/15830.htm DOI: http://
There are few reports from the Middle East and the
dx.doi.org/10.3748/wjg.v20.i42.15830
Gulf on the prevalence of CD, and to our knowledge no
study exists on the prevalence of CD in UAE nationals.
Therefore, this study aims at estimating the prevalence
of CD among healthy adult Emiratis.
INTRODUCTION
Celiac disease (CD) is a chronic inlammatory condition
in the small intestine, as a response to eating gluten in MATERIALS AND METHODS
genetically susceptible individuals. Many symptoms are Study design
associated with CD including chronic diarrhea, anemia, This study was a prospective cross sectional concerning
and iron/vitamins deficiencies; but what is called as CD prevalence in Al Ain city among adult Emiratis who
silent or latent CD is also common. Therefore, CD is were undergoing the tests of prenuptial examination.
considered as one of the less diagnosed diseases and af- Sample size calculation was based on an estimated CD
fected persons are mostly unaware of having the disease. prevalence of 1%, and a lower 95% conidence limit of
Moreover, diagnosis of CD often is required for extra- 0.58%. The estimated minimum number of subjects to
intestinal manifestations, including psychiatric[1], skin[2], be included was 1150; and was adjusted to around 1200
and autoimmune diseases[3]. Those who remain undi- to include about 4% more than the required number.
agnosed are at risk of many long-term complications
including but not limited to infertility, osteoporosis, and Study area
lymphoma. The basis of treatment of CD is abiding to Al Ain is the second largest city in the Emirate of Abu
a diet free of gluten[4]. Therefore, timely diagnosis is es- Dhabi, it is located inland on the country’s eastern bor-
sential not just to enable proper treatment of symptoms der with Oman about 165 km from Abu Dhabi and
but also to avoid possible complications[5]. about 140 km from Dubai. The area of this city covers
The early epidemiological studies of CD in Europe over 1.17 million hectares mostly of sand dunes, the
were based on clinical presentation followed by intesti- temperature during the year ranges between 10 ℃ up
nal biopsies led to undervaluing the prevalence of the to 48 ℃. Al Ain city is the country hub for learning,
disease. Development of highly sensitive and specific harboring the UAE University and is famous as a tourist
serological tests on which subsequent epidemiological destination. The city is divided into 35 districts with a
studies were based upon, resulted in reporting higher total population of 0.63 million, 30.8% of whom were
CD prevalence and revealing many clinical features of Emiratis (estimation of mid 2012).
the disease[6]. Although intestinal biopsy is considered as Al Ain Hospital is one of two major governmental
the gold standard in diagnosis, serological tests are need- hospitals in Al Ain city and at the time of sampling, it
ed to screen for people who need the biopsy. Serology is was the only place in the city performing the prenuptial
also useful in distinguishing between the disease and the examination tests for UAE nationals.
other causes of intestinal villi atrophy. The recommend-
ed test for CD screening is anti-tissue transglutaminase Study population and blood sampling
(tTG) antibodies. The test detects both IgA and IgG The study population is Emiratis who visited Al Ain
antibodies. The sensitivity of anti tTG antibodies test is Hospital for the prenuptial examination between Sep-
more than 90% but the speciicity is less compared with tember 2007 and April 2008. The inclusion criteria were:

WJG|www.wjgnet.com 15831 November 14, 2014|Volume 20|Issue 42|

 Abu-Zeid YA et al . Seroprevalence of CD among Emiratis
being an adult (16 years of age or more), not previously
diagnosed as a CD patient and willing to participate in
the study. The exclusion criteria were: Emiratis less than
16 years of age, Emiratis who were diagnosed as hav-
ing CD, Emiratis with serological equivocal results for
CD diagnosis and all non-Emiratis. Blood sampling was
carried out at Al Ain Hospital; 5 mL was obtained from
each subject. Sera were separated on the same day and
stored at -80 ℃. Sera were tested for anti-tissue transglu-
taminase (tTG) IgA antibodies, total IgA measurement
was carried out for sera which were negative in tTG IgA.
Seropositive sera in anti tTG IgA antibodies were tested
for anti EMA IgA antibodies and the following criteria
were used to deine a serum as CD positive: positive in
both anti tTG IgA and anti EMA IgA antibody tests;
or in sera with total IgA deiciency, positive in both anti
tTG IgG and anti EMA IgG antibodies. The criteria for
a serum sample to be designated as CD seronegative
were if suficient in total IgA to be negative in anti tTG
IgA, or if deficient in total IgA to be negative in anti
tTG IgG.
Demographic and clinical recall data
For each subject a structured interview was done and
included information on name, contact address, age,
gender, education status, knowledge about CD, if he/she
was previously diagnosed as CD patient, diagnosis of
CD in 1st degree relatives, history of: chronic diarrhea,
anemia, headache, diabetes, tumor, hepatitis and thyroid
disorder.
Anti tTG IgA antibodies
Anti tTG IgA antibodies were measured using an ELISA
method based on human recombinant transglutaminase
(IBL International, Hamburg, Germany). The test was
carried out according to the manufacturer instruction.
Interpreting the results for tTG IgA qualitatively was
based on OD cutoff ratio values as described in the
footnote of Table 1.
Total human serum IgA
Quantitative determination of human IgA in serum was
carried out using an ELISA method. The test was car-
ried out according to the manufacturer recommendation
(XEMA, Medica Co., Moscow, Russia). Sera with IgA
level < 0.05 g/L are considered IgA deicient.
Anti-endomysial IgA antibody
The test is based on indirect immunoluorescence assay
for semi-quantitative assessment of endomysial antibod-
ies. The test was carried out according to the manufac-
turer instruction (Immco diagnostics, New York, United
States).
Ethical aspects
Al Ain Medical District Human Research Ethics Com-
mittee approved the ethical application in July 2007.
Upon fully explaining the objectives and the expected
WJG|www.wjgnet.com 15832
beneits from participating in the study, each subject in-
cluded in the study gave his/her consent for the blood
sample and to provide the required information for the
structured interview.
Statistical analysis
Data analysis was carried out on personal computer using
SPSS (version 15, SPSS Inc., Chicago, IL, United States).
The difference in age between “men and women” and
between “diabetics and non-diabetics” was assessed by
the student’s t-test. The linear by linear (for ordinal vari-
ables), the Pearson χ 2 test and the Fisher exact test were
used to compare dichotomous nominal variables between
women and men. Binary and multiple logistic regres-
sions were used to analyze the association between the
variables obtained from the structured interview with CD
serology.
RESULTS
Study population attributes
Fourteen hundred and thirty persons were requested to
participate in the study and 1211 (84.7%) approved. Four-
teen were excluded due to grossly hemolyzed samples (11)
or equivocal CD serology (3). Therefore, 1197 Emiratis
(573 women and 624 men) were included in the study.
The age range was 16-70 years with a mean ± SD of
24.87 ± 6.35. The mean age for men 26.36 ± 7.413 was
higher (P < 0.001) compared to women 23.247 ± 4.427.
The distribution according to age of the study popula-
tion into 6 groups (16-20, 21-25, 26-30, 31-35, 36-40 and
> 40 years of age) and according to gender, showed that
most men and women (87.4%) were between 16 and 30
years and there were more men in all the age groups ex-
cept in the age group 16-20 years (data not shown).
Serological data
All sera tested for total IgA antibodies were IgA sufi-
cient (data not shown). Fourteen blood samples (1.17%;
14/1197) were seropositive for anti tTG IgA and anti
EMA IgA and fulfilled the CD seropositive definition
and therefore their donors were considered serologically
as CD patients (Table 1). The 14 seropositive patients
were 13 women and 1 man and therefore the seropreva-
lence of CD was 1:86 (14/1197) for adult Emiratis: 1:44
(13/573) for women and 1: 624 for men.
Association of variables with CD serology
In order to test for any association between variables
obtained through the structured interview and CD serol-
ogy, results of binary logistic regression analyses are pre-
sented in Table 2. The History of chronic anemia (OR =
7.09, 95%CI: 2.32-21.61, P = 0.003) and being a woman
(OR = 14.46; 95%CI: 1.89-110.91, P < 0.001) were as-
sociated with CD seropositivity. Whereas, the thyroid
disorder showed a positive association with CD serol-
ogy that approach statistical signiicance (OR = 11.30;
95%CI: 1.32-96.95, P = 0.09) and therefore was included
November 14, 2014|Volume 20|Issue 42|
 Abu-Zeid YA et al . Seroprevalence of CD among Emiratis

Table 1 Demographic, serology and clinical history data in In the Middle East, there are few studies on the
adult Emiratis diagnosed serologically with celiac disease prevalence of CD in the general population, most of the
studies focus on populations at risk, such as those hav-
Subject Gender Age tTG IgA
1
EMA IgA Clinical history ing autoimmune disease e.g., diabetes mellitus type Ⅰ and
1 M 24 7.6 +++ a autoimmune thyroiditis[15]. Generally CD prevalence is
2 F 28 1.27 + t undervalued and its clinical features have not been fully
3
4
F
F
22
24
2.42
3.6
+++
++
n
n
determined due to small sample size, selection bias,
5 F 23 8.25 +++ a limited knowledge about CD and insufficient research
6 F 20 3.15 ++ n funds [6,16]. In Libya, as an example of a Middle East
7 F 20 6.6 +++ n country, CD prevalence among school students was (1:41)
8 F 22 4.87 +++ a
much higher than those reported in Europe or North
9 F 25 9.1 +++ n
10 F 18 9.89 + a America [17]. In Saudi Arabia, CD prevalence among
11 F 24 9.13 +++ n healthy adolescents was (1:45) for both sexes; (1:33) for
12 F 27 7.6 + n females and (1:68) for males. The investigators conclud-
13 F 24 4.25 +++ n ed that the CD prevalence in their study may be among
14 F 22 6.78 ++ a
the highest worldwide[18].
1
Using qualitative evaluation ratio for tissue transglutaminase (tTG) IgA To our knowledge, this is the irst study on CD prev-
the cutoff for the positive > 1.2, equivocal 0.85-1.2, and negative subjects < alence in UAE. This study is prospective cross-sectional
0.85. a: Anemia; t: Thyroid disorder; n: No complain; M: Male; F: Female; concerning CD prevalence among adult UAE nationals
EMA: Anti-endomysial antibodies.
who were in the course of undertaking the prenuptial
examination. The prenuptial tests include screening for
in the multiple logistic regression analysis. Using mul- HIV, hepatitis B, syphilis and anemia. The only targeted
tiple logistic regressions (for the statistically signiicant population was men and women who were apparently
variables in binary logistic regression in addition to the healthy at time of recruitment. Choosing this population
variable thyroid disorder) revealed that only history of is satisfactory because the aim of the study is to detect
chronic anemia and being a woman were independently silent/latent CD in healthy adult UAE nationals. Further-
associated with CD serology (Table 2). Five out of the more, from a logistic point of view, those Emiratis were
14 CD patients reported a history of chronic anemia in the process of giving blood for the prenuptial tests,
and one patient reported a thyroid disorder. None of the therefore, there was no need for much effort to persuade
remaining eight CD patients complained from diarrhea them to participate in the study. Moreover, the choice of
or any symptoms or signs of any disease (Table 1). the study population may be reason for the nearly equal
gender ratio in this study. The slight men majority in our
CD serology and structural interview variables in men study can be explained in part that women refused more
and women to participate in the study compared to men; also, some
The distribution of gender in relation to CD serology men came alone because their intention was to marry
and the structural interview data was analyzed. Most foreigners and the prenuptial tests for foreigners is not
of the CD seropositive were women (P = 0.0006) and carried at the test center at Al Ain Hospital.
most of the anemic persons were women (P < 0.001), In this study, the overall prevalence of CD is 1:86
whereas, most of the diabetics were men (P < 0.005). among UAE nationals of Al Ain city is higher than the
The difference in diabetes between the two sexes is most CD prevalence in the general population of Western
likely due to age. Diabetics (mostly men) had signifi- Europe; in Denmark (1:330), Finland (1:130), Germany
cantly higher (P < 0.001) age (35.76 ± 12.454) than non- (1:500), Italy (1:184) and Netherland (1:198)[8]. The CD
diabetics (24.67 ± 6.028). No other signiicant difference high prevalence among healthy adult Emiratis emphasize
in the studied variables was found between the two sexes the CD iceberg terminology (that refers to many undiag-
(Table 3). nosed CD patients in the general population).
Chronic anemia is a major manifestation of CD; it
was shown to be associated with seropositivity for CD.
DISCUSSION Five seropositive subjects have a history of chronic ane-
The epidemiological pattern of CD in the world has mia. Several studies reported anemia as the most com-
changed due to many factors e.g., more awareness to the mon sign of CD among adults. In a study of 200 CD
wide variation in the clinical presentations of CD and patients, 5% of them were anemic due to nutritional de-
discovering new serological tests which are simpler, in- iciency[19]. Thus, it is suggested that all patients who have
expensive and led to increase in the power of detection anemia or iron deficiency should be examined for CD.
and hence increase in the reported prevalence of CD[6]. Iron deficiency usually affects 2%-5% of adolescents,
The new serological tests have helped in diagnosis of CD adult girls and women[20]. Most of the anemic subjects in
and reporting a higher disease prevalence (1:133) in some this study were women, which is in agreement with the
countries[14]. However, the actual prevalence of CD is still fact that anemia is more common in women compared
not clear in spite of these efforts to detect the disease. with men.

WJG|www.wjgnet.com 15833 November 14, 2014|Volume 20|Issue 42|

 Abu-Zeid YA et al . Seroprevalence of CD among Emiratis

Table 2 Distribution and association of variables according to celiac disease serology in Emiratis distribution n (%)

1 2
Variable CD-ve CD+ve OR (95%CI) OR (95%CI)
[P value] [P value]
CD in family No3 1181 (99.8) 14 (100) 0.998 (0.99-1.00) -
Yes 2 (0.2) 0 (0.0) [0.828]
Anemia No3 1097 (92.7) 9 (64.3) 7.09 (2.32-21.61) 4.58 (1.45-14.48)
Yes 86 (7.3) 5 (35.7) [0.003] [0.01]
Headache No3 1171 (99.0) 14 (100) 0.997 (0.99-1.00) -
Yes 12 (1.0) 0 (0.0) [0.594]
Diarrhea No3 1178 (99.6) 14 (100) 0.99 (0.98-1.00) -
Yes 5 (0.4) 0 (0.0) [0.731]
Diabetes No3 1162 (98.2) 14 (100) 0.996 (0.99-1.00) -
Yes 21 (1.7) 0 (0.0) [0.480]
Tumor No3 1182 (99.9) 14 (100) 0.98 (0.97-0.99) -
Yes 1 (0.1) 0 (0.0) [0.878]
Thyroid disorder No3 1175 (99.3) 13 (92.9) 11.30 (1.32-96.95) -
Yes 8 (0.7) 1 (7.1) [0.09]
Hepatitis No3 1172 (99.1) 14 (100) 0.998 (0.99-1.00) -
Yes 11 (0.9) 0 (0.0) [0.610]
Sex Man3 623 (52.7) 1 (7.1) 14.46 (1.89-110.91) 10.47 (1.33-82.14)
Woman 560 (47.3) 13 (92.9) [0.001] [0.026]

1
Crude odd ratio; 2Adjusted odd ratio; 3Reference group. CD: Celiac disease.

Table 3 Distribution of celiac disease serology and structural interview data in adult Emiratis men and women distribution n (%)

Parameter Frequency Men Women P value

CD Serology -ve 1183 (98.8) 623 (99.8) 560 (97.7) 0.00061
+ve 14 (1.2) 1 (0.2) 13 (2.3)
CD in family No 1195 (99.8) 624 (100) 571 (99.7) 0.2291
Yes 2 (0.2) 0 (0.0) 2 (0.3)
Anemia No 1106 (92.4) 601 (96.3) 505 (88.1) < 0.0012
Yes 91 (7.6) 23 (3.7) 68 (11.9)
Headache No 1185 (99.0) 618 (99.0) 567 (99.0) 1.0002
Yes 12 (1.0) 6 (1.0) 6 (1.0)
Diarrhea No 1192 (99.6) 621 (99.5) 571 (99.7) 1.01
Yes 5 (4.4) 3 (0.5) 2 (0.3)
Diabetes No 1176 (98.2) 606 (97.1) 570 (99.5) < 0.0052
Yes 21 (1.8) 18 (2.9) 3 (0.5)
Tumor No 1196 (99.9) 623 (99.8) 573 (100) 1.01
Yes 1 (0.1) 1 (0.2) 0 (0.0)
Thyroid disorder No 1188 (99.2) 622 (99.7) 566 (98.8) 0.0961
Yes 9 (0.8) 2 (0.3) 7 (1.2)
Hepatitis No 1186 (99.1) 617 (98.9) 569 (99.3) 0.6422
Yes 11 (0.9) 7 (1.1) 4 (0.7)

1
Fisher's Exact Test; 2χ 2 with continuity correction. CD: Celiac disease.

The women-to-men ratio of those who are sero-
positive for CD in this study (13:1) is much higher than
that reported in Finland (11:21)[21], Sweden (7:3)[22], and
Argentina (2:1)[23] but comparable to the ratio reported
from eastern Switzerland (10:1)[24]. In this study, the se-
roprevalence of CD in Emirati women was considerably
higher compared with men; this dichotomy in gender-
related CD prevalence was more remarkable compared
to studies from other countries. Most of our subjects
(87.4%) were in the young age category (16-30) which
agrees with the conclusion of Dixit and coworkers[25]
that “gender disparity was most marked in young adults
between the ages 18 and 29 years of whom only 18% of
the patients diagnosed with CD were males”. There are
unknown factors that contribute to the high prevalence
of latent CD among women; two obvious factors are
the amount of gluten consumption and the extent of
intestinal damage[26]. There is no study comparing the
consumption of wheat in women and men in UAE and
this study didn’t include this variable in the structured in-
terview. There are indications that autoimmune diseases
have common genetic risk factors and many of these
are gender-predisposed[27]. Possibly women are geneti-
cally more susceptible to environmental exposure fac-
tors that affect the immunological processes leading to
CD. Smoking may be protective against CD and in UAE
men constitute the bulk of smokers[28,29], also some en-
doscopy-conirmed CD patients who were smokers had
negative CD serology[30]. Therefore, smoking may partly
explain why in this study the prevalence of celiac disease

WJG|www.wjgnet.com 15834 November 14, 2014|Volume 20|Issue 42|


in men was much lower compared with women. In sup-
port of this interpretation a retrospective study, from
Sheikh Khalifa Medical City, Abu Dhabi, UAE, reported
that only 48% of CD children patients were females[31].
Therefore, on the assumption that those children were
nonsmokers at the time of study, it is imperative to in-
terpret the difference in CD prevalence between women
and men in this study on epigenetic or environmental
factors e.g., smoking rather than on inherent genetic sus-
ceptibility between the genders. On the other hand, the
gender discrepancy may be related to the failure of the
serological test to detect the disease in young men due
to hormonal or environmental factors. Therefore, one
may suggest that for young men with clinical symptoms
suggestive of the disease, endoscopy and biopsy should
be the basis for diagnosis with less emphasis on the se-
rological tests.
There are some limitations in this study; most of the
study population were at the age range of 16-30 years;
therefore, compared to the general population older age
groups were less represented. The diagnosis relied only
on highly speciic serological tests but was not proved
by biopsy. There was no information on the diet of the
sampled population, but it is well known that due to the
modern lifestyle, the consumption of fast food (wheat-
based diets) among Emiratis has increased considerably
during the last decades[32]. Finally, the study includes only
the major risk factors for CD and does not include fac-
tors that may be protective against CD such as smoking.
In conclusion, as anemia is a major manifestation rath-
er than a risk factor of CD, gender is the most important
risk factor associated with CD seropositivity in this study,
with much higher prevalence in women (1:44) compared
with men (1:624). These indings are of importance from
a public health perspective and should be conveyed to the
health authority for raising the awareness of the disease
among health workers and the general population. Health
workers should know that there are many undiagnosed
CD women patients among UAE nationals. Therefore,
they should refer any patient with vague symptoms, com-
plications or signs suggestive of CD to the healthcare
specialists for further examination. Among the measures
to diagnose latent/silent or unrecognized CD in the gen-
eral population is the screening of all women who suffer
from chronic anemia.
ACKNOWLEDGMENTS
Most of this study is from the M. Sc. thesis of WSJ. We
express our sincere appreciation to the Research Affairs
at the United Arab Emirates University, for the inancial
support. We express our gratitude to the staff at Al Ain
Hospital; sampling was not possible without their help.
Thank to Prof. Miodrag Lukic at College of Medicine
and Health Sciences (CMHS), UAE for permission to
carry out some of the laboratory analyses at CMHS. Fi-
nally, our sincere thanks extend to all subjects who par-
ticipated in this study.
WJG|www.wjgnet.com
Abu-Zeid YA et al . Seroprevalence of CD among Emiratis
COMMENTS
COMMENTS
Background
Celiac disease (CD) can be easily mistaken for many other diseases due to its
vast clinical symptoms and presentations. CD is a chronic inlammatory condi-
tion in the small intestine, in response to eating gluten in genetically susceptible
individuals. It is a lifelong disease and the only treatment up-to-date is the
complete abiding to a gluten-free diet. The highest prevalence of the disease
worldwide has been reported in the Middle East. The aim of this study is to de-
termine CD prevalence and associated manifestations or risk factors in healthy
adult Emiratis.
Research frontiers
The lack of information on the prevalence of the disease from many countries is
hindering the effort to draw a worldwide prevalence map of the disease. There
is no previous report on the prevalence of CD in the United Arab Emirates.
Innovations and breakthroughs
The authors have reported for the irst time the prevalence of CD among Emi-
ratis. Furthermore, from public health perspective our indings of the highest
worldwide gender disparity in the CD prevalence has great impact, the preva-
lence in women was 1:44 compared with 1:624 in men. The study points to the
importance of considering CD as an etiological agent particularly in Emiratis
women who suffer from chronic anemia.
Applications
The results suggest that CD is common among young Emiratis women in Al
Ain; therefore, further studies on CD in UAE are warranted to determine the
actual CD prevalence in UAE.
Peer review
CD prevalence is unknown in UAE and Screening for CD is very important. This
is the irst study on CD prevalence among Emiratis and it reports the highest
gender difference in CD seroprevalence worldwide.
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S- Editor: Ding Y L- Editor: A E- Editor: Liu XM
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