Early detection of celiac disease could theoretically prevent most of the disease-associated complications, but long-term effects of this approach are unclear.
To investigate features at diagnosis and adulthood health in celiac disease patients diagnosed in early childhood in 1965–2014.
Medical data on 978 pediatric patients were collected and study questionnaires sent to 559 adult patients who were diagnosed in childhood. Results were compared between patients diagnosed in early (≤3.0 years) and later (3.1-17.9 years) childhood.
Early diagnosed patients (n=131) had more often total villous atrophy (37% vs 25%, p=0.001), gastrointestinal presentation (61% vs 47%, p<0.001), growth disturbances (70% vs 32%, p=0.001) and severe symptoms (30% vs 9%, p<0.001) and were less often screen-detected (10% vs 27%, p<0.001) at diagnosis than those diagnosed later (n=847).
Among 239 adult responders, early diagnosed patients (n=36) had fewer comorbidities (33% vs 53%, p=0.034) but considered their health less often good/excellent (69% vs 84%, p=0.029). The groups were comparable in current age, dietary adherence, symptoms and health-related quality of life.
Despite more severe initial presentation, the long-term health in early diagnosed patients was mostly comparable or even better to those diagnosed later in childhood. Poorer self-perceived health suggests a need for support during the transition to adulthood care.
Abbreviations:EmA (endomysial antibody), GSRS (gastrointestinal symptom rating scale questionnaire), PGWB (psychological general well-being questionnaire), TG2ab (transglutaminase 2 antibody)
Celiac disease, a chronic immune-mediated disorder driven by dietary gluten, is a significant public health problem affecting up to 2% of population [
1]. Nevertheless, due to the diverse and often mild clinical characteristics, many patients go unrecognized or have a long diagnostic delay [
2]. This is a cause for concern, since untreated celiac disease may predispose to severe long-term complications [
4], especially in those diagnosed later in adulthood [
5], and even to increased mortality [
3]. Although many of the complications do not manifest before adulthood, e.g. dental enamel defects, stunted growth, and reduced bone accrual may be preventable only if the disease is diagnosed and a gluten-free diet initiated in early childhood [
9]. Furthermore, it seems that children recover from their symptoms and villous atrophy faster than adults [
One option to reduce the risk of complications could be early screening of at-risk children. However, there is a lack of data on how this approach would affect the long-term treatment outcomesat individual level [
11]. The youngest patients comprise in many ways a special group. They are thought to have more classic and severe disease presentation, but the actual evidence is limited[
16]. They may not later remember their symptoms before diagnosis nor the benefits after starting a gluten-free diet. Moreover, adherence to the diet is usually caregivers’ responsibility. These aspects could hamper acceptance of the demanding life-long dietary restriction [
17]. On the other hand, early diagnosis has been linked with lower celiac disease-associated burden [
18] and dietary adherence might feel effortless since it has been part of their life as long as they can remember. Assessing these issues could help to weigh up the value of early screening and to pave the way for more personalized follow-up.
In the present study we aimed to evaluate the clinical characteristics of celiac disease at diagnosis and long-term treatment outcomes of the disease in adulthood in patients diagnosed before and after 3 years of age. This exact cut-off was selected based on the similar classification in previous studies [
19]and the finding that celiac autoantibodies develop in many cases already before the age of four [
2. Material and methods
2.1 Patients and study design
The study was conducted in Tampere University and Tampere University Hospital. Altogether 1,096 pediatric celiac disease patients were identified from a research database [
21]. After careful evaluation of the medical records, the diagnosis was confirmed in 978 (Fig. 1). During the whole study period, nationwide guidelines were systematically applied, and biopsy-proven diagnosis of celiac disease was required for all children to receive the financial compensation from the government. To examine adulthood health and treatment outcomes, study questionnaires were sent to 559 originally pediatric patients who had reached the age of 18 years and were alive as of September 2016. Relevant medical data and questionnaire results were compared between patients diagnosed at ≤3.0 years and at 3.1–17.9 years of age.
2.2 Medical data
The medical data collected included demographic information, nature and severity of symptoms and presence of complications such as anemia and poor growth. Serological and histopathological data and blood hemoglobin results were also gathered.
Main clinical characteristics of celiac disease at diagnosis were categorized as gastrointestinal symptoms; extra-intestinal complaints e.g. anemia, skin symptoms, arthralgia and poor growth; or screen-detected comprising those found by at-risk screening, such as close relatives of celiac disease patients and individuals with type 1 diabetes. Severity of symptoms was classified as none, mild, moderate or severe as described in detail elsewhere [
Anemia was defined as a hemoglobin value below the age- and gender-specific reference. Growth was evaluated from national growth charts with age- and gender-specific reference values and parental height information and categorized as normal or poor [
22]. It was also described with numeric parameters.
In our clinical routine, duodenal histopathology is evaluated from at least four representative and well-oriented biopsy samples in cases of suspected celiac disease. The degree of diagnostic villous atrophy is graded into partial, subtotal or total by a pathologist and the same classification has been used during the whole study period.
Endomysial antibodies (EmA) were introduced in 1983 [
23] and have been used in our clinical practice since the end of the 1980s. EmA are measured by an indirect immunofluorescence-based in-house method [
24]. An EmA dilution of 1:≥5 is considered positive. Transglutaminase 2 antibodies (TGA2ab) were introduced in 1997 [
25] and have been used since the end of the 1990s. TG2ab are measured by either automatized fluorescence enzyme immunoassay (Phadia AB, Uppsala, Sweden) or, before 2011, by conventional enzyme-linked immunosorbent assay (Phadia). Values of 7 U/L or higher are considered positive; 120 U/L being the highest reported value.
Adult celiac disease patients diagnosed in childhood were invited to complete a specific study questionnaire and validated questionnaires evaluating gastrointestinal symptoms and quality of life.
The study questionnaire was used to evaluate current sociodemographic characteristics and the presence of celiac disease-related and other concomitant chronic diseases. Patients were also asked to report their allergies and possibly celiac-associated complications, such as fractures, malignancies, miscarriages and osteoporosis, as well as current height and weight for calculation of body mass index (kg/m2). Complications and allergies were not included into calculation of overall comorbidities. Patients described their health experiences, possible persistent symptoms, adherence to and experiences of gluten-free diet and follow-up for celiac disease. Regularity of physical exercise and smoking status were asked to describe common health behavior and as possible confounding factors affecting the overall health.
Self-perceived general health was categorized as excellent, good, moderate or poor; and concerns about health as none, minor, moderate or severe. Adherence to a gluten-free diet was classified as strict, occasional lapses (lapses less than once a month), regular lapses (1-5 lapses per month) or no diet (weekly lapses); and experiences of maintaining the diet as easy, variable at times or difficult. The frequency of follow-up was categorized as regular (every 3 years or more often) or occasional/none.
The Gastrointestinal Symptom Rating Scale (GSRS) consists of 15 questions evaluating the presence and severity of gastrointestinal symptoms [
26]. Each question is rated with a seven-point Likert scale from asymptomatic to severe symptoms and the total score is a mean of all the questions. Sub-scores of five categories – diarrhea, indigestion, constipation, abdominal pain and reflux – are counted as a mean of 2-4 questions related to the category.
The Psychological General Well-Being (PGWB) questionnaire comprises 22 questions which evaluate different aspects – anxiety, depressive mood, positive well-being, general health and vitality – of health-related quality of life [
27]. The questions are scored on a Likert scale from 1 to 6 and the total score is the sum of all scores. Sub-scores are calculated as a sum of questions related to the category. Higher scores indicate better psychological well-being.
2.4 Ethical aspects
The Ethics Committee of the Pirkanmaa Hospital District and the Department of Pediatrics of Tampere University Hospital approved the study design (ethics committee code R16091, 31 May 2016). All patients completing the study questionnaires gave written informed consent. The study protocol follows the ethical guidelines of the Declaration of Helsinki.
Categorical variables are reported as numbers and percentages and compared using χ2 or Fisher's exact test. Based on visual assessment and Kolmogorov-Smirnov and Shapiro-Wilk tests, numeric variables were non-normally distributed and are thusreported as medians with quartiles and compared with Kruskal-Wallis or Mann-Whitney U test. P-value <0.05 was considered statistically significant. Logistic regression analysis was used to adjust the year of diagnosis between patients diagnosed in early and later childhood. All analyses were conducted with SPSS version 24 (IBM, Corporation, Armonk, NY).
Altogether 131 (13%) patients were diagnosed at ≤3.0 years of age (median age at diagnosis 1.7 [quartiles 1.2 and 2.2] years) and 847 (87%) at >3.0 years of age (10.7 [7.3, 14.0] years). Median age of all patients was 9.2 (quartiles 5.9 and 13.3) years. The groups did not differ in gender distribution (girls 62% vs 63%, p=0.769), but those diagnosed at older ages received their diagnoses in more recent years (median 1999 vs 2005, p<0.001). Annual incidence of patients diagnosed at ≤3.0 years of age remained quite stable in 1965–2014, whereas the number of those diagnosed later in childhood increased substantially from the 1970s to the present (Fig. 2).
Patients diagnosed at ≤3.0 years of age had more often gastrointestinal presentation, severe symptoms, and severe villous atrophy at diagnosis and were less often screen-detected than children diagnosed later (Fig. 3). Of specific symptoms, they suffered more often from diarrhea, vomiting and poor growth and less often from abdominal pain and skin symptoms, whereas the groups did not differ in the frequency of constipation, arthralgia or anemia (Fig. 4). At diagnosis, those diagnosed at ≤3.0 years of age were also shorter (median of height SD -0.6 vs 0.1, p<0.001), had lower median weight-to-height percentage (-6.0% vs 0.0%, p=0.004) and higher median EmA (1:1000 vs 1:500, p<0.001) and TG2ab values (120 U/l vs 86 U/l, p<0.001). After adjustment for year of diagnosis, differences between the groups persisted in diagnostic characteristics except in abdominal pain (p=0.052).
Altogether 239 (42%) of adult patients diagnosed in childhood returned the study questionnaires. Based on medical record data, the responders were more often women (69% vs 52%, p<0.001), had less often coexisting type 1 diabetes (9% vs 16%, p=0.029) and more often celiac disease in first degree relatives (56% vs 44%, p=0.035) than non-responders, while there were no differences in the proportion of those diagnosed ≤3.0 years of age (15% vs 12%, p=0.304), age at and year of diagnosis, main clinical presentation, presence of poor growth and anemia, or the severity of villous atrophy at diagnosis (data not shown).
Of 239 adult responders diagnosed in childhood, 36 (15%) were diagnosed at ≤3.0 years and 203 (85%) at >3.0 years of age. Those diagnosed at ≤3.0 years of age had, as a whole, fewer chronic comorbidities in adulthood than those diagnosed later, although there were no significant differences in any individual condition (Table 1). The groups were comparable in current age and gender distribution, presence of children, family history of celiac disease, smoking status and use of prescribed medication (Table 1), as well as in median height (167 cm vs 168 cm, p=0.481), body mass index (24 kg/m2 vs 24 kg/m2, p=0.277), and in employment status and regularity of physical exercise (data not shown).
Table 1Demographic characteristics, comorbidities, and medication in adult celiac disease patients diagnosed in early and later childhood.
|Age at diagnosis|
|≤3.0 years, n=36||>3.0 years, n=203|
|Current age, median (IQR)||36||33.8 (23.7, 38.4)||203||26.5 (22.1, 36.1)||0.109|
|Presence of children||20||56||80||40||0.086|
|Celiac disease in the family|
|Any coexisting chronic disease|
|Celiac disease-related comorbidity|
|Type 1 diabetes||1||3||17||9||0.322|
|Other coexisting condition|
| Gastrointestinal disease|
a First-degree relative;
b Celiac disease-related comorbidities and other coexisting conditions included;
c Other than celiac disease, e.g. inflammatory bowel diseases, irritable bowel syndrome and gastroesophageal reflux;
d E.g. melanoma and Hodgkin's lymphoma;
e Contraception excluded;After adjusting for year of diagnosis fp = 0.162 and gp = 0.004. Bold face indicates statistically significant difference.IQR, interquartile range.
Patients diagnosed at ≤3.0 years of age considered their health less often good/excellent in adulthood than did those diagnosed later, whereas the groups did not differ in everyday life restrictions due to the diet, use of oats, frequency of health concerns, current symptoms, or implementation of follow-up (Table 2). After adjusting with the year of diagnosis, the groups did not differ in the adherence to a gluten-free diet (Table 2) nor in presence or severity of current gastrointestinal symptoms or quality of life measured by GSRS and PGWB (Supplementary Table 1, online only).
Table 2Gluten-free diet (GFD), health, and symptoms in adult celiac disease patients diagnosed in early and later childhood.
|Age at diagnosis|
|≤3.0 years, n = 36||>3.0 years, n = 203|
|Adherence to GFD||0.047|
|Use of gluten-free oat||34||94||178||95||1.000|
|Experiences of GFD||0.061|
|Varying at times||4||11||43||21|
|Everyday life restrictions|
a Due to the dietary treatment;
b Experienced to be related to celiac disease;After adjusting with the year of diagnosis
c not statistically significant;
d remained statistically significant. Bold face indicates statistically significant difference.GFD, gluten-free diet.
We found children diagnosed with celiac disease at ≤3.0 years of age to have more advanced disease at diagnosis than those diagnosed at a later age. This was manifested by more severe villous atrophy, higher frequency of growth disturbances and higher levels of celiac autoantibodies. There have been few studies on this issue so far and, although different designs hamper comparison, diarrhea has usually been overrepresented and abdominal pain underrepresented among the youngest patients [
28]whereas findings about growth disturbances have been controversial [
29]. In line with the present study, some studies have reported more severe villous atrophy and higherantibody levels among patients diagnosed earlier [
15]. Interestingly, children with early onset inflammatory bowel disease often have a more severe initial presentation [
30], indicating that age-dependence of the phenotype could be a shared feature among autoimmune gastrointestinal diseases. Genetic factors could partly explain these findings, as there is, for example, evidence that HLA DQB1*02 homozygosity is associated with more severe features and younger age at celiac disease onset [
Genetics, however, cannot explain the increase in the number of diagnoses over time observed here. Better awareness of the disease together with increased at-risk group screening and less invasive diagnostic tools likely explain most of the changes [
29]. Screening enables diagnosis of asymptomatic patients and those with unrecognized, often atypical or mild complaints likely explaining also part of the concurrently changed clinical features of celiac disease [
22]. However, clinical incidence did not increase among the youngest patients here. It is possible that the incidence among the youngest patients has truly remained the same, but this could also be explained by inadequate recognition and therefore delayed diagnosis of young children with mild presentation. Supporting this theory, in prospective birth cohort studies a significant number of patients develop celiac disease antibodies already before the age of four years [
Patients diagnosed at ≤3.0 years of age had lower prevalence of comorbidities in adulthood suggesting a possible protective effect of an early initiated gluten-free diet. However, we found no differences in any specific disease, including known celiac disease-associated autoimmune conditions, thus we must be cautious before drawing firm conclusions. There is some evidence that gluten-free diet prevents complications such as short stature and fractures at least in symptomatic patients [
32]. However, the results for overall mortality and risk for malignancies [
5]and coexisting autoimmune diseases have been inconsistent [
35]. The discrepancies in the results between studies could be due to differences in study design and patient selection, particularly as regards age at diagnosis [
36]. Although it would be logical to assume that diagnosis in early childhood could provide the most efficient prevention of avoidable complications, more studies are needed.
Despite lower frequency of comorbidities and comparable quality of life in adulthood, early diagnosed patients perceived their general health poorer than those diagnosed later. Younger age at celiac disease diagnosis has previously been associated with better quality of life and lower disease-related burden after diagnosis in some [
39] but not in all studies [
41]. However, all participants in previous studies have been ≤20 years of age and the effect of transition to adulthood could not have been consistently assessed. Severe clinical characteristics before the diagnosis may cause concerns to be transferred from caregivers to children, thereby affecting their later health experiences. On the other hand, in some patients, early diagnosis could make adapting to the dietary treatment easier since it has been an ordinary part of their lives as long as they can remember.
Contrary to the hypothesis about easier dietary adherence, we saw that early diagnosed patients had poorer adherence to gluten-free diet than later diagnosed patients. However, this was affected by the longer time elapsing from the diagnosis in early diagnosed patients and after adjusting for year of diagnosis the difference was no longer significant. Surprisingly, the groups experienced maintaining the diet similarly challenging. In our earlier study evaluating dietary adherence in general, we reported comparable strictness of the diet in children diagnosed before and after the age of 13 years. However, the youngest children were not evaluated separately [
42]. In contrast, Högberg et al. reported better dietary adherence among 15 patients diagnosed before the age of four years than among 14 later diagnosed children [
43]. Their study was nevertheless published already in 2003, since when the availability of gluten-free products has improved considerably, which could at least partly explain the difference from the present result. Overall, several factors, such as availability and price of gluten-free products and national dietary patterns, as well as the general knowledge and attitudes towards celiac disease, may affect the convenience of dietary treatment [
4.1 Strengths and limitations
A major strength of the present study is the large number of celiac disease patients with a well-defined diagnosis. The diagnostic data, although mostly retrospective, were collected from comprehensive and systematically maintained medical records. The use of structured and widely used questionnaires in evaluating gastrointestinal symptoms and health-related quality of life increases the generalizability of the results, although the questionnaires are not celiac disease-specific [
46]. As a limitation, we did not evaluate dietary adherence with a validated questionnaire [
47] or used serology or recently introduced urinary or fecal gluten peptides to verify the adherence [
48]. Also, patients were still quite young and sufficient time may not have elapsed for all the comorbidities and complications to develop. Furthermore, comorbidities in adulthood were self-reported, which makes the results less robust than if they had been systemically confirmed from the medical records. However, there is evidence that self-reporting is overall fairly reliable [
49]. The response rate to the questionnaires was moderate, and although there were some differences between responders and non-responders, their age distribution and the proportion of those diagnosed ≤3.0 years of age were similar and response rate should therefore not affect the comparison of patients diagnosed at different age.
Children diagnosed with celiac disease during the first years of life often suffer severe initial presentation, but whether this is partly due to failure to recognize those with mild and atypical features remains unclear. The results support early screening of at-risk children, especially as we found the objectively measured long-term treatment outcomes to be good in those diagnosed at ≤3.0 years of age. However, their increased risk for poorer self-perceived adulthood health emphasizes the need for careful surveillance during the transition to adulthood care.
This study was supported by the Foundation for Pediatric Research, the Competitive State Research Financing of the Expert Area of Tampere University Hospital, the Sohlberg Foundation, the Maire Rossi Foundation, the Maud Kuistila Foundation, the Mary and Georg Ehrnrooth Foundation, the Paolo Foundation, the Emil Aaltonen Foundation, the Finnish Celiac Society and the Sigrid Juselius Foundation.
Prior presentation of data
Portions of this study were presented as posters at the 18th International Celiac Disease Symposium (ICDS), 2019, Paris, France and at the 51st Annual Meeting of the European Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN), 2018, Geneva, Switzerland.
Declaration of Competing Interests
Laura Kivelä, Katri Kaukinen and Kalle Kurppa have received personal fees for lectures from the Finnish Celiac Society outside the submitted work and serve as members of the advisory committee of the Finnish Celiac Society. The other authors declare no conflict of interest.
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Published online: September 06, 2020
Accepted: August 6, 2020
Received: April 27, 2020
© 2020 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.