Novel Communications in Diabetes

Screening and Treatment Outcomes in Adults and Children With Type 1 Diabetes and Asymptomatic Celiac Disease: The CD-DIET Study

  1. Farid H. Mahmud1⇑,
  2. Antoine B.M. Clarke1,
  3. Kariym C. Joachim1,
  4. Esther Assor1,
  5. Charlotte McDonald2,
  6. Fred Saibil3,
  7. Heather A. Lochnan4,
  8. Zubin Punthakee5,
  9. Amish Parikh6,
  10. Andrew Advani7,
  11. Baiju R. Shah8,
  12. Bruce A. Perkins9,
  13. Caroline S. Zuijdwijk10,
  14. David R. Mack11,
  15. Dror Koltin6,
  16. Emilia N. De Melo1,
  17. Eugene Hsieh12,
  18. Geetha Mukerji13,
  19. Jeremy Gilbert8,
  20. Kevin Bax14,
  21. Margaret L. Lawson10,
  22. Maria Cino15,
  23. Melanie D. Beaton16,
  24. Navaaz A. Saloojee17,
  25. Olivia Lou18,
  26. Patricia H. Gallego19,
  27. Premysl Bercik20,
  28. Robyn L. Houlden21,
  29. Ronnie Aronson22,
  30. Susan E. Kirsch23,
  31. William G. Paterson24 and
  32. Margaret A. Marcon25
  1. 1Division of Endocrinology, Department of Pediatrics, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
  2. 2Division of Endocrinology and Metabolism, St. Joseph’s Health Care, London Health Sciences Centre, Western University, London, Ontario, Canada
  3. 3Division of Gastroenterology, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, Ontario, Canada
  4. 4Department of Endocrinology, The Ottawa Hospital, Ottawa, Ontario, Canada
  5. 5Department of Medicine, McMaster University, Hamilton, Ontario, Canada
  6. 6Division of Endocrinology, Trillium Health Partners, Toronto, Ontario, Canada
  7. 7Division of Endocrinology, St. Michael’s Hospital, Toronto, Ontario, Canada
  8. 8Division of Endocrinology and Metabolism, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada
  9. 9Division of Endocrinology and Metabolism, University Health Network, University of Toronto, Toronto, Ontario, Canada
  10. 10Division of Endocrinology and Metabolism, University of Ottawa, Children’s Hospital of Eastern Ontario, Ottawa, Ontario, Canada
  11. 11Division of Gastroenterology, Hepatology and Nutrition, University of Ottawa, Children’s Hospital of Eastern Ontario, Ottawa, Ontario, Canada
  12. 12Department of Pathology, Sunnybrook Health Sciences Centre, Toronto, Ontario, Canada
  13. 13Division of Endocrinology, Women’s College Hospital, Toronto, Ontario, Canada
  14. 14Pediatric Gastroenterology, Department of Pediatrics, Children’s Hospital, London Health Sciences Centre, Western University, London, Ontario, Canada
  15. 15Division of Gastroenterology, University Health Network, University of Toronto, Toronto, Ontario, Canada
  16. 16Division of Gastroenterology, London Health Sciences Centre, London, Ontario, Canada
  17. 17Department of Gastroenterology, The Ottawa Hospital, Ottawa, Ontario, Canada
  18. 18JDRF, New York, NY
  19. 19Division of Endocrinology, Children’s Hospital, London Health Sciences Centre, Western University, London, Ontario, Canada
  20. 20Department of Gastroenterology, McMaster University, Hamilton, Ontario, Canada
  21. 21Department of Endocrinology, Kingston General Hospital, Kingston, Ontario, Canada
  22. 22LMC Diabetes & Endocrinology, Toronto, Ontario, Canada
  23. 23Division of Endocrinology, Markham-Stouffville Hospital, Markham, Ontario, Canada
  24. 24Department of Gastroenterology, Kingston General Hospital, Kingston, Ontario, Canada
  25. 25Division of Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, The Hospital for Sick Children, University of Toronto, Toronto, Ontario, Canada
  1. Corresponding author: Farid H. Mahmud, farid.mahmud{at}sickkids.ca
Diabetes Care 2020 Jul; 43(7): 1553-1556. https://doi.org/10.2337/dc19-1944

Abstract

OBJECTIVE To describe celiac disease (CD) screening rates and glycemic outcomes of a gluten-free diet (GFD) in patients with type 1 diabetes who are asymptomatic for CD.

RESEARCH DESIGN AND METHODS Asymptomatic patients (8–45 years) were screened for CD. Biopsy-confirmed CD participants were randomized to GFD or gluten-containing diet (GCD) to assess changes in HbA1c and continuous glucose monitoring over 12 months.

RESULTS Adults had higher CD-seropositivity rates than children (6.8% [95% CI 4.9–8.2%, N = 1,298] vs. 4.7% [95% CI 3.4–5.9%, N = 1,089], P = 0.035) with lower rates of prior CD screening (6.9% vs. 44.2%, P < 0.0001). Fifty-one participants were randomized to a GFD (N = 27) or GCD (N = 24). No HbA1c differences were seen between the groups (+0.14%, 1.5 mmol/mol; 95% CI −0.79 to 1.08; P = 0.76), although greater postprandial glucose increases (4-h +1.5 mmol/L; 95% CI 0.4–2.7; P = 0.014) emerged with a GFD.

CONCLUSIONS CD is frequently observed in asymptomatic patients with type 1 diabetes, and clinical vigilance is warranted with initiation of a GFD.

Introduction

Celiac disease (CD) is an immune reaction–mediated condition triggered by gluten, a protein found in wheat, barley, and rye. CD risk is increased in patients with type 1 diabetes and is characterized by a broad spectrum of presentations, including gastrointestinal symptoms, growth alterations, and anemia, but many patients are asymptomatic (1–4).

Serologic screening for CD has high sensitivity and specificity, but few reports have evaluated CD rates and the impact of treatment with a gluten-free diet (GFD) in asymptomatic CD (aCD) patients with type 1 diabetes. The Celiac Disease and Diabetes-Dietary Intervention and Evaluation Trial (CD-DIET) prospectively screened a large cohort of patients aged 8–45 years with subsequent engagement in a randomized, dietary treatment trial to evaluate changes in HbA1c and glycemic variability.

Research Design and Methods

Recruitment of Participants

Patients aged 8–45 years with type 1 diabetes (≥1 year duration) were approached to undergo CD testing at 22 diabetes centers in Ontario, Canada, as part of the CD-DIET study (clinicaltrials.gov, NCT01566110) (5). Exclusion criteria included CD symptoms (gastrointestinal symptomology or evidence of growth impairment, anemia, or osteoporosis), a previous CD diagnosis, and pregnancy.

CD Screening

Eligible participants (Supplementary Fig. 1) were screened using tissue transglutaminase IgA (TTG-IgA; Inova Diagnostics). CD-seropositive participants (TTG-IgA ≥30 chemiluminescent units [CU]) progressed to a gastroenterology consultation with centralized biopsy confirmation (Marsh score ≥2).

Dietary Intervention Study

Interested participants with biopsy-confirmed CD were randomized in a 1:1 ratio to a GFD or a gluten-containing diet (GCD) and followed for 1 year. Study visits with a dietitian occurred every 3 months using a standardized educational curriculum. Dietary adherence was also evaluated through quantification of dietary gluten intake and repeat TTG-IgA testing. Safety laboratory tests were evaluated (see Supplementary Material) with monitoring of growth, symptomology, and pregnancy. GCD participants who became symptomatic were transitioned to a GFD with the completion of outcome measures. A Data Safety Monitoring Committee evaluated adverse events. The primary outcome of CD-DIET was the change in HbA1c from baseline to 12 months. HbA1c was assessed centrally at baseline and at 6 and 12 months, with additional testing by local laboratories. Continuous glucose monitoring (CGM) was conducted using the iPro2 CGM system (Medtronic, Inc.) for blinded assessment.

Analysis was by intention to treat. Longitudinal differences in HbA1c between groups were analyzed using the difference in differences approach and confirmed using linear mixed-effects regression. CGM results were summarized using standard parametric methods, while paired t tests were used to assess within-group differences in HbA1c and postprandial glucose levels. All analyses were completed using R Statistics 3.5.1.

A sample size of n = 60 (30 patients per arm) was determined to be sufficient for our between-group analysis to reach 80% power at a 5% significance level under two-sided conditions. Paired analysis of HbA1c in the GFD arm, a sample size of n = 25 before versus after pairs, reached a power above 80% using a two-sided paired t test with significance set at P = 0.05.

Results

Recruitment and CD Screening

Overall, 2,585 patients consented and 2,387 subjects completed CD screening, including 1,298 adults (54.4%, 19–45 years) and 1,089 children (45.6%, 8–18 years) (see Supplementary Material). Higher rates of any prior CD serologic screening were seen in pediatric participants (n = 475, 43.6%, 95% CI 40.7–46.5%) as compared with adult participants (n = 89, 6.9%, 95% CI 5.5–8.3%) (odds ratio [OR] 10.5, P < 0.0001) (Fig. 1A). Adults had higher CD seropositivity rates (n = 88, 6.8%; 95% CI 5.4–8.2%) compared with children (n = 51; 4.7%; OR 1.48, 95% CI 3.4–5.9%, P = 0.035), but rates did not differ within each age-group on the basis of previous CD screening status. Biopsies were completed in 104 participants, and 82 were confirmed by biopsy with CD positivity rates of 4.2% (n = 54; 95% CI 3.1–5.3%) and 2.6% (n = 28; 95% CI 1.6–3.5%) for adult and pediatric participants, respectively (OR 1.64, P = 0.042) (Fig. 1B).

Figure 1
Figure 1

The results from the CD-DIET screening of asymptomatic patients with type 1 diabetes. A: The percentage of participants previously (black bars) and nonpreviously (white bars) screened for CD by age-group showing lower screening rates in adults (6.9% vs. 44.2%, P < 0.0001). B: CD serology– (TTG-IgA) and CD biopsy–confirmed rates of CD among the 2,387 subjects screened. Hatched bars indicate combined rates of CD serology and biopsy positivity, black bars illustrate pediatric data (8–18 years, N = 1,089), and white bars show adult rates (19–44 years, N = 1,298). Error bars represent 95% CIs. *Significant differences, P < 0.05.

Dietary Intervention Study

The 51 participants were randomized into the intervention phase, with 27 to the GFD group and 24 to the GCD group. Adherence to the assigned diet, as assessed by serial measures of gluten intake and TTG antibody titers, was deemed excellent (Fig. 2A). Ultimately, we observed no longitudinal difference in HbA1c between the GFD group and GCD group (+0.14% [1.5 mmol/mol], 95% CI −0.79 to 1.08, P = 0.76). Within the GFD group, an increase in HbA1c of +0.30% (3.3 mmol/mol) was observed over 12 months (95% CI 0.04–0.57%, P = 0.028) (Fig. 2B).

Figure 2
Figure 2

The results from CD-DIET. Data from the GFD arm shown in black with a dashed line, while data from the GCD are shown with solid gray line. A: Dietary adherence to the assigned group was assessed using serial serologic testing. TTG-IgA antibody titers were similar in the GCD and the GFD groups at baseline. They appropriately decreased in the GFD arm by 6 months and continued to drop among GFDs, resulting in a significant difference between GCDs (1,698.0 ± 1,834.0 CU) and GFDs (73.4 ± 83.9 CU) at 12 months (P < 0.0001). B: The change in HbA1c between study groups. No difference in HbA1c was seen between the GFD group relative to those on a GCD over the 12 months (+0.14% [1.5 mmol/mol], P = 0.76); however, within the GFD group, HbA1c increased (+0.30% [3.3 mmol/mol], 95% CI 0.04–0.57%, P = 0.028). C: Changes in postprandial glucose assessed by CGM. Postprandial glycemia in the GFD was higher compared with premeal levels at both the 2-h time point (+1.6 mmol/L [29 mg/dL]; P = 0.0015) and 4-h time point (+1.5 mmol/L [27 mg/dL]; P = 0.014), while glucose levels of the GCD arm returned to premeal levels (Δ = 0.1 mmol/L [1.8 mg/dL]). Error bars represent 95% CIs. *Significant differences, P < 0.05.

Using blinded CGM, no differences were seen in the percentage of time spent in hypoglycemic, euglycemic, or hyperglycemic ranges at 12 months. Despite this, postprandial glycemia was higher with the GFD relative to premeal levels at both the 2-h (+1.6 mmol/L, 95% CI 0.7–2.6, P = 0.0015) and 4-h (+1.5 mmol/L, 95% CI 0.4–2.7, P = 0.014) time points, while glucose levels of the GCD arm returned to premeal levels (Δ = 0.1 mmol/L after 4 h; 95% CI −0.8 to 1.0) (Fig. 2C). No differences were observed between groups in growth parameters (including height, weight, or BMI in children and adults; Supplementary Figs. 2 and 3), total daily insulin dose, or total daily insulin dose per kilogram.

Hypoglycemic adverse events that were nonsevere were reported with the GCD group (N = 3, 12.5%), with none reported with the GFD group (P = 0.097).

Conclusions

This study describes screening and treatment outcomes from a large prospective assessment of adult and pediatric patients with type 1 diabetes with aCD. We observed high rates of aCD with 1.5-fold higher rates in adults as compared with children. This result is consistent with increasing rates of CD in adults (6) and changes in the symptom profile toward a more subtle and less classical malabsorptive presentation with increasing age (7). In addition, age-related increases in autoimmune comorbidities are also well recognized, with recent T1D Exchange clinic registry data confirming rising rates of autoimmune comorbidities from adolescence into adulthood (8,9).

Adult participants in our study were also less likely to be screened for CD than children. This may reflect a lack of clarity about CD screening recommendations in adults and the absence of outcome studies in this population. Current North American diabetes guidelines advise consideration of screening patients with type 1 diabetes for CD, but actual details regarding screening tests, timing, and intervals are only explicitly described for children (10,11).

Dietary intervention with a GFD did not result in a difference in HbA1c between randomized groups but led to greater postprandial glucose excursions relative to a GCD. These changes are consistent with mucosal recovery, which can be prolonged (1–3 years), with subsequent improvements in absorption (2,12). Nonetheless, transition to a GFD was safe with no significant differences observed in hypoglycemic time or adverse events.

Strengths of this report include the large number of patients screened and the rigor in delineating an asymptomatic cohort. In addition, participants in the intervention phase, who were provided with frequent dietitian-based support, exhibited clear differences in gluten intake and follow-up TTG serology. Limitations of this study include a small sample size and the heterogeneity of participant characteristics that limits generalization of these findings. In addition, our data do not represent the prevalence rates, as we were challenged by enumeration of the complete population at risk in the clinics where screening was completed. It was also our experience that despite facilitated and no-cost access to care, many asymptomatic participants were overwhelmed by the diagnostic process and by the prospect of managing these two conditions, each with significant lifestyle implications.

In summary, diabetes clinicians should be aware of CD as an important autoimmune comorbidity of type 1 diabetes that is frequently asymptomatic. In addition, clinical vigilance is warranted during dietary transition, as GFD treatment may impact short-term glycemic variability. Given the additional risks for CD-related microvascular and bone complications, longitudinal studies are also needed to assess the clinical impact of this double diagnosis across the patient’s life span (13–15).

Article Information

Acknowledgments. This trial was funded by the JDRF Canadian Clinical Trial Network. We are grateful to the research staff at clinical sites and to patients and their families who participated in this trial.

Duality of Interest. F.H.M. served on advisory boards for Eli Lilly and Insulet. E.A. was employed as a dietitian with CD-DIET. Z.P. received grants, speaker fees, and consulting fees from Abbott, AstraZeneca, Boehringer Ingelheim, Bristol-Myers Squibb, Eli Lilly, Janssen, Lexicon, Merck, Medtronic, Novo Nordisk, Pfizer, and Sanofi. A.P. received consulting fees for education-related activities and advisory boards from Medtronic, Sanofi, Novo Nordisk, Janssen, AstraZeneca, Boehringer Ingelheim, and Eli Lilly. A.A. received research support from Boehringer Ingelheim and AstraZeneca, is listed as an inventor on a patent application (WO 2015/128453) from Boehringer Ingelheim, has received an unrestricted educational grant from Eli Lilly, and has received honoraria from Novo Nordisk, Eli Lilly, Boehringer Ingelheim, Abbott, and Dexcom. B.A.P. received personal fees from Medtronic, Eli Lilly, Abbott, Novo Nordisk, Insulet, Sanofi, Janssen, and Boehringer Ingelheim, as well as grants from the Bank of Montreal and Boehringer Ingelheim, all outside the scope of the submitted work. C.S.Z. is currently a coinvestigator for a Children’s Hospital of Eastern Ontario site of the Medtronic multicentre randomized controlled trial of home use of a hybrid closed-loop system (no monetary gain) and participated on an Eli Lilly Canada Advisory board once in February 2019 (honorarium directed to institution). J.G. received honoraria for speaking from Abbott, AstraZeneca, Boerhinger Ingelheim, Dexcom, Eli Lilly, Insulet, Janssen, Merck, Novo Nordisk, and Sanofi and is on advisory boards for AstraZeneca, Boerhinger, Dexcom, Eli Lilly, Janssen, Merck, Novo Nordisk, and Sanofi. M.D.B. received honoraria from Shire and Allergan; served on advisory boards for AbbVie, Takeda, Janssen, Lupin, and Gilead; and received grants from AbbVie, Novo Nordisk, and Gilead. R.L.H. participated in clinical trials (in the last 2 years) for AstraZeneca, Boehringer Ingelheim, Eli Lilly, and Novo Nordisk. R.A. has received research grants from Sanofi, Novo Nordisk, Janssen, AstraZeneca, Becton Dickinson Technologies, Boehringer Ingelheim, Eli Lilly, Zealand, Xeris, Medpace, Kowa, Insulet, Dexcom, Bausch Health, Tandem Diabetes, and Bayer and consultancies and personal fees from Sanofi, Novo Nordisk, Janssen, AstraZeneca, Becton Dickinson Technologies, Boehringer Ingelheim, Eli Lilly, HTL Strefa, Gilead, and Merck. No other potential conflicts of interest relevant to this article were reported.

Author Contributions. F.H.M., A.B.M.C., E.A., and M.A.M. wrote the first draft of the report and contributed to the study design, statistical analysis, and data interpretation. A.B.M.C., K.C.J., C.M., F.S., H.A.L., Z.P., A.P., A.A., B.R.S., B.A.P., C.S.Z., D.R.M., D.K., E.H., G.M., J.G., K.B., M.L.L., M.C., M.D.B., N.A.S., O.L., P.H.G., P.B., R.L.H., R.A., S.E.K., and W.G.P. were involved in the data collection and analyses. F.H.M., K.C.J., E.A., C.M., H.A.L., Z.P., A.P., A.A., B.R.S., B.A.P., C.S.Z., D.K., G.M., J.G., M.L.L., P.H.G., R.L.H., R.A., S.E.K., and M.A.M. recruited patients into the study. K.C.J., C.M., F.S., H.A.L., Z.P., A.P., A.A., B.R.S., B.A.P., C.S.Z., D.R.M., D.K., E.N.D.M., E.H., G.M., J.G., K.B., M.L.L., M.C., M.D.B., N.A.S., O.L., P.H.G., P.B., R.L.H., R.A., S.E.K., and W.G.P. contributed to the drafting and review of the report. F.H.M. is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Prior Presentation. Parts of this study were presented at the 2019 European Association for the Study of Diabetes Conference (EASD 2019), 16–20 September 2019, Barcelona, Spain.

Footnotes

  • Received September 30, 2019.
  • Accepted March 25, 2020.
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Screening and Treatment Outcomes in Adults and Children With Type 1 Diabetes and Asymptomatic Celiac Disease: The CD-DIET Study
Farid H. Mahmud, Antoine B.M. Clarke, Kariym C. Joachim, Esther Assor, Charlotte McDonald, Fred Saibil, Heather A. Lochnan, Zubin Punthakee, Amish Parikh, Andrew Advani, Baiju R. Shah, Bruce A. Perkins, Caroline S. Zuijdwijk, David R. Mack, Dror Koltin, Emilia N. De Melo, Eugene Hsieh, Geetha Mukerji, Jeremy Gilbert, Kevin Bax, Margaret L. Lawson, Maria Cino, Melanie D. Beaton, Navaaz A. Saloojee, Olivia Lou, Patricia H. Gallego, Premysl Bercik, Robyn L. Houlden, Ronnie Aronson, Susan E. Kirsch, William G. Paterson, Margaret A. Marcon
Diabetes Care Jul 2020, 43 (7) 1553-1556; DOI: 10.2337/dc19-1944
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