Celiac disease and upper secondary school achievement in Sweden A retrospective cohort study

Celiac disease is an autoimmune disease that causes an immune-mediated enteropathy triggered by oral consumption of gluten [1]. The prevalence is around 1–3% [1, 2] and higher among females [1]. Celiac disease can cause a wide range of symptoms with both intestinal and extra-intestinal manifestation. Celiac disease is associated with an increased risk for other autoimmune diseases, like type one diabetes and autoimmune thyroid disease [1]. Untreated the disease is associated with an increased risk for other diseases like anemia, depression, lymphoma, and slightly increased mortality [1, 3]. Celiac disease is life-long and treated with a strict gluten-free diet [1]. Following a strict gluten-free diet can be challenging and previous studies have shown an adherence rate between 23–98% in children and 42–91% in adults [4, 5]. The expected effects of the treatment are mucosal healing with subsequent reduction in symptoms, serological markers, and co-morbidity [1]. Still, symptoms are common and often caused by voluntary and involuntary dietary lapses [6].

Several chronic conditions such as type one diabetes, epilepsy, and recurrent pain have been associated with poorer school achievements [7‐9]. To our knowledge few previous studies have investigated celiac disease and school achievements in children and adolescents. Namatovu et al. performed a cohort study on Swedish children showing that school performance in ninth grade was not affected by celiac disease [10]. Similarly, an Italian cross-sectional study showed that participants with celiac disease passed high school and upper secondary school to the same degree as the regional reference data [11]. Undiagnosed celiac disease was not associated with lower academic achievements in upper secondary school, but differences were seen in higher education in a small Finnish study [12].

In Sweden, the progression of education is structured as nine-year compulsory school and after completion adolescents can apply for upper secondary school. Upper secondary school is a vocational and/or university preparing three-year education. Achievements in upper secondary school in Sweden affects eligibility and competitiveness when applying for higher education, or when looking for work, thus future career prospects [13]. Therefore, we aimed to investigate if celiac disease influenced the choice of upper secondary school program, the completion of upper secondary school, and the final grade from upper secondary school in Swedish adolescents.

A nationwide register-based retrospective cohort study was performed.

In this register-based retrospective cohort study we showed that the adolescents with celiac disease diagnosed during childhood received similar or slightly better mean final grade from upper secondary school compared to the non-celiac disease adolescents born during the same period (1991–1997). The adolescents with celiac disease chose similar upper secondary school programs and completed upper secondary school to the same extent as other adolescents. Achievements in upper secondary school in Sweden affects future possibilities in life for example eligibility and competitiveness when applying to higher education, career prospects or when looking for work.

Previous research has investigated socioeconomic position and celiac disease which have shown inconsistent results. A Swedish study did not find any association with socioeconomic position and childhood onset celiac disease [19]. Another Swedish study showed that low socioeconomic position was associated with celiac disease in boys [20]. However, these studies did not investigate if celiac disease caused socioeconomic consequences. Namatovu et al. investigated childhood onset celiac disease and school achievements in ninth grade in a Swedish population and did not find any association [10] which is in line with our findings. On the other hand, socioeconomic consequences in terms of increased work loss both before and after diagnosis have been shown in adults with celiac disease [21].

It is previously known that health is an important factor for achievements in school. School achievement can be affected through several ways such as impaired cognitive and executive function, concentration problems, stress, and absenteeism [7‐9]. Celiac disease increases the risk for development of depression, anxiety, and headache [22], which all have been suggested to negatively affect school achievements [23, 24]. Furthermore, celiac disease has been associated with cognitive impairment [25, 26], which could be related to learning difficulties. While risk for co-morbidity decreases with treatment, patients with celiac disease experience a high treatment burden and impact on quality-of-life, often caused by stigma and difficulties to adhere to a gluten-free diet [27‐30]. The adherence rate to the gluten-free diet in Sweden is high (86–98%) but adolescence constitutes a period in life when both involuntary and voluntary dietary lapses are more common [5].

Adolescents with celiac disease daily face difficulties with the social situation when dining out with friends, difficulties with increased risk for mental illness, and difficulties with the transition from adolescents to adulthood [30]. Unexpectedly, we found that adolescents with celiac disease had similar or slightly better grades from upper secondary school compared to other adolescents. Why celiac disease did not affect school achievements in upper secondary school is therefore unclear. Lichtwark et al. showed that cognitive impairment in celiac disease improved on a gluten-free diet [25]. In Sweden follow-up in pediatric patients is every year to every second year at the pediatric department where adherence to a gluten-free diet and co-morbidity are determined [29]. A Swedish study showed that follow-up occurs according to recommendations [31]. All celiac disease cases in this study were diagnosed before 15 years of age, meaning that they had received their diagnosis before entering upper secondary school, had time from their diagnosis and should have received follow-up in the pediatric care for at least three years. Our result could therefore suggest that those with diagnosed celiac disease manage their disease and treatment, at least when supported through regular follow-up. If this is the case the importance of follow-up within health care beyond pediatric care is stressed.

In this study the celiac disease population received comparable final mean grade to the non-celiac disease population even when potential confounders were considered. When performing stratified analysis, only females with celiac disease performed a higher mean final grade. The reason why females with celiac disease perform better than their healthy peers can only be hypothesized. Previous research has associated high degree of personal responsibility, measured as a high internal locus of control, to high level of treatment adherence among children with celiac disease [32]. High internal locus of control has been associated with higher school achievements [33]. It could be that the requirement of strict adherence to a gluten-free diet, and the self-management this entails, reinforces traits which lead to better academic achievement. Of note, however, is that hypervigilance to a gluten-free diet can be concerning and extreme vigilance is associated with lower quality-of-life [34].

Although the Umeå SIMSAM Lab is a unique data infrastructure with data recorded prospectively and independently through administrative authorities’ control, we recognize some limitations. In this study population there were few from the celiac disease population with low Apgar score, even though the study population covered whole Sweden and included 3 257 individuals with celiac disease. Apgar score at five minutes, small for gestational age and low birth weight did not affect the outcomes on school achievement in the celiac disease population (Supplementary material, table A) and were therefore not included in the adjusted analyses. Apgar score and other factors from birth are previously known to be associated with lower school achievements [35]. Due to limited power, we could not investigate this further. An inherent limitation of the register-based studies is lack of data not routinely collected. In our study it would have been interesting to have individual data about adherence to the gluten-free diet and follow-up. However, Swedish studies indicates high adherence in adolescents and follow-up according to recommendations [5, 31]. The National Swedish Childhood Celiac Disease Register became nationwide 1998. Therefore, individuals who were diagnosed between 1991–1998, and not residents of the included areas during those years were not included. We have assessed the impact and found no significant effect. Inflation in school grades found in the study, might have resulted in an overestimation of final grades, thus they should be interpreted with caution. This study is performed in the Swedish school system. Thus, we cannot be certain that our findings can be generalized to other countries since a multitude of factors within both school- and health care systems may affect school achievements. Still, we believe that our findings are applicable to at least well-adherent adolescents who attend a follow-up program.

In conclusion, we found that celiac disease diagnosed during childhood does not negatively affect school achievements in upper secondary school in Sweden. In this study celiac disease was diagnosed before 15 years of age. Thus, the majority had lived with celiac disease for several years prior to upper secondary school and should have received follow-up medical care at the pediatric department. Our findings therefore suggest that diagnosis, adherence to a gluten-free diet and follow-up programs can minimize potential negative effects of the celiac disease on school achievements at upper secondary school. Future studies are necessary to determine if other school and health care systems have an effect and if socioeconomic consequences appear later in life.