The Dental Implications of Gastro-oesophageal Reflux Disease in Children

Gastro-oesophageal reflux (GOR) is the passage of gastric contents into the oesophagus.¹ It is a physiological phenomenon occurring multiple times daily in children and infants, most often resolving spontaneously by the second year of life.² Gastro-oesophageal reflux disease (GORD) is when the reflux of gastric contents causes troublesome symptoms and/or complications.³ First described in the paediatric literature in 1982, and only a few decades later, is now one of the most common causes of foregut symptoms in children.^4,5

The extra-oesophageal manifestations of reflux are often considered separate entities and bear many names, such as extra-oesophageal reflux disease, laryngopharyngeal reflux disease or pharyngeal reflux. However, the extra-oesophageal manifestations are significant because the acidic refluxate, composed of acid, pepsin, bile salts and trypsin, can reach the oral cavity with effects on the hard and soft tissues in the mouth.

References to GORD pertain to GORD in children, unless otherwise specified Prevalence estimates are primarily based on questionnaire studies. They range from 1.8% to 22%, reaching 50% of infants younger than 3 months.^6,7 The incidence of the extra-oesophageal manifestations of GORD in children is poorly established. Many symptoms are non-specific and may be confused with other common childhood illnesses. A recent systematic review indicated a significant global burden, with an estimated 1.03 billion adults experiencing GORD.⁸

Two main hypotheses have been proposed for GORD: reflux (direct contact of aspirated gastric refluxate with the mucosa); and reflex (vagally mediated reflex triggered by acidification of the distal portion of the oesophagus) theories. Studies on twins support the possibility of genetic predisposition, indicating an estimated heritability of 31%.⁹ Also, GORD may have a polygenetic basis owing to its high genetic correlation with Barrett's oesophagus and oesophageal adenocarcinoma.¹⁰ Therefore, despite the several hypotheses, the exact aetiology of the extra-oesophageal manifestations of GORD remains unknown.

Clinical presentation of GORD

The association between pathological GORD and its extra-oesophageal manifestations is increasingly well established (Figure 1). In addition, the physiological GOR and GORD continuum can lead to various systemic manifestations and complications. For example, regurgitation, irritability and vomiting are common in infants with GORD.⁵ Symptoms of GORD in older children and adolescents are similar to adults, and may include heartburn and retrosternal or epigastric pain.

Diagnosis

A thorough history and examination are often essential in most paediatric patients to diagnose GORD and initiate therapy. However, some children with a significant family history, anatomic or developmental issues are at greater risk of developing severe symptoms of GORD, which may present with endoscopic evidence of mucosal breaks in the oesophagus and erosive reflux oesophagitis (Figure 2).¹³ For example, erosive tooth wear (ETW) resulting in pulpal exposure may present in Prader-Willi syndrome.¹⁴ However, ETW is not linearly associated with this condition. Nevertheless, dentists must be vigilant for these red flags predisposing to GORD-related dental complications.

There is no gold-standard test to diagnose GORD in children. The choice of investigation depends on the clinical situation for which it is required and could include endoscopy, barium oesophagram, ambulatory pH monitoring and the proton-pump inhibitor test. The detection of pepsin in the saliva has been proposed as a potentially promising, non-invasive method for diagnosing GORD.¹⁵

Dental implications of GORD and their management

GORD and its treatment can have numerous dental implications manifesting as erosive lesions, salivary changes, bruxism, sleep-disordered breathing, oral mucosal inflammatory changes, and caries (Figure 3).

Dental erosion

Pindborg described dental erosion (DE) as ‘the superficial loss of the hard tissues of the teeth by a chemical process that does not involve the action of bacteria’.¹⁶ Conversely, ETW is defined as tooth wear with DE as the primary aetiological factor.¹⁷ Repeated exposure to gastric acid (with a pH of 1 to 1.5) over a prolonged timeframe favours tooth structure loss via DE or ETW. It is well established that DE is the predominant dental manifestation of GORD.³ A recent systematic review and meta-analysis of 12 studies concluded that children with GORD had a 4.4 times higher risk for enamel erosion and 13.3 times higher risk for DE.¹⁸

The frequency, duration, composition, pH, and form of the refluxate (regurgitation or acidic vapours), along with the saliva's buffering and clearance capacity, mainly influence DE severity. A combination of factors, including the volume, titratable acidity and mineral content of the saliva can lead to the erosive refluxate overwhelming saliva's protective effects, removing dental plaque and salivary pellicle, which makes the tooth surfaces prone to erosion.¹⁹ DE has differing manifestations in the primary and permanent dentitions. Primary teeth are more susceptible to acid attack than permanent teeth owing to their decreased enamel thickness and microhardness. Because of these morphological differences, dentine involvement may occur more rapidly in prolonged GORD, leading to increased pulpal complications.

DE occurs in plaque-free areas where acids have direct access to tooth surfaces. Although, the loss of perikymata is the first sign of erosion, identifying DE in its early stages in primary teeth may be challenging. Initial symptoms include a change from a shiny surface to a dull appearance of enamel which progresses into the involvement of dentine, with concavities and tooth surface loss (Figure 4.) In children with GORD, ETW appears more frequently on the palatal surfaces of maxillary incisors and occlusal surfaces of posterior teeth.^20,21 In cases with dentine exposure, an intact enamel ring may be spared, which remains surrounding the gingival margins of teeth. This has been hypothesized to be due to plaque remnants or neutralization of the acid by gingival crevicular fluid.^22,23 Existing restorations may ‘rise’ above the levels of adjacent tooth surfaces, and at advanced stages, further changes in morphology result in pulpal exposure.

Although low levels of tooth wear in children do not cause a significant impact on their quality of life (QoL), early erosive damage can serve as a risk predictor for potential ETW in permanent teeth. Ganss and co-workers reported that children with DE in the primary dentition exhibited an increased risk of erosive lesions in the permanent dentition.²⁰ In a longitudinal study, Harding et al demonstrated that erosive lesions in the primary dentition, particularly with dentine exposure, were significantly associated with tooth wear on the occlusal surfaces of first permanent molars.²¹

Comorbidities with DE that may complicate the management in patients with GORD include developmental defects of enamel. Kazoullis and co-workers, examined 714 Australian schoolchildren, found that DE was strongly associated with enamel hypoplasia and highlighted the benefits of preventive measures in these patients.²⁴

Saliva

Saliva maintains homeostasis of the oral cavity, with its protective effects extending into the digestive tract. In the mouth, saliva and its components dilute acids, neutralizing and buffering them. Therefore, salivary factors such as flow rates, pH, buffering capacity and the protective effect of the salivary pellicle may change an individual's susceptibility to hard and soft tissue changes in the oral cavity.

Studies have shown contradictory results linking salivary flow, secretory function, and volume abnormalities with symptoms of GORD.^25,26,27 For example, Meurman et al observed no significant differences in salivary parameters in 117 patients with GORD.²⁵ However, in another case-controlled study of 120 GORD patients, significant differences in the secretory function of the salivary glands and increased reported xerostomia were observed.²⁶ Other studies have found reductions in salivary flow volume and swallowing function in GORD-affected patients compared to healthy controls.²⁷

Conversely, a sudden increased salivation in response to heartburn symptoms, also known as ‘water brash’, is well acknowledged.²⁸ In infants and children, this may manifest as excessive hypersalivation or drooling. Although problematic for the parent or patient, it is a beneficial symptom inducing adequate salivary secretory response and allowing the acidic pH to neutralize.

There is a significantly higher level of abnormal reflux activity in children with cerebral palsy than in control subjects.²⁹ Although more commonly associated with swallowing dysfunction and inadequate lip closure, GORD has been linked as an indirect cause of prolonged drooling in children with cerebral palsy and other neurological impairments. Treatment options include pharmacological and surgical interventions. However, functional appliance therapy using intra-oral stimulating plates has successfully managed drooling in children with cerebral palsy.³⁰

Bruxism and sleep-disordered breathing

GORD and bruxism can contribute to ETW. Sleep bruxism is a common disorder in children, and evidence supports a bidirectional relationship with GORD.³¹ Although the aetiology of bruxism is complex and unclear, it may involve both the central and autonomic nervous systems. In addition, the acidic refluxate may reduce the pH of the oesophagus and increase the rhythmic masticatory muscle activity and nocturnal bruxism in adults.³² Nonetheless, this association is yet to be confirmed in children.

Because sleep-disordered breathing and GORD are common childhood disorders, it remains unclear whether a contributory relationship exists between them or if the processes share common risk factors. However, in adults, the treatment of GORD improves obstructive sleep apnoea (OSA), and OSA therapy via continuous positive airway pressure (C-PAP) reduces GORD, demonstrating an association between the conditions.^33,34 Similarly, in infants, apnoea-related issues improve after successful treatment of GORD.³⁵

Oral mucosal lesions

Although oral mucosal changes may result from GORD, they are not pathognomonic. Also, little is known concerning its effect on the oral mucosa, especially in children. Acid refluxate may exacerbate oral mucosal changes associated with concurrent hyposalivation, which could arise from associated systemic conditions or intake of drugs, including proton pump inhibitors.

A retrospective study of 105 adult patients with GORD found an association with oral soft tissue inflammatory lesions.²⁷ Similarly, in a case-controlled study of 200 adult GORD-affected patients, a significant association was noted with erythema of the mucosa of the palate and uvula.³⁶ In children, changes in the mucosa of the upper aerodigestive tract can be detected with a fibre-optic examination.³⁷ Histological analysis of these regions show epithelial atrophy and increased fibroblasts in the palatal mucosa.³⁸

Caries

There are conflicting results and a need for more information on children's caries experience with GORD, possibly due to the small sample numbers in the studies. Although an acidic oral environment is conducive to the growth of aciduric bacteria, severe acidity can also reduce bacterial growth. Linnett and co-workers reported a higher prevalence of caries experience in children with GORD than in healthy controls.³⁹ Conversely, Ersin and co-workers did not confirm this observation in their study.⁴⁰

Sequelae

ETW can lead to various consequences, resulting in pain, infection, and subsequent tooth loss, which may adversely affect individual QoL (Figure 5).⁴¹ It is essential to provide patients exhibiting these consequences with appropriate management to avoid adverse effects on their QoL.

Management

Several clinical guidelines, namely NICE, are available for managing GORD in children.⁴² The primary focus in managing the dental implications of GORD is preventing and reducing irreversible tooth loss. Therefore, it is prudent to ensure that children with GORD have a regular dental assessment with preventive dental measures to limit damage to their dentition. In addition, dentists should be aware of the ‘red flags’ (Figure 2) predisposing to severe GORD in children because it will facilitate a timely referral and appropriate interventions.

For ETW, a risk-based management strategy is illustrated in Figure 6, showing the various at-home and in-office options. Bruxism management is not evidence-based but eminence-based owing to the lack of published studies and a scarcity of available data on a limited number of patients.⁴³ Behavioural strategies, including biofeedback, relaxation and improvement of sleep hygiene, have been described in the literature. Sleep hygiene is intended to manage conditions influencing sleep, including behaviours conducive to proper sleep, such as adequate sleep and wake schedules, environments, and physiological practices that aid sleep. Nevertheless, oral appliances are commonly not indicated in primary dentition. Children with sleep-disordered breathing may benefit from an ear, nose and throat specialist referral for airway assessment and appropriate management. If GORD-related soft tissue changes exist within the oral cavity, conservative management with regular dental surveillance and monitoring is warranted.

Monitoring

Clinical photographs, digital intra-oral scanning and diagnostic models can aid in monitoring the progression of ETW. Eccles and Jenkins developed a range of indices to measure ETW.⁴⁴ However, many need to reflect morphological defects adequately, allow comparison of results, and lack inter-national validation. Therefore, a simple universal scoring system, the Basic Erosive Wear Examination (BEWE) index, is increasingly used to assess the severity and progress of ETW.⁴⁵ It consists of a sextant-based examination where the tooth surface with the worst wear in each sextant is graded, resulting in a cumulative score that aids the decision-making process for the management of ETW. Although clinical guidelines according to BEWE scores are based on the adult population, in children, it is recommended that the cumulative score of all sextants is lowered, with recall intervals decreased to between 6 and 12 months dependent on the child's level of risk.⁴⁶

Oral hygiene

Toothbrushing has been linked to ETW. Once an acidic challenge softens the tooth structure, it may be more prone to the abrasive effects of a toothbrush. Therefore, avoiding toothbrushing immediately after an erosive challenge has been recommended to prevent ETW. However, saliva does not remineralize softened enamel over a short time frame and may suffer mineral loss even without tooth brushing. Nevertheless, based on a case-controlled study of 300 adults, there are suggestions to advise patients not to brush within 10 minutes after an acidic episode.⁴⁷ In addition, based on in vitro studies, it has been advocated that patients at risk of DE use low-abrasive dentifrices.⁴⁸

Remineralization

Traditional fluoride formulations such as sodium and amine fluorides in low–medium concentrations at neutral pH have limited anti-erosion effects.⁴⁹ However, adding polyvalent metal ions such as stannous and titanium ions to fluoride allows the formation of a metal-rich surface coating, with increased fluoride uptake and higher resistance to acids. Therefore, high-concentration, acidic fluoride formulations provide a higher benefit level, with the best evidence for effectiveness available for stannous fluoride formulations.⁴⁹ Chitosan (cationic polysaccharide) also increases enamel's protective effects by forming a protective layer against erosive challenges. Furthermore, a stannous chitosan formulation appears more effective than a corresponding sodium fluoride formulation.⁵⁰ Hence, fluoridated toothpaste containing stannous fluoride (with additives like chitosan) should be a preventive strategy based on the child's risk factors.

Remineralizing agents such as casein-phosphopeptide–amorphous calcium phosphate (CPP-ACP) can also be considered. There are mixed results from in vitro studies regarding the remineralization potential against erosive challenges.^51,52 It may have a protective effect against acidic challenges based on limited studies. However, it appears less effective than fluoride in controlling DE. Alternatively, high-concentration fluoride gels and varnishes may be applied. Yet, in patients with increased frequency of acid exposure, the protection offered by these fluoride forms may be of short duration, requiring frequent application. The protective effect caused by fluoride varnishes is due to the mechanical barrier imparted on the tooth surfaces.⁵³ This temporary mechanical barrier may not be a long-lasting preventive measure, particularly for primary teeth. Nonetheless, it may provide some desensitizing relief over short periods. Therefore, light-curable fluoride varnishes may be a reasonable alternative.⁵⁴ Nonetheless, clinical evidence to support these products' efficacy against erosion is limited.

Performing sodium bicarbonate rinsing after acidic challenge is recommended to neutralize acids within the oral cavity. Although it may minimize the effects of an immediate acid challenge, it does not remain in the mouth to protect against future erosive episodes.⁵⁵ In a study of 31 adults, chewing sugar-free gum after a meal reduced postprandial reflux.⁵⁶ This non-pharmacological option may be suitable for older children with GORD. In cases of xerostomia and salivary hypofunction, treatment strategies aim to increase hydration using mucosal lubricants and saliva substitutes and avoid irritating dentifrices in severe cases. Furthermore, modifying acid-resistant proteins within the acquired pellicle may have a role in preventing erosion. Using ‘acquired pellicle engineering’, sugar-cane cystatin has been shown to adhere to the enamel and protect against initial and prolonged erosion.^57,58 Although additional research is required, particularly for primary teeth, these findings open a future avenue for preventive approaches against ETW.

Restorative treatment

Restorative treatment is generally not indicated in the primary dentition unless there is evidence of exposed dentine, hypersensitivity, or pulpal exposure. Therefore, early diagnosis of ETW is essential for minimally invasive treatment approaches. For example, sealants, varnishes, or dentine bonding agents can create a physical barrier between the teeth and erosive refluxate. Glass ionomer cement may have reduced efficacy in GORD-affected children as they are susceptible to acid dissolution. However, resin-based fissure sealants or dentine bonding agents applied to the surface of eroded dentine mitigate the progression of ETW.^59,60 Exposed dentine surfaces should be cleaned with a pumice slurry or a slow speed before etching to allow removal of the salivary pellicle and enhance bonding to sclerotic dentine.

Full coverage restorations restore lost tooth structure to maintain pulpal vitality and minimize sensitivity. Nevertheless, tooth extractions may be required in severe ETW with pulpal exposure and infection. Although preventive measures minimize dental treatment, extensive dental treatment for younger children may need treatment under general anaesthesia. Alternatively, biological management of ETW can be through placing stainless steel crowns using the Hall technique on the primary molars. This approach has been increasingly used to manage caries in the primary dentition.⁶¹

Conclusion

GORD is a common disorder in children with a range of extra-oesophageal effects that require dental practitioners' awareness. Despite the high risk of bias among published studies and conflicting evidence, a potential causative link exists between GORD and its dental manifestations. Therefore, failure to recognize the ‘red flags’ or diagnose dental consequences of GORD can result in potentially negative outcomes, reducing the individual's oral health-related QoL. The proposed risk-based management system and interprofessional collaboration can guide clinicians in managing the dental effects in both primary and permanent dentitions.