Art & science | gastroenterologyArt & science | acute care

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Art & science | The synthesis of art and science is lived by the nurse in the nursing act JOSEPHINE G PATERSON

AbstractCoeliac disease is an autoimmune condition caused by the ingestion of gluten-containing foods and affects about 1% of children and young people in the UK. Classic symptoms include diarrhoea, bloating, weight loss and abdominal pain. However, extra-intestinal manifestations, such as iron deficiency anaemia, faltering growth, delayed puberty and mouth ulcers, are increasingly being recognised. Some children have an increased risk of developing coeliac disease, such as a strong family history, certain genetic conditions and type 1 diabetes, therefore there is a need for increased awareness and early diagnosis before symptoms occur.

If coeliac disease is suspected, a child should have serological screening with anti-tissue transglutaminase titres. Diagnosis is traditionally confirmed by a small bowel biopsy while the child

remains on a ‘normal’ diet that does not exclude gluten. More recently, for a selective group of children, modification of the European Society for Paediatric Gastroenterology, Hepatology and Nutrition guidelines has enabled non-biopsy (serological) diagnosis of coeliac disease.

Children’s nurses have an important role in recognising and diagnosing coeliac disease earlier as well as offering ongoing dietary support. Enabling children to maintain a gluten-free diet is essential for general wellbeing and preventing long-term complications.

Keywordschild health, coeliac disease, European Society for Paediatric Gastroenterology, Hepatology and Nutrition, gluten-free diet, paediatrics, serological diagnosis

Correspondencesiba.paul@nhs.net

Siba Prosad Paul is specialty trainee, year 8, paediatrics, Yeovil District Hospital NHS Foundation Trust

Lauren McVeigh is a specialist paediatric dietitian

Elena Gil-Zaragozano is a clinical nurse specialist in paediatric gastroenterology

Dharamveer Basude is a consultant paediatric gastroenterologist

All at Bristol Royal Hospital for Children

Date of submissionJune 25 2015

Date of acceptanceSeptember 24 2015

Peer reviewThis article has been subject to open peer review and has been checked using antiplagiarism software

Author guidelinesjournals.rcni.com/r/ncyp-author-guidelines

DIAGNOSIS AND NURSING MANAGEMENT OF COELIAC DISEASE IN CHILDREN

et al 2004). In the UK the overall incidence in children appears to be increasing (White et al 2013, Whyte and Jenkins 2013). It is estimated that about 90% of cases remain unidentified (Ravikumara et al 2007). Greater awareness among healthcare professionals is therefore necessary to recognise and diagnose the condition as early as possible (National Institute for Health and Care Excellence (NICE) 2015).

Breastfeeding is considered to have a protective effect, and continuing breastfeeding and gradually introducing gluten-containing solid foods from four months of age may lower the risk of developing coeliac disease (Akobeng et al 2006, Steele 2011).

COELIAC DISEASE is as an immune-mediated systemic disorder elicited by the ingestion of gluten and related prolamins in genetically susceptible people. It is characterised by a variable combination of gluten-dependent clinical manifestations, specific antibodies, human leucocyte antigen (HLA)-DQ2 or HLA-DQ8 haplotypes and small bowel enteropathy (Murch et al 2013). Gluten is found in wheat, rye and barley.

EpidemiologyCoeliac disease affects about 1% of children and young people in the UK (Murch et al 2013, Bingley

Siba Prosad Paul and colleagues discuss the importance of spotting coeliac disease promptly and supporting children who need to follow a gluten-free diet

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Art & science | gastroenterology

Clinical presentation Coeliac disease can affect organs throughout the body to varying degrees. The immune reaction displayed in coeliac disease causes damage to the mucosal lining of the small intestine and results in malabsorption of vital nutrients, fat-soluble vitamins and minerals. Children may present with classic gastrointestinal symptoms, such as persistent diarrhoea, abdominal pain and weight loss. However, other extraintestinal symptoms (including unexplained iron deficiency anaemia, short stature, faltering growth, liver disease, arthropathy, mouth ulcers, muscle weakness, dermatitis herpetiformis, delayed menarche or onset of puberty) are increasingly being recognised (NICE 2015).

A significant number of children might remain asymptomatic despite substantial biochemical and intestinal mucosal changes.

ScreeningScreening using serological blood testing with immunoglobulin A (IgA)-based antitissue transglutaminase (anti-tTG) antibody titre is

Symptomatic children with intestinal and/or extraintestinal features

Asymptomatic children at high risk of developing coeliac disease

■■ Recurrent abdominal pain■■ Abdominal distension (bloated appearance)

■■ Persistent diarrhoea ■■ Constipation ■■ Vomiting■■ Faltering growth■■ Unexplained iron deficiency anaemia■■ Delayed menarche or onset of puberty ■■ Recurrent aphthous stomatitis ■■ Dermatitis herpetiformis ■■ Dental enamel defects

■■ First-degree relative with coeliac disease

■■ Type 1 diabetes mellitus■■ Down’s syndrome ■■ Selective immunoglobulin A deficiency

■■ Autoimmune thyroid disease ■■ Turner syndrome ■■ Williams syndrome ■■ Autoimmune liver disease

Table 1 Recommended screening for coeliac disease recommended for children with either intestinal or extraintestinal symptoms or asymptomatic children who belong to high-risk groups (Table 1) (NICE 2015, Husby et al 2012).

DiagnosisIn addition to recognising the symptoms, healthcare professionals should be alert to the possibility of coeliac disease in children who are either displaying non-specific symptoms or belong to high-risk groups.

History and examination A full patient history is required detailing all symptoms and identifying any conditions or family history that mean the child is at risk of developing coeliac disease (Table 1).

The child’s height, weight and body mass index should be plotted on an age and sex-appropriate growth chart (Sultan et al 2008, van Dommelen et al 2008) and a detailed physical examination to identify faltering growth, signs of nutritional deficiencies, abdominal distension, wasting of buttocks, short stature and other extraintestinal features, conducted (Sultan et al 2008, NICE 2015).

Investigations In total, 1% of children with coeliac disease are known to be IgA-deficient, therefore initial blood tests should include anti-tTG titres, IgA level as well as full blood count, liver and renal function tests (Husby et al, 2012, NICE 2015).

Until recently all children with suspected coeliac disease needed an upper gastrointestinal endoscopy for small bowel mucosal biopsies. A diagnosis would be confirmed if villous atrophy (Figure 1) and increased intraepithelial lymphocytic infiltrate were present (NICE 2015). In 2012, the European Society for Paediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) modified the pathway for diagnosing paediatric coeliac disease (Husby et al 2012). These modified guidelines recommend that symptomatic children with a high anti-tTG titre (greater than 10 times the normal upper

Figure 1 (a) Normal small intestinal mucosa and (b) villous atrophy in coeliac disease

a) b)

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limit) follow the non-biopsy serological pathway (Husby et al 2012, Murch at al 2013).

To confirm a diagnosis, children must have further positive blood results for IgA-based endomysial antibodies (EMA) or a second anti-tTG of greater than 10 times the normal upper limit (if EMA is unavailable) plus genetic typing for HLA-DQ2/DQ8 (Husby et al 2012, Murch et al 2013). The upper limit of normal is the cut off value for anti-tTG reported by a particular laboratory. This will vary depending on the laboratory reporting the anti-tTG and the assay it uses.

Symptomatic children

Positive antitissue transglutaminase (anti-tTG) titre of <10 times normal upper limit

Positive anti-tTG titre of >10 times normal upper limit and a negative HLA-DQ2/8 haplotype

Asymptomatic children

Positive anti-tTG titre (irrespective of value)

Figure 2 Algorithm to decide diagnostic pathway for coeliac disease

(Adapted from Husby et al 2012, Murch et al 2013, Paul and Spray 2014)

If a symptomatic child’s blood results do not fall into the category for non-biopsy diagnosis (Table 2), or the child is asymptomatic and has a positive anti-tTG titre, the modified ESPGHAN guidelines still recommend that small bowel biopsies are necessary while the child remains on a normal non-restrictive diet that does not avoid gluten (Husby et al 2012, Murch et al 2013, Paul et al 2015). This is shown in Table 2.

The ESPGHAN guidelines have been endorsed and adapted, with minor amendments, for the diagnosis of coeliac disease in children in the UK by the British Society of Paediatric Gastroenterology, Hepatology and Nutrition and Coeliac UK (Murch et al 2013). Figure 2 is an algorithm following the approved pathway for diagnosing coeliac disease in children in the UK.

Management The management of coeliac disease in children remains the same irrespective of the pathway used at diagnosis and involves maintenance of a strict gluten-free diet as well as the correction of any nutritional deficiencies. Children should initially be seen by a specialist paediatric dietitian and have follow-up appointments with a paediatrician or paediatric gastroenterologist and paediatric

(Husby et al 2012)

anti-tTG titre>10x upper limit normal, child symptomatic

Perform endoscopy and small-bowel biopsies

Positive histology, diagnosis of coeliac disease is confirmed

Use the ESPGHAN diagnostic pathway, obtain further blood samples for EMA and HLA-DQ2/DQ8 typing.

If EMA is not available, take a second sample for tTG.

anti-tTG titre<10× upper limit of normal (symtomatic) or aysmptomatic with positive anti-tTG titre

If HLA-DQ2/DQ8 is negative, continue with a normal diet

If EMA is positive (or second anti-tTG titre >10x upper

limit of normal) and either HLA-DQ2 or DQ8 is positive, diagnosis of coeliac

disease can be confirmed

Start gluten-free diet and provide follow up with paediatricians and paediatric dietitians

Suspicion of coeliac disease in children (symptomatic/asymptomatic)

Serological screening with anti-tTG titre and IgA levels. Advise that the child continues with a normal diet that contains gluten.

Table 2 Children who still need small bowel biopsies to confirm diagnosis

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dietitian, initially every six months and then at least annually (Husby et al 2012, Paul and Spray 2014).

Healthcare professionals have a vital role in explaining and reinforcing to children and their families the importance of a lifetime adherence to a strict gluten-free diet. Maintaining such a diet will enable healing of the intestinal villi, correction of nutrient deficiencies and allow the child to have a normal life expectancy without complications related to the disease. Conversely, poor adherence is likely to result in persistence of the short and long-term risks associated with the disease (NICE 2015, Steele 2011) as outlined in Box 1.

Support given by specialist nurses and dietitians, running clinics for children with coeliac disease, has been found to be equally as effective as those conducted by medical professionals and provides better continuity of care (Rajani et al 2013, Ross et al 2013).

Role of the children’s nurse There is an important role here in the early recognition and diagnosis of coeliac disease and nurses must be alert to the varied, and often non-specific, features of coeliac disease in children. Such symptoms may be picked up when children attend hospital or clinics for unrelated issues or when a nurse conducts routine investigations (Paul et al 2015). Identification of asymptomatic children from high-risk groups (Table 1) can help to highlight the need for serological screening.

Nurses can also provide valuable information and support to children, their families and community healthcare professionals on maintaining a gluten-free diet. To prevent long-term complications nurses must communicate with the wider multidisciplinary team if they suspect that a child is not adhering to a gluten-free diet.

Role of children’s dietitians Coeliac disease is a chronic long-term condition that is treated by

■ Impaired nutrition■ Impaired growth and delayed onset and disordered

progression of puberty■ Osteoporosis and low bone mineral density■ Increased risk of pathological fractures■ Small bowel lymphoma■ Fertility issues■ Unfavourable pregnancy outcomes, such as low

birth weight and miscarriage■ Development of other autoimmune conditions,

for example diabetes and hypothyroidism

Box 1 Risks associated with non-adherence to a gluten-free diet

strict, lifelong adherence to a gluten-free diet. This can be extremely challenging for some children and their families, particularly for those who have mild symptoms or were asymptomatic at diagnosis.

Dietitians have an integral role in the management of children following a diagnosis of coeliac disease. Initial education focuses on the role of a gluten-free diet to manage the disease, highlights sources of gluten in different food and provides culturally-appropriate advice about gluten-free foods. Dietitians also provide advice and information about food labelling, cooking, cross-contamination and prescribing as well as general support to achieve a balanced diet.

Paediatric dietitians are also trained to assess children’s nutritional status and discuss the nutritional deficiencies that can arise in coeliac disease (Alzaben et al 2015). In rare cases, a lactose-free diet may also be temporarily required if damage to the brush border epithelium has caused secondary lactose intolerance (Ojetti et al 2005) and the paediatric dietitian can provide relevant advice on diet until the gut has healed sufficiently for lactose digestion to be recommenced.

Children should receive lifelong follow up, usually through an annual review (Murch et al 2013) with a paediatric dietitian, the most skilled person to provide this. As well as offering support and expert advice, a dietitian can monitor adherence to a gluten-free diet, helping children and their families to overcome any barriers and ensure that even patients who have had a lot of experience of coeliac disease do not inadvertently consume gluten-containing foods.

Faltering growth and weight loss are common symptoms at diagnosis of coeliac disease and there is further evidence that children with gastrointestinal disorders, including coeliac disease, are at increased risk of undernutrition (Aurangzeb et al 2010). Once a gluten-free diet is commenced and mucosal healing begins, nutritional status will often improve. However, some children may need nutritional support as an inpatient. In these cases, as well as the initial education surrounding a gluten-free diet, the dietitian will advise on a plan for nutrition support using gluten-free oral nutritional supplement drinks or nasogastric feeding if required.

In severe cases of malnutrition, a dietitian will provide advice on the risk, prevention and management of refeeding syndrome (RFS) (Lenicek Krleza et al 2013). RFS broadly encompasses a severe electrolyte disturbance – principally low-serum concentrations of intracellular ions such as phosphate, magnesium, and potassium –

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and metabolic abnormalities in undernourished patients undergoing refeeding whether orally, enterally, or parenterally. RFS reflects the change from catabolic to anabolic metabolism and if not recognised early can lead to serious consequences.

Inpatient care A gluten-free diet must be followed whenever a child with coeliac disease is admitted to hospital (Mårild et al 2010). Since January 2015, there are mandatory standards covering hospital food and the provision of a gluten-free diet. Hospitals are required to provide a gluten-free menu and should clearly label which foods do and do not contain gluten (Department of Health 2014). However, dietetic support may still be required to enable the ordering of a gluten-free diet as well as educating ward staff in avoiding cross-contamination with gluten-containing meals. Dietitians must also educate staff to identify non-food items such as

modelling dough, crayons and glues that may contain gluten or become cross-contaminated. Although gluten is not absorbed through the skin, young children have a tendency to put objects in their mouths so it is important that such play products are not accessible to children in hospital (Barnard et al 2012).

Nursing and other ward staff play an important role in supporting the dietary management of children with coeliac disease by observing dietary intake and highlighting any concerns about non-adherence to a gluten-free diet. Nutritional screening completed on admission can help identify any signs of malnutrition that may be an indication of ongoing mucosal damage due to the non-adherence of a gluten-free diet. Palatability issues of gluten-free foods or parents unable to prepare culturally appropriate food items with gluten free flour can result in non-adherence to gluten-free diet and

Case studyA 16-month-old previously healthy boy, Tom (not his real name) was admitted with a three-week history of vomiting after eating food, reduced appetite, lethargy and weight loss. Initial observations revealed a heart rate of 132 beats per minute, respiratory rate 34 breaths per minute, temperature 36.9°C and a central capillary time of two seconds. Plotting his weight on a growth chart revealed a fall in growth velocity from the 75th centile at four months of age to below the 25th centile at presentation. He was admitted for observation, further investigations and optimising nutrition.

A diagnosis of faltering growth was recorded in medical notes although concerns about other serious pathologies – space-occupying intracranial lesion, malrotation and metabolic conditions – were also considered. He was reviewed by a dietitian and was commenced on a nutritional supplement that contains higher levels of energy (100kcal per 100mL). Initial nursing care included two-hourly observation including paediatric early warning score, neurological observations, administering nasogastric tube feeds, but this was not tolerated, and strict fluid input/output documentation. Intravenous fluids were necessary for 36 hours.

Blood investigations, including anti-tissue transglutaminase (anti-tTg) and immunoglobin A (IgA) levels, were sent. Abdominal ultrasound scan, barium swallow and meal, and computed tomography (CT) brain scan were reported as normal. Paediatric gastroenterology opinion was sought by the paediatrician and, in the light of the history and

normal blood, including ammonia and radiological investigation results, a diagnosis of coeliac disease was suspected.

He underwent upper gastrointestinal endoscopy and small bowel biopsies the next day while waiting anti-tTG results. Endoscopic appearance revealed flattening of the intestinal mucosa suggestive of coeliac disease and a gluten-free diet was started immediately by the specialist children’s dietitian. A week later, histopathology results confirmed a diagnosis of coeliac disease with an anti-tTG titre of 112 units/mL (normal <10 units/mL).

If anti-tTG titre results were available at initial assessment Tom could have been diagnosed with coeliac disease via the non-biopsy serological pathway (Figure 2). Tom is doing well on a strict gluten-free diet two years after his diagnosis. The anti-tTG titres and growth velocity (currently on the 91st centile) have also normalised.

His older brother, Jack (not his real name) – who was asymptomatic, underwent serological screening with anti-tTG titre which was found to be 74 units/mL. He then had an endoscopy and small bowel biopsies and this confirmed a diagnosis of coeliac disease. He is now following a gluten-free diet. Both brothers remain under follow up with a paediatric gastroenterologist and dietitian. The family has also registered with the charity Coeliac UK to obtain advice and guidance.

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faster diagnosis of coeliac disease via the serological pathway in a selective group of symptomatic children. Coeliac disease cannot be cured and management involves a lifelong strict adherence to a gluten-free diet, which is essential to prevent long-term complications.

subsequently children presenting with malnutrition and/or undernutrition (Rajpoot and Makharia 2013). Nurses should highlight these or similar issues to a paediatric dietitian so that the whole family can receive further education and support.

Children and adolescents may experience low self-esteem due to dietary restrictions identifying them as being different from their peers, and this can negatively affect their adherence to a gluten-free diet. In a questionnaire study of children with coeliac disease, more than one third of participants reported feeling angry ‘always’ or ‘most of the time’ about having to follow a gluten-free diet and nearly 20% reported feeling different from others and were misunderstood because of coeliac disease ‘always’ or ‘most of the time’ (Altobelli et al 2013).

An inpatient admission for a non-coeliac-related issue may be a good time for children’s nurses to identify these psychological issues and highlight the need for psychological support to ensure better adherence to a gluten-free diet.

ConclusionThere is a need for further improved awareness about coeliac disease in children especially among children’s nurses and primary care staff. Wider availability of specific serological screening tests enables earlier identification and specialist referral to confirm a diagnosis of coeliac disease by small bowel biopsy.

The modified ESPGHAN guidelines are expected to streamline the diagnostic process by enabling

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Points for practice

■ Identify asymptomatic children from high-risk groups and highlight the need for serological screening in such children

■ Children who are unwell may need inpatient care, dietary supplements and nasogastric tube feeding

■ Nutritional screening can help identify any signs of malnutrition resulting from non-adherence to a gluten-free diet

■ Ensure parents/carers are given comprehensive information and support about maintaining a gluten-free diet as well as gluten-containing play items

■ Highlight cultural beliefs and dietary practices to dietitians

■ Communicate with community healthcare professionals to ensure that the child receives adequate care and support

■ Report any suspicions of non-adherence of a gluten-free diet to the child’s medical team

■ Children and adolescents may experience low self-esteem and may need additional psychological support Conflict of interest

None declared

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