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a
Institute of Endocrinology and Diabetes, The Children’s Hospital at Westmead, Sydney, Australia; bDiscipline of Pediatrics and Child Health, University of Sydney, Sydney, Australia; cJohn Hunter
Hospital, Newcastle, Australia; dRoyal Prince Alfred Hospital and Charles Perkins Centre, Sydney Medical School, University of Sydney, Sydney, Australia; and eSchool of Women’s and Child’s
Health, University of New South Wales, Sydney, Australia
Ms Pham-Short designed the study, carried out the initial analyses, drafted the initial manuscript, and reviewed and revised the manuscript; Drs Donaghue, Ambler,
Twigg, and Craig designed the study and reviewed and revised the manuscript; Ms Phelan designed the study, carried out the initial analyses, and reviewed and revised
the manuscript; and all authors approved the final manuscript as submitted.
www.pediatrics.org/cgi/doi/10.1542/peds.2014-2883
DOI: 10.1542/peds.2014-2883
Accepted for publication Apr 2, 2015
Address correspondence to Maria E. Craig, MBBS, PhD, FRACP, MMed(ClinEpi), Institute of Endocrinology and Diabetes, The Children’s Hospital at Westmead, Locked Bag
4001, Westmead, NSW 2145, Australia. E-mail: m.craig@unsw.edu.au or maria.craig@health.nsw.gov.au
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2015 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: No external funding.
POTENTIAL CONFLICT OF INTEREST: Professor Donaghue has consulted for Eli Lilly, received grants from Novo Nordisk and Medtronic, and received payments for lectures
from Eli Lilly, Novo Nordisk, and Sanofi Aventis; the other authors have indicated they have no potential conflicts of interest to disclose.
REVIEW ARTICLE Downloaded from http://pediatrics.aappublications.org/ by guest on February 12, 2018Volume 136, number 1, July 2015
PEDIATRICS
The association between type 1 increased morbidity, there are no individuals with T1D, and no reports
diabetes (T1D) and celiac disease systematic reviews examining the of screening frequency. The diagnosis
(CD) is well documented in young incidence of CD or optimal screening of T1D was based American Diabetes
people, although reported rates vary. frequency for CD in T1D. Association criteria,21 and CD was
Prevalence rates from both cross- Contemporary guidelines for T1D confirmed by small bowel biopsy.
sectional and longitudinal studies recommend screening by
range from 1.6% to 16.4% measurement of tissue Data Sources and Searches
worldwide,1–5 with the majority of transglutaminase (TTG) or anti- Two reviewers (A.P.-S. and H.P.)
studies only including children and endomysial antibodies (EMAs).18–20 independently searched Medline,
adolescents. In contrast, CD Recommendations for screening Embase, and the Cochrane Library
prevalence is 0.3% to 1.0% in the frequency are variable and not from 1946 to November 30, 2014, for
general population of all ages.6 evidence based. The International studies of celiac autoimmunity and
A greater risk is conferred by female Society for Pediatric and Adolescent biopsy-proven CD in people with T1D.
gender,1,7 younger age, and, in type 1 Diabetes recommends screening at Search terms were as follows:
diabetes, younger age at diabetes the time of diagnosis and every 1 to “Diabetes Mellitus, type 1/or diabetes
diagnosis.7,8 2 years thereafter, with more mellitus, type 1.mp,” “celiac disease or
frequent assessment if clinically celiac disease.mp,” “celiac sprue or
Recognized adverse effects of
indicated or if there is a first-degree celiac sprue.mp,” “celiacs or coeliacs.
untreated CD include iron deficiency,
relative with CD,18 whereas the mp,” “silent celiac or silent celiac.mp,”
anemia, growth retardation, and
American Diabetes Association “asymptomatic celiac or
osteoporosis.9 In T1D, undiagnosed
recommends considering CD asymptomatic celiac.mp,” “subclinical
CD may be associated with unstable
screening soon after diabetes celiac or subclinical celiac.mp,”
blood glucose levels, a greater risk of diagnosis and in those with clinical “gluten sensitive enteropathy.mp or
hypoglycemia,10 and increased risk of symptoms suggestive of CD.20 In exp celiac disease,” “reticulin.mp or
retinopathy.11 In those with view of these variable exp Reticulin,” “gliadin.mp or exp
confirmed CD and T1D, nonadherence recommendations, we systematically Gliadin,” “endomysial or endomysium.
to a gluten-free diet (GFD) is reviewed the epidemiology of CD in mp,” “tissue transglutaminase.mp,”
associated with early elevation of people with T1D to inform screening “antireticulin.mp,” “antigliadin.mp,”
albumin excretion rate,12 whereas CD guidelines. “antiendomysial.mp,” and
duration .10 years, irrespective of
“antiendomysium.mp.” We also
GFD adherence, is a risk factor for the
METHODS performed manual searches through
development of diabetic
article reference lists.
retinopathy.13 Other clinical Study Aims
improvements associated with GFD Data Extraction and Quality
compliance, including weight z scores, There are 2 specific aims of this
review. First, we systematically Assessment
hemoglobin, and serum ferritin, have
reviewed the epidemiology of biopsy- Two reviewers independently
been reported,14 as well as height z
proven CD in people with T1D, with extracted data from the included
scores and the reversal of iron-
subgroup analysis by age, gender, and studies. For each individual study,
deficiency anemia.15 In contrast,
duration of diabetes. Our second data were collected regarding study
noncompliance with a GFD was
specific aim was to examine the risk design, country, population and size,
associated with lower total bone
of CD in people with T1D, at diagnosis duration of follow-up, age at CD
mineral density, lower volumetric
and at specific time intervals after diagnosis, age at diabetes diagnosis,
lumbar spine z score, higher bone
diagnosis, to determine the optimal gender, diagnostic test(s) performed,
turnover, lower vitamin D, and lower
frequency of screening. frequency of screening, small bowel
ferritin.16 The rationale for CD
biopsy results, and prevalence rates.
screening is to prevent these adverse Study Selection Reports of CD-related symptoms
effects and complications, and to
Inclusion criteria were longitudinal around the time of CD diagnosis were
maximize growth. Because
cohort studies that screened for CD also collated. Study quality was
seroconversion from negative to
by using either EMAs and/or TTG in assessed by using the Newcastle-
positive CD autoantibodies can occur
children, adolescents, or adults with Ottawa quality assessment scale for
beyond 10 years of diabetes
T1D at least twice. Only studies in cohort studies.22 This scale evaluates
duration,17 repeated screening for CD humans and reported in the English 3 areas, selection, comparability
is necessary. language were included. Exclusion (confounding factors), and outcome
Despite the well-recognized increased criteria were studies other than (assessor blinding and follow-up),
risk of CD in T1D and the potential for longitudinal cohort studies, not in giving a possible total score of 9, with
2 studies8,17 Six studies reported CD Three studies reported no diagnosis. The proportion of patients
prevalence by age at diabetes relationship with age at diabetes screened decreased from 50% at
diagnosis,7,8,17,24,26,28 2 studies diagnosis.17,24,28 the end of year 1, to 35% (P , .001)
reported an association between at the end of year 5, and 12% at the
younger age (,5 years) at T1D Association Between CD and end of year 10.
diagnosis and development of CD,7,8 Diabetes Duration
with 1 study noting a tendency Of the 546 CD cases diagnosed after Symptomatology
toward younger age at diabetes diabetes, 40% were within 1 year of Five studies reported data on
diagnosis, although the relationship diabetes, 55% within 2 years, and CD-related symptoms and signs
was not statistically significant.26 79% within 5 years of diabetes (gastrointestinal, short stature,
anemia, or asymptomatic; n =
308),1,7,25,28,29 with 85% of cases
asymptomatic at the time of CD
diagnosis.
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has been published continuously since . Pediatrics is owned, published, and trademarked by the
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located on the World Wide Web at:
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Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it
has been published continuously since . Pediatrics is owned, published, and trademarked by the
American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois,
60007. Copyright © 2015 by the American Academy of Pediatrics. All rights reserved. Print
ISSN: .