The Impact of Coexisting Coeliac Disease on Type 1 Diabetes
Coeliac disease (CD) co-exists with type 1 diabetes (T1D) more commonly than CD alone within the general population (between 1.6% – 16.4% compared to 0.3 – 1.0% respectively)1. With over one million children and adolescents living with T1D worldwide according to the International Diabetes Federation2, there can be up to 100,000 individuals living with both T1D and CD. As both autoimmune conditions require significant dietary management and can impact on blood glucose levels, dietitians and diabetes educators play pivotal roles in the diagnosis and management of both chronic conditions.
This article addresses the presentation of CD in individuals with T1D, screening practices, the effect of both conditions on glycaemic variability, quality of life, complications risk, bone health, and particularly, how maintaining a strict gluten free diet (GFD) impacts on the above. Facilitators and barriers to maintaining the GFD will also be addressed.
Coeliac disease presentation and screening
CD often presents asymptomatically in T1D and is often diagnosed via screening. Screening guidelines for CD in paediatrics exist and generally recommend being performed at the time of diabetes diagnosis, and at two and five years thereafter, with more frequent assessment if clinical suspicion arises1, 3. We’ve shown CD is more prevalent in those diagnosed with T1D at a younger age, with the greatest risk in those with diabetes onset before 5 years of age4. While it is also advised that adults with T1D be considered for screening, there are no clear guidelines on frequency. Screening for CD should be performed using IgG-specific antibody tests (tTG or EmA IgG, or both). CD presentations in T1D are not necessarily associated with poor growth, nor deterioration in glycaemic management. While CD often presents asymptomatically in T1D, the severity of small bowel atrophy is similar to those with clinically suspected CD. A Finnish study published in 2017 found that half of those with T1D displayed subtotal or total villous atrophy at the time of small bowel biopsy5, while the other half had partial villous atrophy.
A recent large Canadian study found adults with T1D had a 1.5-fold higher rate of asymptomatic CD compared with children with T1D6. This finding is consistent with increasing rates of CD in adults7, with symptoms more likely to be subtle, with fewer classical malabsorptive presentations8. A Harvard study assessing body mass index (BMI) changes after CD diagnosis reported that 20.5% were classified as overweight (BMI 25-29.9 kg/m2) at the time of CD diagnosis, which increased to 24.2% after adopting the GFD9. This weight gain is attributed to increased energy intake owing to the resolution of gastrointestinal symptoms and absorption following intestinal healing9. Education around the GFD and weight management thus needs to be considered by dietitians.
When adopting a GFD , wheat, rye, barley and oats, which must be avoided, are often replaced by white rice or corn10. Such foods may contribute to a higher glycaemic index (GI)11, higher glycaemic load12 and lower fibre diet13, 14, compared to the gluten-containing equivalents. The restrictive nature of the GFD places an individual at risk of nutritional deficiencies, requiring increased vigilance in growing children and adolescents15. The mandatory fortification of wheat flour, but not gluten free grains, with micronutrients such as thiamin and folic acid16, further places those consuming a GFD at risk of inadequate nutrient intake. In adults consuming the GFD, inadequate intakes of thiamin, folate, vitamin A and calcium have been reported14, 17 .
Adults and youth with CD have lower carbohydrate intakes compared with the general population 14, 18 which has been attributed to poor palatability and increased costs of the GFD19 . Carbohydrate intakes in individuals with T1D is often at the lower level of dietary guidelines20 , which may be due to a conscious effort to reduce the risk of postprandial hyperglycaemia21 . However, whether the coexistence of T1D and CD is associated with a greater reduction in carbohydrate intake has not been previously examined. Our study in youth showed the total energy and macronutrient intake didn’t differ between the two groups, however those with T1D and CD were more likely to meet their vitamin C requirements (100% vs 43%, p=0.006) from increased fruit consumption, and were twice as likely to meet their calcium requirements (from increased yoghurt, milk and cheese), all of which are naturally gluten free foods. The reduced carbohydrate intake in those with CD is often due to a reduction in grains, which in our study was offset by an increased intake of fruit and dairy. However, the majority of participants collectively had inadequate intakes of calcium (76%), folate (71%) and fibre (53%) with excessive saturated fat intake (12% EER) and sodium (>2,000mg/day). Dietary advice for individuals with T1D should emphasise increasing fibre, folate and calcium intake, and reducing saturated fat and sodium intake, with further attention to increase thiamin intake for those on the GFD.
We conducted a case-control study of youth with T1D and CD vs T1D alone22 , where participants kept weighed 3-day food diaries, and were all given a test breakfast of GF cereal and milk to consume on the first three days. Participants wore a blinded continuous glucose monitor (Medtronic iPro2) uninterrupted for six days, and for each main meal (n=222), we assessed the pre-meal blood glucose level (BGL), peak BGL, time to peak, and 2 hour post prandial BGL. We found greater postprandial glucose excursions in those with T1D and CD, including a shorter time to peak BGL (77 vs 89 mins, p=0.03), higher peak (9.3 vs 7.3mmol/L, p=0.001) and higher postprandial BGLs than those with T1D alone (8.4 vs 7.0mmol/L, p=0.01), despite similar pre-meal BGLs (9.2 vs 8.6 mmol/L, p=0.28). The Canadian study mentioned earlier similarly found a GFD to be associated with greater glycaemic excursions6 .
Why the GFD may cause glucose variability
Studies measuring glucose absorption in the small intestine, conducted by infusing solutions with increasing glucose concentrations, found increased glucose absorption with longer duration of GFD consumption23 . Similarly, we found those who had CD for longer had a higher 2-hour postprandial BGL from both the test meal, and the participants’ usual meals. This suggests that chronic exposure to the GFD, which can have a higher GI, modifies glucose transport, resulting in a more rapid absorption of glucose, than individuals consuming gluten-containing high GI foods .In support of this hypothesis, it has been shown that three glucose transport molecules (SGLT1, PEPT1 and NHE3) were higher in people with treated vs untreated CD24 , implying that carbohydrates specific to the GFD may alter intra-intestinal gene transcription. The consideration of insulin timing given 10-15mins pre-prandially and lower GI choices, in addition to stronger insulin to carbohydrate ratios, may minimise the glycaemic excursions reported in our study.
Glycaemic variability associated with the GFD may have further health implications that warrant investigation, particularly as the GFD gains popularity in the general population25 , and as CD prevalence increases26 . Clinical management should address both glycaemic variability and dietary quality.
Adherence and barriers to maintaining the GFD
GFD adherence in youth with CD has been reported to vary from 25% to 96% in those with or without coexisting T1D5, 27-30. Factors found to increase adherence are being female, of younger age, having better school academic performance and higher self-esteem31 . CD diagnosis at a younger age has a higher compliance, with dietary transgressions most likely to occur in adolescents32 . GFD adherence is influenced by parental support, CD awareness, and availability of GF products33 .
Barriers are often multifactorial and overlapping in nature. GFD adherence tends to be lower during adolescence compared to other age groups28, 34 . Identified barriers include: eating outside the family home, limited social support and knowledge by teachers, friends and extended family members, unavailability and palatability of GF foods, and lack of symptoms or knowledge of health-related harms of gluten ingestion. However, the availability of GF products has increased considerably in recent times which may alleviate some of these barriers.
Quality of life
The coexistence of T1D with CD has been shown to negatively affect quality of life (QoL) in adults35. This is not surprising, considering the daily demands of managing T1D, including constant blood glucose monitoring, insulin administration, carbohydrate counting, mealtime behavioural challenges, and considerations around exercise and activity, overlaid with the requirements of a life-long GFD. Typical age-associated food behaviours such as transient food preferences, variable appetites, food refusal, neophobia, pickiness and behavioural resistance present additional challenges in those with T1D36 . The presence or absence of CD-related symptoms prior to diagnosis, or upon gluten ingestion is also expected to influence QoL.
We, and others37 have shown that youth with T1D + CD report similar generic and diabetes-specific QoL to those with T1D only38 . However, once stratified by GFD adherence, those who were unable to maintain a GFD, and their parents, reported lower QoL and general well-being, while glycaemic management was also suboptimal and higher (9.6% vs 8.0%, p = 0.02), indicating youth are struggling with both CD and T1D respectively, compared to those who maintained a GFD (GFD+). GFD adherence was measured by both serological parameters, as well as an in-depth dietary review by an Accredited Practicing Dietitian. Those that maintained the GFD were more likely to adopt the GFD within the first year of CD diagnosis, indicating a crucial time for follow-up of the GFD and to discuss any barriers the family may face.
While most cases presented asymptomatically, half of these individuals reported to be feeling ‘much better’, or ‘somewhat better’ after starting the GFD, noting retrospective improvement. Of note, parents of CD symptomatic youth reported a greater strain on their family relationships, emotional and social well-being. This may be owing to parents actively supporting the GFD for their children by educating others and preplanning for meals eaten outside of the home. Although burdensome, this extra support has proven beneficial for the well-being and GFD adherence of adolescents39 . Families who maintained the GFD were more likely to consider the diet beneficial, and were more likely to eat together, which is also a recognised indicator of greater nutritional quality in the general population40 , as well as T1D41 . This greater level or parental involvement may also extend to T1D management, which is reflected in the better glycaemic management in those who maintained the GFD.
For dietitians, while families may be daunted by the prospects of major dietary modifications in the absence of symptoms, informing them of possible improvements in feelings of well-being once starting the GFD may be a motivator. Encouraging family meals, and increasing awareness of carers, schools and restaurants will also assist with maintaining the GFD. Suggestions to join the Coeliac Society, or online support groups will also facilitate maintenance of the GFD.
Microvascular complications and bone health
There is strong evidence that individuals with either T1D or CD are at risk of complications that have a multifactorial aetiology including poor adherence with treatment. Undetected CD in adults with T1D is associated with worse glycaemic management (8.2% vs 7.5%, p= 0.05), and a higher prevalence of retinopathy and nephropathy42 . GFD commencement following confirmation of CD has been shown to reduce the risk of nephropathy and retinopathy, independent of glycaemic management42, 43 . CD was an independent risk factor for retinopathy and nephropathy in individuals with T1D44 , with CD duration > 15 years associated with a 2.8 fold increased risk of death37 . These studies highlight the importance of screening and treating CD in T1D. The role of GFD adherence also plays a role in the development of microvascular complications. We have demonstrated that non-adherence to the GFD was associated with early evidence of renal disease, as demonstrated by elevated albumin excretion rates45 , independent of HbA1c.
We have also found the coexistence of CD and T1D confers an additional burden on bone health, resulting in a low bone turnover state (thus resulting in older and stiffer bones), which results in high bone mineral density with reduced response to muscle pull, compared to those with T1D alone. These structural differences were independent of glycaemic management and dietary calcium intake. The findings suggest regular monitoring of bone health is needed to enable early interventions such as regular weight bearing exercise, and supporting GFD adherence to optimise bone health. These recommendations are particularly important in those with longer T1D duration, which is associated with increased fracture risk46 , and because GFD adherence for five years was associated with full recovery of bone mineral density in those with CD alone47 .
CD occurs more commonly in T1D, but is often asymptomatic and detected upon screening. When they occur together, there is evidence of an additive effect upon glycaemic variability, dietary quality, complications risk, bone health and QoL. A strict GFD is important in the treatment and prevention of adverse health effects of untreated CD. Accredited Practising Dietitians and Credentialled Diabetes Educators play an important role in providing education and supporting to help those affected to adopt and maintain a GFD.
- CD is more prevalent in those diagnosed with T1D at a younger age.
- CD often presents asymptomatically in youth and adults with T1D, with small bowel biopsies showing partial to total villous atrophy.
- CD presentations are not always associated with poor weight gain, low BMI, or deterioration in glycaemic management.
- The GFD is associated with increased glycaemic variability in youth with T1D and CD, as well as poor dietary quality – with excessive saturated fat, inadequate folate, iron and fibre intake.
- Insulin doses and the timing of insulin and meals may need adjusting for individuals with T1D + CD once they adopt a GFD.
- Those who adopt a GFD within the first year of CD diagnosis are more likely to maintain the GFD in the long term, indicating a crucial time for follow-up of the GFD and discussion of any barriers.
- Half of those who adopted the GFD reported feeling ‘much better’, or ‘somewhat better’ once starting a GFD, despite previously reporting they had no symptoms.
- Additional diagnosis of CD does not seem to impair QoL in youth and their parents. However, it is more likely to impact adults. Youth who maintained GFD also have improved glycaemic management and higher well-being and diabetes-specific QoL scores.
- GFD adherence is influenced by parental support, same family meal routines, CD awareness, and availability of GF products.
- Coexistence of T1D and CD is associated with early signs of kidney disease, and additional effects on bone health. Regular weight bearing exercise and GFD adherence may improve bone health.
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