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Coeliac disease (CD), an autoimmune enteropathy characterised by a permanent intolerance to dietary gluten, is a common disorder affecting about 1% of the general population worldwide.1 Ingestion of gluten containing cereals causes progressive damage to the small intestine in genetically susceptible individuals, leading to a variety of gastrointestinal and extra-gastrointestinal manifestations, including poor growth, irritability, iron deficient anaemia and dental enamel defects.2 CD is associated with other autoimmune diseases, such as type 1 diabetes, autoimmune thyroid disease and autoimmune liver disease.2 Exclusion of gluten from the diet is currently the only treatment option, and aside from alleviation of symptoms is important for establishing normal growth in children, and prevention of anaemia, osteoporosis and certain cancers.2–4 This treatment is challenging, as gluten is a common component of the typical New Zealand diet.

The incidence of CD has increased worldwide in both children and adults, and this is not entirely explained by an increased awareness of, and testing for the disease. Among Scottish children aged less than 16 years the incidence of CD increased from 1.8 to 11.7 per 100,000 between 1990–94 and 2005–09.5 In Denmark, incidence rates increased from 1.6 to 15.2 per 100,000 between 1980–84 and 2015–16 among all ages, with the largest increase in incidence among 0–9 year olds.6 Similarly, in New Zealand incidence increased from 0.9 per 100,000 in 1970 to 12.9 per 100,000 in 1999 among all ages.7 While the change in incidence among New Zealand children is unknown, the prevalence among 8–12 year old children is about 1%.8

With an increasing number of children diagnosed with CD internationally, and the changing presentation of the disease, we sought to obtain information about the clinical features, and the length and nature of the diagnostic process in New Zealand children aged less than 16 years with CD, and the difficulties associated with managing the disease.

Methods

Setting

The New Zealand Coeliac Health Survey was undertaken between 21 June and 6 August 2012 in collaboration with Coeliac New Zealand Incorporated (CNZ), a national organisation whose membership was the study population. At the time of the survey the membership of CNZ was 2,720, which included adults and parents or guardians of children with CD. The Multi-region Ethics Committee of New Zealand approved the study (MEC/12/EXP/072).

Survey development and administration

The survey has been described elsewhere.9 In brief, permission was obtained to use and modify the Canadian Celiac Health Survey.10,11 The Canadian survey was minimally adapted to fit the New Zealand context. Questions were added in order to obtain data on ethnicity, financial subsidies for CD, frequency of accidental consumption of gluten and difficulties with following a gluten-free (GF) diet. Following pilot testing at two regional CNZ support groups, and with a further three individuals, the questionnaire was further modified slightly to clarify the interpretation of a few questions.

The survey was self-administered, primarily online using Survey Monkey Software (www.surveymonkey.net). A study invitation and an information sheet along with a link to the survey were emailed to 2,383 members of CNZ and posted to a further 337 members by the organisation to maintain anonymity. Parents or guardians of children with CD were invited to complete the survey on their behalf. Efforts to maximise the response rate included speaking at two local CNZ meetings, sending an email reminder to complete the survey after four weeks and six weeks of sending the original invitation, and offering a chance to win a book voucher for survey participants. Informed consent was obtained by the choice of whether or not to complete the survey.

Data

The postal surveys were entered into Survey Monkey by KS and an assistant using the same Survey Monkey software. A 10% sample of postal surveys were randomly selected to check for data entry accuracy.

The data were exported from Survey Monkey to Microsoft Excel, cleaned and checked for errors. The data were analysed using STATA Data Analysis and Statistical Software integrated (version 15, StataCorp LP). Proportions and the mean ± SD or median (min-max) were calculated, as appropriate.

Results

Participants

Survey data were obtained for 123 children aged less than 16 years who were diagnosed with CD by a doctor. Most (87.8%) children had biopsy-confirmed CD (n=108). Thirteen children reported elevated CD antibodies without biopsy-confirmed CD, while 66 (53.7%) reported both a positive biopsy and elevated antibodies. Two children had CD diagnosed by a paediatrician without either a biopsy or positive antibodies. Both had a parent with biopsy positive CD.

Diagnosis of CD and ongoing symptoms

Table 1 shows the demographic characteristics of the study population. The median age of children at the time of diagnosis was four years (range 0–13 years). The time between the onset of symptoms and diagnosis varied between 0 and 11 years with the median time being 1.5 years. Prior to being diagnosed with CD, the symptoms of 45 (36.6%) children were reported to be attributed to other disorders such as acid reflux (n=20), a food allergy (n=18), anaemia (n=13), vitamin deficiency (n=10) or irritable bowel syndrome (n=7) (Table 2).

Table 1: Demographic characteristics and diagnostic details of children aged less than 16 years diagnosed with coeliac disease.

*unless otherwise specified.

Table 2: The different diagnoses made prior to a diagnosis of coeliac disease (n=123).

*Some participants were given more than one diagnosis.

Table 3 shows the number and proportion of children experiencing the various symptoms associated with CD at the time of diagnosis, and whether they had fully recovered from these symptoms after initiating a GF diet. The five most common symptoms present at diagnosis were bloating, gas and abdominal pain (79%), diarrhoea (59%), extreme weakness or tiredness (56%), poor growth (55%) and large, pale, foul-smelling stools (50%). Many children continued to experience symptoms despite following a GF diet. Of those with ongoing symptoms, 68 participants selected one or more reasons for not having fully recovered, including an unknown cause (61.8%), hidden sources of gluten (44.1%), another food allergy (29.4%) or problems adhering to a GF diet (14.7%).

Table 3: The clinical signs and symptoms present prior to, and ongoing symptoms following, a diagnosis of coeliac disease (n=123).

At the time of diagnosis, 96% of the children and their parents reported being told they needed to follow a GF diet for life and 84% reported being referred to a nutritionist or dietitian. Most children (94%) reported following a GF diet all the time, while 2% reported following a GF diet only some of the time. For those following a GF diet, there was a marked improvement in health for 104 (90%) children and a moderate improvement for eight (7%) children. Only one child was reported to have no improvement in health following the adoption of a GF diet.

Challenges with adopting a gluten free diet and quality of life issues

Following a GF diet was not easy for many families, with 12% finding it very difficult and 31% finding it moderately difficult. Accidental consumption of gluten was reported to occur at least weekly or monthly for 17% of participants. Free text comments highlighted that adopting a GF diet was easier for children when parents put in a lot of time and effort to ensure their child’s diet was GF, and when there was good family support or the whole family adopted a GF diet.

The need to consume a GF diet presented numerous challenges for children and their families. Table 4 shows some quality of life challenges of a GF diet for children. More than one-third (37%) felt different from other children because of their CD all or most of the time, and 31% felt embarrassed because they had to bring GF foods to parties all or most of the time. About one-quarter felt angry about having to consume a different diet all or most of the time and half felt angry some of the time. Most children however had a very strong understanding of the importance of following a GF diet, but 25% felt their teachers and friends did not understand why they could not eat foods with gluten all or most of the time.

Table 4: The quality of life challenges of a gluten-free (GF) diet for children aged less than 16 years with coeliac disease (CD).

The biggest challenge was eating away from home with 47% avoiding restaurants, and 19% avoiding travel all or most of the time. More than half reported not being invited out for meals at least some of the time. Birthday parties, school functions and eating at friends’ houses were particularly challenging. Organising and ensuring GF food was available at these functions, combined with a sense of being different from others, other people’s lack of understanding about a GF diet and cross contamination made social occasions with food present very difficult. Other reported challenges and difficulties were remembering to have GF food on hand when out and about, preparing GF food in advance, finding GF food products in smaller towns and the expense of GF food products.

Discussion

CD is an increasingly common chronic disorder12 for which the only treatment is a life-long GF diet. This study demonstrated that a diagnosis of CD in children can be considerably delayed, with symptoms commonly attributed to other diagnoses initially. Following a diagnosis of CD, the overall health of most children improved with a GF diet, but gastrointestinal and extra-gastrointestinal symptoms persisted for some children. Eating GF meals away from home was socially challenging for many children.

The clinical presentation of CD has changed over time, with the classic presentation of abdominal distention, anorexia, chronic diarrhoea, weight loss, irritability and failure to thrive now being less common.13–16 Most cases now present with non-classical symptoms, many of which are non-specific, or are diagnosed following screening in at risk groups, such as children with type 1 diabetes or Down’s syndrome.13–16 In this study, and the Canadian Celiac Health Survey,17 many children presented with a wide range of non-specific symptoms, including tiredness, weight loss, poor growth, mood swings and skin conditions such as eczema and itchy skin.2 This non-classical type of presentation can contribute to delays in the diagnosis of CD.18

In Canada, the median time between the onset of symptoms was one year and the range was 0–12 years,17 compared with a median time of 1.5 years (range of 0–11 years) in New Zealand children. Since the Canadian survey in 2002 and the New Zealand survey in 2012, awareness of CD has continued to increase, and serological testing for CD antibodies is more available. Consequently, it is possible that delays in the diagnosis of CD reported for children in the New Zealand survey may have shortened, as has been observed elsewhere.19 Diagnosing CD as early as possible after the onset of symptoms is important, particularly as differences in height growth between children with and without CD, are apparent from the age of 12 months even though the diagnosis may be at an older age.20

The most prevalent symptom prior to the diagnosis of CD reported in our study was bloating, gas and abdominal pain in four of five children, of which only 60% reported to have fully recovered after initiating a GF diet. This was despite 84% of participants and their caregiver(s) being referred to a dietitian following diagnosis to learn about a GF diet, and almost all stating they always consumed a GF diet. It is possible that the reported ongoing symptoms were secondary to non-coeliac causes, and participants most commonly attributed these to either an unknown cause or hidden sources of gluten in the diet.

This survey illustrates the difficulties in avoiding gluten for children with CD in New Zealand, and that their symptoms may not completely resolve either through poor adherence to the GF diet, particularly among teenagers, or inadvertent consumption of gluten.21–23 The popularisation of the GF diet into a ‘fad’ diet and the greater availability of GF foods24,25 has complicated the treatment for those with CD.26 The increased consumption of GF food by those without CD has contributed to the poor understanding of the severity of CD, especially in relation to the risks of cross-contamination and hidden gluten. Continued symptoms, even if intermittent, clearly have an impact on quality of life.27 Previous research has shown that social isolation can occur in children due to the misunderstanding of CD by others and that social isolation and misunderstandings of CD are important barriers to adherence to a GF diet.22 In this study, approximately one in three children reported feeling different from other children because of their CD, and feeling embarrassed because of having to bring GF foods to parties all or most of the time, and one-quarter felt their teachers and friends did not understand why they needed to eat GF foods.

Contamination of foods labelled as being GF is a recognised issue, both in New Zealand and internationally,28–32 and is one possible reason for ongoing symptoms. A recent Australian study found repeat batches of three GF labelled food items produced in dedicated GF factories tested positive for gluten. In New Zealand, Food Standards Australia New Zealand (FSANZ) develops standards for the food industry in Australia and New Zealand,33 and a claim to the effect that a food for medicinal purposes is GF may be made if the food contains (a) no detectable gluten; and (b) no oats or oats products; and (c) no cereals containing gluten that have been malted, or products of such cereals. Whereas in most of Europe, the UK and the US, food products can be considered GF if they contain less than 20 parts per million (ppm) of gluten as defined by the Codex Alimentarius Commission, a joint programme of the World Health Organization and Food and Agriculture Organization that develops international standards for food.34,35 Although the definition of GF is based on no detectable gluten in New Zealand and Australia, contamination still occurs during processing and packaging of food,29,30 and GF food preparation in cafes and restaurants is not necessarily adequate.36,37 The extent of GF food contamination in New Zealand is most likely to be under-reported as FSANZ does not enforce the code, and there is no regular monitoring of adherence to these standards.33 Further, most food recalls by the Ministry of Primary Industries (MPI) are voluntarily initiated by businesses when they become aware of a potential food safety or suitability issue.38

This survey population were members of CNZ, a non-profit organisation that supports New Zealanders with CD, and they may not be representative of the New Zealand population with CD. Further, it is possible that those participating in the survey are more motivated individuals or have different experiences compared with non-respondents. It was not possible to determine the survey response rate for children, as the CNZ membership list did not distinguish between adults and children. While respondents reported that their CD had been formally diagnosed, this and any prior diagnoses were not validated by checking medical records. However, it is unlikely that families would pay a CNZ membership fee, if their children did not have paediatrician-confirmed CD. Recall bias particularly in relation to symptoms at the time of diagnosis is possible, given the time between diagnosis and this survey was up to 14 years. Another limitation of the survey is that the experiences in quality of life were framed by a quantitative questionnaire format with defined questions. This may not capture the full range of challenges, including cost, that are experienced by families and children living with CD.39 Future research should engage mixed-methods or qualitative research methods to fully capture the challenges of those diagnosed with CD.

In conclusion, the prevalence of CD has been increasing over the past 30 years, yet timely diagnosis of CD in children and difficulty adhering to a GF diet, determined by the persistence of symptoms, remain an issue. The quality of life of children with CD can be impacted by social pressures related to having to adhere to a GF diet and a limited availability of safe uncontaminated GF options when attending parties, restaurants and travelling. Recognition of the symptoms and challenges associated with the diagnosis and treatment of CD in childhood remains an important issue in addressing the needs of children with CD, and their families.

Summary

Abstract

Aim

Coeliac disease (CD) is an increasingly common immune-mediated disorder. Treatment is a life-long gluten-free diet. The aim of this study was to describe the presenting symptoms, delays in diagnosis and difficulties associated with managing CD in children.

Method

The New Zealand Coeliac Health Survey was undertaken in collaboration with Coeliac New Zealand Incorporated, whose membership was the study population. The questionnaire enquired about presenting and ongoing symptoms, and challenges associated with treatment. Children aged

Results

There were 123 children with doctor-diagnosed CD. The median age at diagnosis was 4 years (range 0-13 years). The median time between symptom onset and diagnosis was 1.5 years (range 0-11 years). Despite a gluten-free diet, many children continued to experience symptoms, which were most commonly attributed to an unknown cause (61.8%), hidden sources of gluten (44.1%) or food allergy (29.4%). Families found that following a gluten-free diet was very (12%) or moderately (31%) difficult, particularly when eating out.

Conclusion

Recognition of the challenges associated with the diagnosis and treatment of CD in childhood is an important issue in addressing the needs of children with CD, and their families.

Author Information

Kirsten J Coppell, Public Health Physician and Research Associate Professor, Edgar Diabetes and Obesity Research, Department of Medicine, University of Otago, Dunedin;- Rosemary A Stamm, Research Fellow and Science Writer, Department of Medicine, Un

Acknowledgements

We thank the Canadian Celiac Association who allowed us to use and modify their questionnaire, Coeliac New Zealand Incorporated who facilitated the distribution of the study invitation to its members and the children and their parents who participated in the survey.

Correspondence

Kirsten Coppell, Department of Medicine, University of Otago, PO Box 56, Dunedin 9054.

Correspondence Email

kirsten.coppell@otago.ac.nz

Competing Interests

Both of Dr Coppell s children have coeliac disease and they both participated in this survey.

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Coeliac disease (CD), an autoimmune enteropathy characterised by a permanent intolerance to dietary gluten, is a common disorder affecting about 1% of the general population worldwide.1 Ingestion of gluten containing cereals causes progressive damage to the small intestine in genetically susceptible individuals, leading to a variety of gastrointestinal and extra-gastrointestinal manifestations, including poor growth, irritability, iron deficient anaemia and dental enamel defects.2 CD is associated with other autoimmune diseases, such as type 1 diabetes, autoimmune thyroid disease and autoimmune liver disease.2 Exclusion of gluten from the diet is currently the only treatment option, and aside from alleviation of symptoms is important for establishing normal growth in children, and prevention of anaemia, osteoporosis and certain cancers.2–4 This treatment is challenging, as gluten is a common component of the typical New Zealand diet.

The incidence of CD has increased worldwide in both children and adults, and this is not entirely explained by an increased awareness of, and testing for the disease. Among Scottish children aged less than 16 years the incidence of CD increased from 1.8 to 11.7 per 100,000 between 1990–94 and 2005–09.5 In Denmark, incidence rates increased from 1.6 to 15.2 per 100,000 between 1980–84 and 2015–16 among all ages, with the largest increase in incidence among 0–9 year olds.6 Similarly, in New Zealand incidence increased from 0.9 per 100,000 in 1970 to 12.9 per 100,000 in 1999 among all ages.7 While the change in incidence among New Zealand children is unknown, the prevalence among 8–12 year old children is about 1%.8

With an increasing number of children diagnosed with CD internationally, and the changing presentation of the disease, we sought to obtain information about the clinical features, and the length and nature of the diagnostic process in New Zealand children aged less than 16 years with CD, and the difficulties associated with managing the disease.

Methods

Setting

The New Zealand Coeliac Health Survey was undertaken between 21 June and 6 August 2012 in collaboration with Coeliac New Zealand Incorporated (CNZ), a national organisation whose membership was the study population. At the time of the survey the membership of CNZ was 2,720, which included adults and parents or guardians of children with CD. The Multi-region Ethics Committee of New Zealand approved the study (MEC/12/EXP/072).

Survey development and administration

The survey has been described elsewhere.9 In brief, permission was obtained to use and modify the Canadian Celiac Health Survey.10,11 The Canadian survey was minimally adapted to fit the New Zealand context. Questions were added in order to obtain data on ethnicity, financial subsidies for CD, frequency of accidental consumption of gluten and difficulties with following a gluten-free (GF) diet. Following pilot testing at two regional CNZ support groups, and with a further three individuals, the questionnaire was further modified slightly to clarify the interpretation of a few questions.

The survey was self-administered, primarily online using Survey Monkey Software (www.surveymonkey.net). A study invitation and an information sheet along with a link to the survey were emailed to 2,383 members of CNZ and posted to a further 337 members by the organisation to maintain anonymity. Parents or guardians of children with CD were invited to complete the survey on their behalf. Efforts to maximise the response rate included speaking at two local CNZ meetings, sending an email reminder to complete the survey after four weeks and six weeks of sending the original invitation, and offering a chance to win a book voucher for survey participants. Informed consent was obtained by the choice of whether or not to complete the survey.

Data

The postal surveys were entered into Survey Monkey by KS and an assistant using the same Survey Monkey software. A 10% sample of postal surveys were randomly selected to check for data entry accuracy.

The data were exported from Survey Monkey to Microsoft Excel, cleaned and checked for errors. The data were analysed using STATA Data Analysis and Statistical Software integrated (version 15, StataCorp LP). Proportions and the mean ± SD or median (min-max) were calculated, as appropriate.

Results

Participants

Survey data were obtained for 123 children aged less than 16 years who were diagnosed with CD by a doctor. Most (87.8%) children had biopsy-confirmed CD (n=108). Thirteen children reported elevated CD antibodies without biopsy-confirmed CD, while 66 (53.7%) reported both a positive biopsy and elevated antibodies. Two children had CD diagnosed by a paediatrician without either a biopsy or positive antibodies. Both had a parent with biopsy positive CD.

Diagnosis of CD and ongoing symptoms

Table 1 shows the demographic characteristics of the study population. The median age of children at the time of diagnosis was four years (range 0–13 years). The time between the onset of symptoms and diagnosis varied between 0 and 11 years with the median time being 1.5 years. Prior to being diagnosed with CD, the symptoms of 45 (36.6%) children were reported to be attributed to other disorders such as acid reflux (n=20), a food allergy (n=18), anaemia (n=13), vitamin deficiency (n=10) or irritable bowel syndrome (n=7) (Table 2).

Table 1: Demographic characteristics and diagnostic details of children aged less than 16 years diagnosed with coeliac disease.

*unless otherwise specified.

Table 2: The different diagnoses made prior to a diagnosis of coeliac disease (n=123).

*Some participants were given more than one diagnosis.

Table 3 shows the number and proportion of children experiencing the various symptoms associated with CD at the time of diagnosis, and whether they had fully recovered from these symptoms after initiating a GF diet. The five most common symptoms present at diagnosis were bloating, gas and abdominal pain (79%), diarrhoea (59%), extreme weakness or tiredness (56%), poor growth (55%) and large, pale, foul-smelling stools (50%). Many children continued to experience symptoms despite following a GF diet. Of those with ongoing symptoms, 68 participants selected one or more reasons for not having fully recovered, including an unknown cause (61.8%), hidden sources of gluten (44.1%), another food allergy (29.4%) or problems adhering to a GF diet (14.7%).

Table 3: The clinical signs and symptoms present prior to, and ongoing symptoms following, a diagnosis of coeliac disease (n=123).

At the time of diagnosis, 96% of the children and their parents reported being told they needed to follow a GF diet for life and 84% reported being referred to a nutritionist or dietitian. Most children (94%) reported following a GF diet all the time, while 2% reported following a GF diet only some of the time. For those following a GF diet, there was a marked improvement in health for 104 (90%) children and a moderate improvement for eight (7%) children. Only one child was reported to have no improvement in health following the adoption of a GF diet.

Challenges with adopting a gluten free diet and quality of life issues

Following a GF diet was not easy for many families, with 12% finding it very difficult and 31% finding it moderately difficult. Accidental consumption of gluten was reported to occur at least weekly or monthly for 17% of participants. Free text comments highlighted that adopting a GF diet was easier for children when parents put in a lot of time and effort to ensure their child’s diet was GF, and when there was good family support or the whole family adopted a GF diet.

The need to consume a GF diet presented numerous challenges for children and their families. Table 4 shows some quality of life challenges of a GF diet for children. More than one-third (37%) felt different from other children because of their CD all or most of the time, and 31% felt embarrassed because they had to bring GF foods to parties all or most of the time. About one-quarter felt angry about having to consume a different diet all or most of the time and half felt angry some of the time. Most children however had a very strong understanding of the importance of following a GF diet, but 25% felt their teachers and friends did not understand why they could not eat foods with gluten all or most of the time.

Table 4: The quality of life challenges of a gluten-free (GF) diet for children aged less than 16 years with coeliac disease (CD).

The biggest challenge was eating away from home with 47% avoiding restaurants, and 19% avoiding travel all or most of the time. More than half reported not being invited out for meals at least some of the time. Birthday parties, school functions and eating at friends’ houses were particularly challenging. Organising and ensuring GF food was available at these functions, combined with a sense of being different from others, other people’s lack of understanding about a GF diet and cross contamination made social occasions with food present very difficult. Other reported challenges and difficulties were remembering to have GF food on hand when out and about, preparing GF food in advance, finding GF food products in smaller towns and the expense of GF food products.

Discussion

CD is an increasingly common chronic disorder12 for which the only treatment is a life-long GF diet. This study demonstrated that a diagnosis of CD in children can be considerably delayed, with symptoms commonly attributed to other diagnoses initially. Following a diagnosis of CD, the overall health of most children improved with a GF diet, but gastrointestinal and extra-gastrointestinal symptoms persisted for some children. Eating GF meals away from home was socially challenging for many children.

The clinical presentation of CD has changed over time, with the classic presentation of abdominal distention, anorexia, chronic diarrhoea, weight loss, irritability and failure to thrive now being less common.13–16 Most cases now present with non-classical symptoms, many of which are non-specific, or are diagnosed following screening in at risk groups, such as children with type 1 diabetes or Down’s syndrome.13–16 In this study, and the Canadian Celiac Health Survey,17 many children presented with a wide range of non-specific symptoms, including tiredness, weight loss, poor growth, mood swings and skin conditions such as eczema and itchy skin.2 This non-classical type of presentation can contribute to delays in the diagnosis of CD.18

In Canada, the median time between the onset of symptoms was one year and the range was 0–12 years,17 compared with a median time of 1.5 years (range of 0–11 years) in New Zealand children. Since the Canadian survey in 2002 and the New Zealand survey in 2012, awareness of CD has continued to increase, and serological testing for CD antibodies is more available. Consequently, it is possible that delays in the diagnosis of CD reported for children in the New Zealand survey may have shortened, as has been observed elsewhere.19 Diagnosing CD as early as possible after the onset of symptoms is important, particularly as differences in height growth between children with and without CD, are apparent from the age of 12 months even though the diagnosis may be at an older age.20

The most prevalent symptom prior to the diagnosis of CD reported in our study was bloating, gas and abdominal pain in four of five children, of which only 60% reported to have fully recovered after initiating a GF diet. This was despite 84% of participants and their caregiver(s) being referred to a dietitian following diagnosis to learn about a GF diet, and almost all stating they always consumed a GF diet. It is possible that the reported ongoing symptoms were secondary to non-coeliac causes, and participants most commonly attributed these to either an unknown cause or hidden sources of gluten in the diet.

This survey illustrates the difficulties in avoiding gluten for children with CD in New Zealand, and that their symptoms may not completely resolve either through poor adherence to the GF diet, particularly among teenagers, or inadvertent consumption of gluten.21–23 The popularisation of the GF diet into a ‘fad’ diet and the greater availability of GF foods24,25 has complicated the treatment for those with CD.26 The increased consumption of GF food by those without CD has contributed to the poor understanding of the severity of CD, especially in relation to the risks of cross-contamination and hidden gluten. Continued symptoms, even if intermittent, clearly have an impact on quality of life.27 Previous research has shown that social isolation can occur in children due to the misunderstanding of CD by others and that social isolation and misunderstandings of CD are important barriers to adherence to a GF diet.22 In this study, approximately one in three children reported feeling different from other children because of their CD, and feeling embarrassed because of having to bring GF foods to parties all or most of the time, and one-quarter felt their teachers and friends did not understand why they needed to eat GF foods.

Contamination of foods labelled as being GF is a recognised issue, both in New Zealand and internationally,28–32 and is one possible reason for ongoing symptoms. A recent Australian study found repeat batches of three GF labelled food items produced in dedicated GF factories tested positive for gluten. In New Zealand, Food Standards Australia New Zealand (FSANZ) develops standards for the food industry in Australia and New Zealand,33 and a claim to the effect that a food for medicinal purposes is GF may be made if the food contains (a) no detectable gluten; and (b) no oats or oats products; and (c) no cereals containing gluten that have been malted, or products of such cereals. Whereas in most of Europe, the UK and the US, food products can be considered GF if they contain less than 20 parts per million (ppm) of gluten as defined by the Codex Alimentarius Commission, a joint programme of the World Health Organization and Food and Agriculture Organization that develops international standards for food.34,35 Although the definition of GF is based on no detectable gluten in New Zealand and Australia, contamination still occurs during processing and packaging of food,29,30 and GF food preparation in cafes and restaurants is not necessarily adequate.36,37 The extent of GF food contamination in New Zealand is most likely to be under-reported as FSANZ does not enforce the code, and there is no regular monitoring of adherence to these standards.33 Further, most food recalls by the Ministry of Primary Industries (MPI) are voluntarily initiated by businesses when they become aware of a potential food safety or suitability issue.38

This survey population were members of CNZ, a non-profit organisation that supports New Zealanders with CD, and they may not be representative of the New Zealand population with CD. Further, it is possible that those participating in the survey are more motivated individuals or have different experiences compared with non-respondents. It was not possible to determine the survey response rate for children, as the CNZ membership list did not distinguish between adults and children. While respondents reported that their CD had been formally diagnosed, this and any prior diagnoses were not validated by checking medical records. However, it is unlikely that families would pay a CNZ membership fee, if their children did not have paediatrician-confirmed CD. Recall bias particularly in relation to symptoms at the time of diagnosis is possible, given the time between diagnosis and this survey was up to 14 years. Another limitation of the survey is that the experiences in quality of life were framed by a quantitative questionnaire format with defined questions. This may not capture the full range of challenges, including cost, that are experienced by families and children living with CD.39 Future research should engage mixed-methods or qualitative research methods to fully capture the challenges of those diagnosed with CD.

In conclusion, the prevalence of CD has been increasing over the past 30 years, yet timely diagnosis of CD in children and difficulty adhering to a GF diet, determined by the persistence of symptoms, remain an issue. The quality of life of children with CD can be impacted by social pressures related to having to adhere to a GF diet and a limited availability of safe uncontaminated GF options when attending parties, restaurants and travelling. Recognition of the symptoms and challenges associated with the diagnosis and treatment of CD in childhood remains an important issue in addressing the needs of children with CD, and their families.

Summary

Abstract

Aim

Coeliac disease (CD) is an increasingly common immune-mediated disorder. Treatment is a life-long gluten-free diet. The aim of this study was to describe the presenting symptoms, delays in diagnosis and difficulties associated with managing CD in children.

Method

The New Zealand Coeliac Health Survey was undertaken in collaboration with Coeliac New Zealand Incorporated, whose membership was the study population. The questionnaire enquired about presenting and ongoing symptoms, and challenges associated with treatment. Children aged

Results

There were 123 children with doctor-diagnosed CD. The median age at diagnosis was 4 years (range 0-13 years). The median time between symptom onset and diagnosis was 1.5 years (range 0-11 years). Despite a gluten-free diet, many children continued to experience symptoms, which were most commonly attributed to an unknown cause (61.8%), hidden sources of gluten (44.1%) or food allergy (29.4%). Families found that following a gluten-free diet was very (12%) or moderately (31%) difficult, particularly when eating out.

Conclusion

Recognition of the challenges associated with the diagnosis and treatment of CD in childhood is an important issue in addressing the needs of children with CD, and their families.

Author Information

Kirsten J Coppell, Public Health Physician and Research Associate Professor, Edgar Diabetes and Obesity Research, Department of Medicine, University of Otago, Dunedin;- Rosemary A Stamm, Research Fellow and Science Writer, Department of Medicine, Un

Acknowledgements

We thank the Canadian Celiac Association who allowed us to use and modify their questionnaire, Coeliac New Zealand Incorporated who facilitated the distribution of the study invitation to its members and the children and their parents who participated in the survey.

Correspondence

Kirsten Coppell, Department of Medicine, University of Otago, PO Box 56, Dunedin 9054.

Correspondence Email

kirsten.coppell@otago.ac.nz

Competing Interests

Both of Dr Coppell s children have coeliac disease and they both participated in this survey.

  1. Lionetti E, Gatti S, Pulvirenti A, Catassi C. Celiac disease from a global perspective. Best Pract Res Clin Gastroenterol. 2015; 29:365–79.
  2. Thomas PC, Tighe MP, Beattie RM. Coeliac disease in children. BMJ. 2018; 363:k3932.
  3. Garnier-Lengline H, Cerf-Bensussan N, Ruemmele FM. Celiac disease in children. Clin Res Hepatol Gastroenterol. 2015; 39:544–51.
  4. Rodrigues M, Yonamine GH, Satiro CAF. Rate and determinants of non-adherence to a gluten-free diet and nutritional status assessment in children and adolescents with celiac disease in a tertiary Brazilian referral center: a cross-sectional and retrospective study. BMC Gastroenterol. 2018; 18:15.
  5. White LE, Merrick VM, Bannerman E, et al. The rising incidence of celiac disease in Scotland. Pediatrics. 2013; 132:e924–31.
  6. Grode L, Bech BH, Jensen TM, et al. Prevalence, incidence, and autoimmune comorbidities of celiac disease: a nation-wide, population-based study in Denmark from 1977 to 2016. Eur J Gastroenterol Hepatol. 2018; 30:83–91.
  7. Cook B, Oxner R, Chapman B, Whitehead M, Burt M. A thirty-year (1970–1999) study of coeliac disease in the Canterbury region of New Zealand. N Z Med J. 2004; 117:U772.
  8. Tanpowpong P, Ingham TR, Lampshire PK, et al. Coeliac disease and gluten avoidance in New Zealand children. Arch Dis Child. 2012; 97:12–6.
  9. Sharp K, Walker H, Coppell KJ. Coeliac disease and the gluten-free diet in New Zealand: The New Zealand Coeliac Health Survey. Nutr Diet. 2014; 71:223–8.
  10. Cranney A, Zarkadas M, Graham ID, et al. The Canadian Celiac Health Survey. Dig Dis Sci. 2007; 52:1087–95.
  11. Cranney A, Zarkadas M, Graham ID, Switzer C. The Canadian Celiac Health Survey-the Ottawa chapter pilot. BMC Gastroenterol. 2003; 3:8.
  12. Singh P, Arora A, Strand TA, et al. Global Prevalence of Celiac Disease: Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol. 2018; 16:823–36.e2.
  13. Kho A, Whitehead M, Day AS. Coeliac disease in children in Christchurch, New Zealand: Presentation and patterns from 2000–2010. World J Clin Pediatr. 2015; 4:148–54.
  14. Roma E, Panayiotou J, Karantana H, et al. Changing pattern in the clinical presentation of pediatric celiac disease: a 30-year study. Digestion. 2009; 80:185–91.
  15. Tapsas D, Hollen E, Stenhammar L, Falth-Magnusson K. The clinical presentation of coeliac disease in 1030 Swedish children: Changing features over the past four decades. Dig Liver Dis. 2016; 48:16–22.
  16. Van Kalleveen MW, de Meij T, Plotz FB. Clinical spectrum of paediatric coeliac disease: a 10-year single-centre experience. Eur J Pediatr. 2018; 177:593–602.
  17. Rashid M, Cranney A, Zarkadas M, et al. Celiac disease: Evaluation of the diagnosis and dietary compliance in Canadian children. Pediatrics. 2005; 116:e754–9.
  18. Fasano A, Catassi C. Current approaches to diagnosis and treatment of celiac disease: an evolving spectrum. Gastroenterology. 2001; 120:636–51.
  19. Riznik P, De Leo L, Dolinsek J, et al. Diagnostic Delays in Children with Coeliac Disease in the Central European Region. J Pediatr Gastroenterol Nutr. Published Online First: 18 June 2019. doi: 10.1097/MPG.0000000000002424.
  20. Kahrs CR, Magnus MC, Stigum H, Lundin KEA, Stordal K. Early growth in children with coeliac disease: a cohort study. Arch Dis Child. 2017; 102:1037–43.
  21. Hollon JR, Cureton PA, Martin ML, Puppa EL, Fasano A. Trace gluten contamination may play a role in mucosal and clinical recovery in a subgroup of diet-adherent non-responsive celiac disease patients. BMC Gastroenterol. 2013; 13:40.
  22. Bacigalupe G, Plocha A. Celiac is a social disease: family challenges and strategies. Fam Syst Health. 2015; 33:46–54.
  23. Czaja-Bulsa G, Bulsa M. Adherence to Gluten-Free Diet in Children with Celiac Disease. Nutrients. 2018; 10:e1424.
  24. Newberry C, McKnight L, Sarav M, Pickett-Blakely O. Going Gluten Free: the History and Nutritional Implications of Today's Most Popular Diet. Curr Gastroenterol Rep. 2017; 19:54.
  25. Hancock D, Al-Shaqsi S, Badron M, et al. The Prevalence of Gluten-Free Diet at the University of Otago: A Cross-Sectional Survey. J Gastroint Dig Syst. 2014; 4:209.
  26. King JA, Kaplan GG, Godley J. Experiences of coeliac disease in a changing gluten-free landscape. J Hum Nutr Diet. 2019; 32:72–9.
  27. Biagetti C, Gesuita R, Gatti S, Catassi C. Quality of life in children with celiac disease: A paediatric cross-sectional study. Dig Liver Dis. 2015; 47:927–32.
  28. Falcomer AL, Santos Araujo L, Farage P, Santos Monteiro J, Yoshio Nakano E, Puppin Zandonadi R. Gluten contamination in food services and industry: A systematic review. Crit Rev Food Sci Nutr. 2018:1–15.
  29. Ministry for Primary Industries. MPI reminds food businesses to be vigilant about gluten free claims. Retrieved 2 August 2019, http://www.mpi.govt.nz/news-and-resources/media-releases/mpi-reminds-food-businesses-to-be-vigilant-about-gluten-free-claims/
  30. Halmos EP, Clarke D, Pizzey C, Tye-Din JA. Gluten in "gluten-free" manufactured foods in Australia: a cross-sectional study. Med J Aust. 2018; 209:448–9.
  31. Sharma GM, Pereira M, Williams KM. Gluten detection in foods available in the United States - a market survey. Food Chem. 2015; 169:120–6.
  32. Verma AK, Gatti S, Galeazzi T, et al. Gluten Contamination in Naturally or Labeled Gluten-Free Products Marketed in Italy. Nutrients. 2017; 9(2).
  33. FSANZ (Food Safety Australia New Zealand). Food Standards Code. Retrieved 2 August 2019, http://www.foodstandards.gov.au/code/Pages/default.aspxhttp://coeliac.org.nz/fsanz-codex/
  34. Coeliac New Zealand. FSANZ & CODEX. Retrieved 2 August 2019,
  35. Joint FAO/WHO Codex Alimentarium Commission. Codex Alimentarius: Standard for foods for special dietary use for persons intolerant to gluten: CODEX STAN 118-1979. Rome: Food and Agriculture Organization, World Health Organization, 2008.
  36. Lerner BA, Phan Vo LT, Yates S, Rundle AG, Green PHR, Lebwohl B. Detection of Gluten in Gluten-Free Labeled Restaurant Food: Analysis of Crowd-Sourced Data. Am J Gastroenterol. 2019; 114:792–7.
  37. Schultz M, Shin S, Coppell KJ. Awareness of coeliac disease among chefs and cooks depends on the level and place of training. Asia Pac J Clin Nutr. 2017; 26:719–24.
  38. MPI (Ministry for Primary Industries). Food recall information for consumers. Retrieved 2 August 2019, http://www.mpi.govt.nz/food-safety/food-recalls/food-recall-information-for-consumers/
  39. Skjerning H, Mahony RO, Husby S, DunnGalvin A. Health-related quality of life in children and adolescents with celiac disease: patient-driven data from focus group interviews. Qual Life Res. 2014; 23:1883–94.

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Coeliac disease (CD), an autoimmune enteropathy characterised by a permanent intolerance to dietary gluten, is a common disorder affecting about 1% of the general population worldwide.1 Ingestion of gluten containing cereals causes progressive damage to the small intestine in genetically susceptible individuals, leading to a variety of gastrointestinal and extra-gastrointestinal manifestations, including poor growth, irritability, iron deficient anaemia and dental enamel defects.2 CD is associated with other autoimmune diseases, such as type 1 diabetes, autoimmune thyroid disease and autoimmune liver disease.2 Exclusion of gluten from the diet is currently the only treatment option, and aside from alleviation of symptoms is important for establishing normal growth in children, and prevention of anaemia, osteoporosis and certain cancers.2–4 This treatment is challenging, as gluten is a common component of the typical New Zealand diet.

The incidence of CD has increased worldwide in both children and adults, and this is not entirely explained by an increased awareness of, and testing for the disease. Among Scottish children aged less than 16 years the incidence of CD increased from 1.8 to 11.7 per 100,000 between 1990–94 and 2005–09.5 In Denmark, incidence rates increased from 1.6 to 15.2 per 100,000 between 1980–84 and 2015–16 among all ages, with the largest increase in incidence among 0–9 year olds.6 Similarly, in New Zealand incidence increased from 0.9 per 100,000 in 1970 to 12.9 per 100,000 in 1999 among all ages.7 While the change in incidence among New Zealand children is unknown, the prevalence among 8–12 year old children is about 1%.8

With an increasing number of children diagnosed with CD internationally, and the changing presentation of the disease, we sought to obtain information about the clinical features, and the length and nature of the diagnostic process in New Zealand children aged less than 16 years with CD, and the difficulties associated with managing the disease.

Methods

Setting

The New Zealand Coeliac Health Survey was undertaken between 21 June and 6 August 2012 in collaboration with Coeliac New Zealand Incorporated (CNZ), a national organisation whose membership was the study population. At the time of the survey the membership of CNZ was 2,720, which included adults and parents or guardians of children with CD. The Multi-region Ethics Committee of New Zealand approved the study (MEC/12/EXP/072).

Survey development and administration

The survey has been described elsewhere.9 In brief, permission was obtained to use and modify the Canadian Celiac Health Survey.10,11 The Canadian survey was minimally adapted to fit the New Zealand context. Questions were added in order to obtain data on ethnicity, financial subsidies for CD, frequency of accidental consumption of gluten and difficulties with following a gluten-free (GF) diet. Following pilot testing at two regional CNZ support groups, and with a further three individuals, the questionnaire was further modified slightly to clarify the interpretation of a few questions.

The survey was self-administered, primarily online using Survey Monkey Software (www.surveymonkey.net). A study invitation and an information sheet along with a link to the survey were emailed to 2,383 members of CNZ and posted to a further 337 members by the organisation to maintain anonymity. Parents or guardians of children with CD were invited to complete the survey on their behalf. Efforts to maximise the response rate included speaking at two local CNZ meetings, sending an email reminder to complete the survey after four weeks and six weeks of sending the original invitation, and offering a chance to win a book voucher for survey participants. Informed consent was obtained by the choice of whether or not to complete the survey.

Data

The postal surveys were entered into Survey Monkey by KS and an assistant using the same Survey Monkey software. A 10% sample of postal surveys were randomly selected to check for data entry accuracy.

The data were exported from Survey Monkey to Microsoft Excel, cleaned and checked for errors. The data were analysed using STATA Data Analysis and Statistical Software integrated (version 15, StataCorp LP). Proportions and the mean ± SD or median (min-max) were calculated, as appropriate.

Results

Participants

Survey data were obtained for 123 children aged less than 16 years who were diagnosed with CD by a doctor. Most (87.8%) children had biopsy-confirmed CD (n=108). Thirteen children reported elevated CD antibodies without biopsy-confirmed CD, while 66 (53.7%) reported both a positive biopsy and elevated antibodies. Two children had CD diagnosed by a paediatrician without either a biopsy or positive antibodies. Both had a parent with biopsy positive CD.

Diagnosis of CD and ongoing symptoms

Table 1 shows the demographic characteristics of the study population. The median age of children at the time of diagnosis was four years (range 0–13 years). The time between the onset of symptoms and diagnosis varied between 0 and 11 years with the median time being 1.5 years. Prior to being diagnosed with CD, the symptoms of 45 (36.6%) children were reported to be attributed to other disorders such as acid reflux (n=20), a food allergy (n=18), anaemia (n=13), vitamin deficiency (n=10) or irritable bowel syndrome (n=7) (Table 2).

Table 1: Demographic characteristics and diagnostic details of children aged less than 16 years diagnosed with coeliac disease.

*unless otherwise specified.

Table 2: The different diagnoses made prior to a diagnosis of coeliac disease (n=123).

*Some participants were given more than one diagnosis.

Table 3 shows the number and proportion of children experiencing the various symptoms associated with CD at the time of diagnosis, and whether they had fully recovered from these symptoms after initiating a GF diet. The five most common symptoms present at diagnosis were bloating, gas and abdominal pain (79%), diarrhoea (59%), extreme weakness or tiredness (56%), poor growth (55%) and large, pale, foul-smelling stools (50%). Many children continued to experience symptoms despite following a GF diet. Of those with ongoing symptoms, 68 participants selected one or more reasons for not having fully recovered, including an unknown cause (61.8%), hidden sources of gluten (44.1%), another food allergy (29.4%) or problems adhering to a GF diet (14.7%).

Table 3: The clinical signs and symptoms present prior to, and ongoing symptoms following, a diagnosis of coeliac disease (n=123).

At the time of diagnosis, 96% of the children and their parents reported being told they needed to follow a GF diet for life and 84% reported being referred to a nutritionist or dietitian. Most children (94%) reported following a GF diet all the time, while 2% reported following a GF diet only some of the time. For those following a GF diet, there was a marked improvement in health for 104 (90%) children and a moderate improvement for eight (7%) children. Only one child was reported to have no improvement in health following the adoption of a GF diet.

Challenges with adopting a gluten free diet and quality of life issues

Following a GF diet was not easy for many families, with 12% finding it very difficult and 31% finding it moderately difficult. Accidental consumption of gluten was reported to occur at least weekly or monthly for 17% of participants. Free text comments highlighted that adopting a GF diet was easier for children when parents put in a lot of time and effort to ensure their child’s diet was GF, and when there was good family support or the whole family adopted a GF diet.

The need to consume a GF diet presented numerous challenges for children and their families. Table 4 shows some quality of life challenges of a GF diet for children. More than one-third (37%) felt different from other children because of their CD all or most of the time, and 31% felt embarrassed because they had to bring GF foods to parties all or most of the time. About one-quarter felt angry about having to consume a different diet all or most of the time and half felt angry some of the time. Most children however had a very strong understanding of the importance of following a GF diet, but 25% felt their teachers and friends did not understand why they could not eat foods with gluten all or most of the time.

Table 4: The quality of life challenges of a gluten-free (GF) diet for children aged less than 16 years with coeliac disease (CD).

The biggest challenge was eating away from home with 47% avoiding restaurants, and 19% avoiding travel all or most of the time. More than half reported not being invited out for meals at least some of the time. Birthday parties, school functions and eating at friends’ houses were particularly challenging. Organising and ensuring GF food was available at these functions, combined with a sense of being different from others, other people’s lack of understanding about a GF diet and cross contamination made social occasions with food present very difficult. Other reported challenges and difficulties were remembering to have GF food on hand when out and about, preparing GF food in advance, finding GF food products in smaller towns and the expense of GF food products.

Discussion

CD is an increasingly common chronic disorder12 for which the only treatment is a life-long GF diet. This study demonstrated that a diagnosis of CD in children can be considerably delayed, with symptoms commonly attributed to other diagnoses initially. Following a diagnosis of CD, the overall health of most children improved with a GF diet, but gastrointestinal and extra-gastrointestinal symptoms persisted for some children. Eating GF meals away from home was socially challenging for many children.

The clinical presentation of CD has changed over time, with the classic presentation of abdominal distention, anorexia, chronic diarrhoea, weight loss, irritability and failure to thrive now being less common.13–16 Most cases now present with non-classical symptoms, many of which are non-specific, or are diagnosed following screening in at risk groups, such as children with type 1 diabetes or Down’s syndrome.13–16 In this study, and the Canadian Celiac Health Survey,17 many children presented with a wide range of non-specific symptoms, including tiredness, weight loss, poor growth, mood swings and skin conditions such as eczema and itchy skin.2 This non-classical type of presentation can contribute to delays in the diagnosis of CD.18

In Canada, the median time between the onset of symptoms was one year and the range was 0–12 years,17 compared with a median time of 1.5 years (range of 0–11 years) in New Zealand children. Since the Canadian survey in 2002 and the New Zealand survey in 2012, awareness of CD has continued to increase, and serological testing for CD antibodies is more available. Consequently, it is possible that delays in the diagnosis of CD reported for children in the New Zealand survey may have shortened, as has been observed elsewhere.19 Diagnosing CD as early as possible after the onset of symptoms is important, particularly as differences in height growth between children with and without CD, are apparent from the age of 12 months even though the diagnosis may be at an older age.20

The most prevalent symptom prior to the diagnosis of CD reported in our study was bloating, gas and abdominal pain in four of five children, of which only 60% reported to have fully recovered after initiating a GF diet. This was despite 84% of participants and their caregiver(s) being referred to a dietitian following diagnosis to learn about a GF diet, and almost all stating they always consumed a GF diet. It is possible that the reported ongoing symptoms were secondary to non-coeliac causes, and participants most commonly attributed these to either an unknown cause or hidden sources of gluten in the diet.

This survey illustrates the difficulties in avoiding gluten for children with CD in New Zealand, and that their symptoms may not completely resolve either through poor adherence to the GF diet, particularly among teenagers, or inadvertent consumption of gluten.21–23 The popularisation of the GF diet into a ‘fad’ diet and the greater availability of GF foods24,25 has complicated the treatment for those with CD.26 The increased consumption of GF food by those without CD has contributed to the poor understanding of the severity of CD, especially in relation to the risks of cross-contamination and hidden gluten. Continued symptoms, even if intermittent, clearly have an impact on quality of life.27 Previous research has shown that social isolation can occur in children due to the misunderstanding of CD by others and that social isolation and misunderstandings of CD are important barriers to adherence to a GF diet.22 In this study, approximately one in three children reported feeling different from other children because of their CD, and feeling embarrassed because of having to bring GF foods to parties all or most of the time, and one-quarter felt their teachers and friends did not understand why they needed to eat GF foods.

Contamination of foods labelled as being GF is a recognised issue, both in New Zealand and internationally,28–32 and is one possible reason for ongoing symptoms. A recent Australian study found repeat batches of three GF labelled food items produced in dedicated GF factories tested positive for gluten. In New Zealand, Food Standards Australia New Zealand (FSANZ) develops standards for the food industry in Australia and New Zealand,33 and a claim to the effect that a food for medicinal purposes is GF may be made if the food contains (a) no detectable gluten; and (b) no oats or oats products; and (c) no cereals containing gluten that have been malted, or products of such cereals. Whereas in most of Europe, the UK and the US, food products can be considered GF if they contain less than 20 parts per million (ppm) of gluten as defined by the Codex Alimentarius Commission, a joint programme of the World Health Organization and Food and Agriculture Organization that develops international standards for food.34,35 Although the definition of GF is based on no detectable gluten in New Zealand and Australia, contamination still occurs during processing and packaging of food,29,30 and GF food preparation in cafes and restaurants is not necessarily adequate.36,37 The extent of GF food contamination in New Zealand is most likely to be under-reported as FSANZ does not enforce the code, and there is no regular monitoring of adherence to these standards.33 Further, most food recalls by the Ministry of Primary Industries (MPI) are voluntarily initiated by businesses when they become aware of a potential food safety or suitability issue.38

This survey population were members of CNZ, a non-profit organisation that supports New Zealanders with CD, and they may not be representative of the New Zealand population with CD. Further, it is possible that those participating in the survey are more motivated individuals or have different experiences compared with non-respondents. It was not possible to determine the survey response rate for children, as the CNZ membership list did not distinguish between adults and children. While respondents reported that their CD had been formally diagnosed, this and any prior diagnoses were not validated by checking medical records. However, it is unlikely that families would pay a CNZ membership fee, if their children did not have paediatrician-confirmed CD. Recall bias particularly in relation to symptoms at the time of diagnosis is possible, given the time between diagnosis and this survey was up to 14 years. Another limitation of the survey is that the experiences in quality of life were framed by a quantitative questionnaire format with defined questions. This may not capture the full range of challenges, including cost, that are experienced by families and children living with CD.39 Future research should engage mixed-methods or qualitative research methods to fully capture the challenges of those diagnosed with CD.

In conclusion, the prevalence of CD has been increasing over the past 30 years, yet timely diagnosis of CD in children and difficulty adhering to a GF diet, determined by the persistence of symptoms, remain an issue. The quality of life of children with CD can be impacted by social pressures related to having to adhere to a GF diet and a limited availability of safe uncontaminated GF options when attending parties, restaurants and travelling. Recognition of the symptoms and challenges associated with the diagnosis and treatment of CD in childhood remains an important issue in addressing the needs of children with CD, and their families.

Summary

Abstract

Aim

Coeliac disease (CD) is an increasingly common immune-mediated disorder. Treatment is a life-long gluten-free diet. The aim of this study was to describe the presenting symptoms, delays in diagnosis and difficulties associated with managing CD in children.

Method

The New Zealand Coeliac Health Survey was undertaken in collaboration with Coeliac New Zealand Incorporated, whose membership was the study population. The questionnaire enquired about presenting and ongoing symptoms, and challenges associated with treatment. Children aged

Results

There were 123 children with doctor-diagnosed CD. The median age at diagnosis was 4 years (range 0-13 years). The median time between symptom onset and diagnosis was 1.5 years (range 0-11 years). Despite a gluten-free diet, many children continued to experience symptoms, which were most commonly attributed to an unknown cause (61.8%), hidden sources of gluten (44.1%) or food allergy (29.4%). Families found that following a gluten-free diet was very (12%) or moderately (31%) difficult, particularly when eating out.

Conclusion

Recognition of the challenges associated with the diagnosis and treatment of CD in childhood is an important issue in addressing the needs of children with CD, and their families.

Author Information

Kirsten J Coppell, Public Health Physician and Research Associate Professor, Edgar Diabetes and Obesity Research, Department of Medicine, University of Otago, Dunedin;- Rosemary A Stamm, Research Fellow and Science Writer, Department of Medicine, Un

Acknowledgements

We thank the Canadian Celiac Association who allowed us to use and modify their questionnaire, Coeliac New Zealand Incorporated who facilitated the distribution of the study invitation to its members and the children and their parents who participated in the survey.

Correspondence

Kirsten Coppell, Department of Medicine, University of Otago, PO Box 56, Dunedin 9054.

Correspondence Email

kirsten.coppell@otago.ac.nz

Competing Interests

Both of Dr Coppell s children have coeliac disease and they both participated in this survey.

  1. Lionetti E, Gatti S, Pulvirenti A, Catassi C. Celiac disease from a global perspective. Best Pract Res Clin Gastroenterol. 2015; 29:365–79.
  2. Thomas PC, Tighe MP, Beattie RM. Coeliac disease in children. BMJ. 2018; 363:k3932.
  3. Garnier-Lengline H, Cerf-Bensussan N, Ruemmele FM. Celiac disease in children. Clin Res Hepatol Gastroenterol. 2015; 39:544–51.
  4. Rodrigues M, Yonamine GH, Satiro CAF. Rate and determinants of non-adherence to a gluten-free diet and nutritional status assessment in children and adolescents with celiac disease in a tertiary Brazilian referral center: a cross-sectional and retrospective study. BMC Gastroenterol. 2018; 18:15.
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