Oral manifestations of gastroesophageal reflux disease

Authors

  • Sarbin Ranjitkar,

    Corresponding author
    1. School of Dentistry, The University of Adelaide, Adelaide, South Australia, Australia
      Dr Sarbin Ranjitkar, School of Dentistry, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia. Email: sarbin.ranjitkar@adelaide.edu.au
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  • Roger J. Smales,

    1. School of Dentistry, The University of Adelaide, Adelaide, South Australia, Australia
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  • John A. Kaidonis

    1. School of Dentistry, The University of Adelaide, Adelaide, South Australia, Australia
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  • Conflict of interest: None.

Dr Sarbin Ranjitkar, School of Dentistry, The University of Adelaide, North Terrace, Adelaide, SA 5005, Australia. Email: sarbin.ranjitkar@adelaide.edu.au

Abstract

Numerous case-control and other studies involving confirmation of gastroesophageal reflux disease (GERD) by esophageal pH-metry and the assessment of dental erosions have shown significant associations between the two conditions in both adults and children. By contrast, when asked to vote on whether GERD may cause dental erosions, only 42% of physicians strongly agreed that such an association existed in adults, and just 12.5% strongly agreed for children, respectively in two global consensus reports. Part of this divergence between the perceptions of physicians and the findings of research publications may reflect a general lack of oral health education during medical training, and cursory oral examinations being made under less-than-ideal conditions. Adequate salivary secretions are essential for the protection of the teeth and the oropharyngeal and esophageal mucosa. The quantity and quality of the saliva require monitoring as many drugs, including several of the proton pump inhibitors (PPIs), can cause hyposalivation. In addition, PPIs do not always result in adequate acid suppression. Therefore, collaboration between physicians and dentists is strongly advocated to prevent or ameliorate possible adverse oral effects from both endogenous and exogenous acids, and to promote adequate saliva production in patients with GERD.

Introduction

There is relatively little information in general medical and gastroenterology literature regarding tooth erosion that may be associated with gastroesophageal reflux disease (GERD). This association is commonly observed by dentists, but is given very cursory mention or omitted entirely when describing extra-esophageal (supra-esophageal) manifestations of GERD.1–7

When 44 medical experts and family physicians from 18 countries voted in the World Congress of Gastroenterology presentation in Montreal on the statement that “The prevalence of dental erosions, especially on the lingual and palatal tooth surfaces, is increased in patients with GERD” (Extra-esophageal Syndromes: Established Associations, Statement #48), the result was a high-grade consensus agreement of 96%.8 However, only 42% of the consensus votes “agreed strongly” with the above statement, 35% “agreed with minor reservations,” and 19% “agreed with major reservations.” Just three selected clinical studies were quoted to support the statement.9–11

Subsequently, when eight pediatric gastroenterologists using a revision of the original Montreal presentation protocol voted on the statement that “GERD may cause dental erosions in pediatric patients” (Extraesophgeal Syndromes: Definite Associations, Statement #53), the result was a low-grade consensus agreement of 100%.12 But, only 12.5% of the votes “agreed strongly,” 37.5% “agreed moderately,” and 50% “just agreed.” One systematic review article13 and four other selected clinical articles14–17 were quoted to support the above statement. Dental erosion was only one of two extra-esophageal conditions considered to be definitely associated with GERD in pediatric patients, the other being Sandifer's syndrome (torticollis).12

In the two previous global consensus reports,8,12 the relatively low percentages of physicians' votes agreeing strongly that GERD may cause tooth erosion in both adults and children is possibly a reflection of a lack of oral health training. One random survey involving 611 graduating pediatric residents found that most received either no training or less than 3 h of oral health training, with only 14% spending clinical observation time with a dentist.18 A national survey of pediatricians also found that only 54% examined the teeth of more than half of their 0–3-year-old patients. Fewer than 25% of these pediatricians had received any oral health education at all during their career.19 In both surveys, most of the pediatricians stated that they should be trained to undertake basic oral health screenings. Compounding this problem, another questionnaire survey found that only three of 104 pediatricians were aware of tooth erosion caused by acidic pediatric medications.20 A recent review article concluded that, “the primary care physician and the gastroenterologist need to pay more attention to the often neglected oral examination.”13

Tooth erosion is usually a slow process occurring over many years, and its subtle appearance is often not adequately observed during a cursory examination under less-than-ideal conditions. It is not surprising that advanced erosive tooth wear is usually detected only after significant damage has occurred to the dentition and the masticatory system.21 Therefore, the diagnosis and preventive management of early stages of erosive tooth wear should be a key step to avoiding a lifetime of debilitating dentition and complex restorative therapy.22 It should also be realized that expensive and extensive treatment for advanced erosive tooth wear can fail catastrophically and may need long-term maintenance.

Tooth wear is a multifactorial condition caused by tooth grinding, abrasion from coarse food or objects, exogenous erosion (e.g. dietary acids and acidic medications) and endogenous erosion (e.g. gastric regurgitation and vomiting). It is beyond the scope of this article to conduct a detailed review of all these wear processes. Therefore, we have focused on issues relating to endogenous erosion associated with GERD (gastric regurgitation). Specifically, these issues include the oral manifestations of GERD, the occurrence of gastric regurgitation with tooth grinding, the oral defense system including salivary protection, and the collaborative medical and dental management.

Oral manifestations attributed to GERD

The principal difficulty with investigating the links between GERD and its possible oral manifestations in humans has been the need to subject them to unacceptable invasive investigative procedures and to withhold any required treatments during long-term prospective studies. Therefore, the principal evidence for such links has been from studies of patients with confirmed GERD who are then found to have tooth erosion, and vice versa.

The most commonly described oral manifestation attributed to GERD (and other causes of stomach contents reaching the mouth), is tooth erosion, which has been widely investigated and reported in dental literature9–11,13–17,23–30 These mainly case-control studies reported that GERD was associated with at least 20–30% of patients with tooth erosion. The majority of clinical studies of tooth erosion with confirmed evidence of GERD (using esophageal endoscopy and pH-metry), have also found similar significant associations between tooth erosion and GERD.9,11,15,17,23–25,30,31 Using optical coherence tomography, a 3-week randomized, double-blind and prospective clinical trial of 29 patients with confirmed GERD reported significantly less enamel erosion in the esomeprazole-treated group than in a placebo group.29 However, several clinical studies have not found significant associations,16,28,32 although one of these studies reported a strong association with other oral manifestations of GERD in the form of burning mucosal sensation, halitosis and mucosal erythema.28 In another study, up to 25% of individuals with tooth erosions and confirmed GERD had silent regurgitation.23 It should be appreciated that a loss of tooth substance is usually only readily observed after a long period of endogenous acid contact and, therefore, early signs of erosion may be easily overlooked.

Because of the large number of persons with undiagnosed GERD are “silent refluxers,”33,34 dentists may be the first to suspect the presence of this potentially serious condition from their observations of otherwise unexplained dental erosion.23 Apart from tooth erosion, the surfaces of glass-ionomer and ceramic dental restorative materials that contain a matrix of glass particles also may be damaged by acids to varying extents. In addition, persons with GERD may complain of a sour or acidic taste, impaired taste (dysgeusia), an oral burning sensation and water brash (flooding of the mouth with saliva in response to an esophageal reflux stimulus). However, oral mucosal changes that may be associated with GERD are described far less frequently.28,35

Tooth erosion (corrosion)

Dental erosion or, more correctly, dental corrosion is described as tooth surface loss produced by chemical or electrolytic processes of non-bacterial origin, which usually involves acids.36 The acids are of endogenous (intrinsic) origin from regurgitated gastric juices and of exogenous (extrinsic) origin from usually dietary, medicinal, occupational and recreational sources. Tooth erosion is highly unlikely to be caused by alkaline bile juices from duodenogastroesophageal regurgitation (DGER).37 The majority of extraesophageal symptoms are more likely to be associated with acid regurgitation than DGER. Acid regurgitation has been implicated as the major factor, even in patients suffering from refractory GERD to proton pump inhibitor (PPI) therapy,38 contrary to previous beliefs about the role of DGER.39

The potential for tooth erosion from gastric contents is modified by many secondary factors. Gastric acid has a pH of approximately 1.2, but the regurgitated gastric contents may also contain varying amounts of partly digested foodstuffs and pepsin, as well as bile acids and the pancreatic enzyme trypsin when there is an accompanying duodenal regurgitation.27 Antacid medications reduce the acidity of the gastric contents, and proton pump inhibitor (PPI) medications decrease the acid output. Therefore, the potential for tooth erosion will vary, and will be modified by factors such as the composition and pH of the refluxate, the frequency and the form it reaches the mouth (regurgitation or belching of acidic vapors), the flow rate and buffering (bicarbonate ion) capacity of stimulated saliva and the duration for clearance from the mouth, and whether patients brush the softened tooth surfaces immediately after regurgitation episodes. The “critical pH” for demineralization of enamel is approximately 5.5 (and even higher for dentin), which may readily be exceeded by the regurgitated gastric contents.

The detection of the early stages of tooth erosion requires adequate isolation of dried tooth surfaces and retraction of oral soft tissues, good lighting and a small mouth mirror. The affected enamel appears smoothly glazed or “silky” with rounded surfaces, which may appear very clean because of the removal of stains, dental plaque and acquired dental pellicle by the gastric juices (Fig. 1). Other characteristic features of erosion lesions include enamel thinning leading to an increased incisal and proximal translucency (Fig. 2a), and a yellowish appearance of the teeth from “shine-through” of the underlying dentin (Fig. 2b). Subsequent erosion of the less-mineralized dentin results in more rapid occlusal “cupping” of posterior cusp tips and anterior incisal edges. The thin unsupported enamel breaks off to leave jagged edges. During active erosion the exposed dentin may become very sensitive to temperature changes (e.g. hot and cold stimuli) and touch (e.g. tooth brushing). The rate of tooth erosion may be exacerbated by superimposed mechanical wear processes (referred to as “erosive tooth wear”) and by exogenous acid sources.40 Mechanical tooth wear can occur from both tooth grinding and mastication occlusally, and from toothbrush abrasion cervically, whereas exogenous acids produce a more generalized pattern of tooth substance loss.40 Each of these wear processes has a specific wear pattern that can be generally identified at both macroscopic and microscopic levels.

Figure 1.

(a) Early erosion lesion has a clean and smoothly glazed appearance, with loss of surface morphology (i.e. grooves and pits) as a result of acid dissolution. (b) Non-eroded teeth showing the presence of pronounced occlusal fissures towards the centre of the teeth.

Figure 2.

(a) Broad shallow erosion with thinning of the enamel has resulted in an increased translucency of the incisal region of the anterior maxillary central incisors, associated with increased grayness (Courtesy Dr A. Dickson). (b) The thinner enamel in the cervical regions (around the neck) of the teeth has been eroded to varying degrees, accentuating the yellow appearance of the underlying dentin. (c) Erosion has resulted in the loss of palatal and incisal enamel of the maxillary incisors. (d) Long-standing erosion has caused severe loss of occlusal enamel and dentin of lower molar teeth, resulting in cupping of these teeth. For example there is a severe cupping of the occlusal surface of the mandibular first molar tooth adjacent to the resin composite restoration (black arrow).

Classically, tooth erosion from acid regurgitation involves the loss of enamel and dentin from initially the palatal surfaces of the maxillary teeth, taking several years to become clinically obvious (Fig. 2c). In long-standing instances, erosion can also affect the occlusal and other surfaces of maxillary teeth as well as mandibular teeth (Fig. 2d). Existing non-eroded restorations appear raised above the adjacent eroded tooth surfaces. The pattern of erosion is affected by the presence and distribution of oral biofilm (dental plaque), the quantity and quality of saliva (which is protective of the mandibular anterior teeth in particular), the number and position of the teeth, and other conditions (such as mouth breathing associated with incompetent lips, facial paralysis and major salivary gland pathology).

Oral mucosal lesions

Oral mucosal lesions may result from GERD by direct acid or acidic vapor contact in the oral cavity. However, there is a paucity of information on the effect of GERD on oral mucosal changes. One large case-controlled study observed a significant association of GERD with erythema of the palatal mucosa and uvula.28 And, a histologic examination of palatal mucosa found a greater prevalence of epithelial atrophy, deepening of epithelial crests in connective tissue and a higher prevalence of fibroblasts in 31 GERD patients compared with 14 control subjects.35 But, these changes were not visible to the naked eye, unlike the mucosal changes that may be more readily observed in esophagitis and laryngitis where the pH of the gastric refluxate at these sites is lower than in the mouth.23,25 Other studies have not found any abnormal appearances of the oral mucosa or associated oral symptoms in patients with confirmed GERD.41,42 However, acid regurgitation may exacerbate oral mucosal changes associated with co-existing hyposalivation, which can arise from systemic conditions, local salivary gland conditions and intake of drugs including PPIs.

Sleep bruxism and GERD

Bruxism (tooth grinding or clenching) is defined as contact of teeth for reasons other than eating and is a common cause of tooth wear in humans.43 It can occur both during the awake state as tooth clenching, and during sleep as tooth grinding or clenching.44 Sleep bruxism sounds or noises are often reported by partners or parents, although bruxism may also occur in silence.45 Some researchers have described bruxism as a sleep-related stereotyped movement disorder,46 and a “devastating” parafunctional habit, because of its association with undesirable dental restorative treatment failures47 and, possibly, temporomandibular pain and dysfunction.48 However, leading experts now describe sleep bruxism as an asymptomatic occurrence in the majority of healthy individuals rather than a pathological condition, raising doubt over its generic classification as a sleep disorder.45

Previous sleep studies support the notion that sleep bruxism is an exaggerated form of oromotor activity associated with sleep microarousal49 and the swallowing of stimulated saliva production.50 Oromotor movements and the significance of saliva during sleep have been reviewed previously.51 Though the etiology of sleep bruxism is poorly understood, it is believed to involve the central and autonomic nervous systems rather than peripheral sensory mechanisms from the orofacial region.44,52 There is a large variation in the occurrence of bruxism episodes during different stages of sleep, with some reports showing its occurrence predominantly during the rapid eye movement (REM) stage while others describing its occurrence during both REM and non-REM stages.53,54 By comparison, gastric regurgitation episodes in individuals suffering from reflux esophagitis have been noted to occur more frequently during non-REM sleep.55

Given the physiology of both sleep bruxism and GERD, it is possible that these conditions may occur concurrently in some individuals. Randomized clinical trials have established a highly significant relationship between sleep bruxism and experimental intraesophageal acidification,56 and between sleep bruxism and physiologic gastroesophageal reflux episodes.57 However, we are unaware of any sleep studies that have investigated associations between sleep bruxism and GERD. The current understanding of this relationship has been extrapolated from the findings of a few case reports and observational epidemiological studies reporting the association between GERD and tooth wear.27 Clinically, it is not unusual for patients with a history of both sleep bruxism and GERD to present with advanced tooth wear, which requires extensive treatment.58 Experimental findings support these observations and indicate that tooth wear under simulated bruxism and gastric acid conditions can occur at an alarming rate.59 While these findings point to the need for early preventive strategies, further research is also required to gain an insight into the relationships between GERD, various oromotor movements, and salivary gland secretions during the different stages of sleep.

The essential roles of saliva

Earlier studies of persons with and without GERD reported an absence of significant differences in stimulated salivary flow rates,35,60,61 buffering capacities and pH values.35,60 However, more recent studies have found a significant association between GERD, hyposalivation and the subjective sensation of “dry mouth” (xerostomia), which is frequently associated with an oral burning sensation.28,62

Though mixed saliva secretions consist of more than 99% water, numerous other variable and complex interacting components also are responsible for the normal functioning and protection of the oropharynx and esophagus. Saliva coats all of the relevant internal anatomical surfaces with mucin-rich secretions, providing a protective diffusion barrier or pellicle against mechanical, thermal, chemical and microbial damage. Saliva also lubricates these surfaces to allow efficient mastication, swallowing and speech. In response to various stimuli, a rapid increase in parotid gland serous secretions containing a high concentration of bicarbonate ions in particular dilutes, neutralizes and clears harmful oral material and acidic esophageal contents by either spitting, or swallowing to induce esophageal peristalsis.

Varying degrees of hyposalivation may result in complaints of xerostomia and an oral burning sensation,62 as well as other common symptoms and signs such as impaired mastication, swallowing and speech, a painful mouth and throat, tooth sensitivity, difficulties in wearing dentures, cracked lips and angular cheilitis, and the frequent need to sip water and chew gum or candies. Furthermore, hyposalivation reduces the potential for saliva to buffer (neutralize) esophageal acid from GERD, resulting in esophageal mucosal damage (reflux esophagitis).63

A subjective assessment of the quantity and quality of the salivary secretions in the mouth should be determined. Scanty unstimulated (resting) saliva may appear foamy and bubbly or, less often, viscous and stringy. After gently blotting the surface of the everted lower lip, seromucous globules of unstimulated saliva from the minor labial glands will take longer than one minute to appear.64

Because acidic and proteolytic stomach contents may readily overwhelm the protective functions of the saliva, resulting in the removal of dental plaque and acquired pellicle from tooth surfaces, the teeth are then very susceptible to demineralization and abrasion. Saliva is readily displaced by acids,65 with the dissolution products of the hydroxyapatite crystals being lost permanently from the exposed tooth surface (Fig. 3).

Figure 3.

When dental pellicle is removed by sustained endogenous acid attacks, demineralized tooth products are lost into the oral environment. HA, hydroxyapatite. (Amended Figure 2.5, pp. 15, from Smales et al.72 With copyright permission from Jaypee Medical Publishers 2011.)

Collaborative medical and dental management

The prevention by physicians of chronic acid regurgitation is required to halt its potential for tooth erosion. A recent Cochrane review found that both PPIs and H2RAs were effective in short-term heartburn remissions (over a period of 2–8 weeks) in adult GERD patients, but PPIs were the most effective.66 However, PPIs were not effective in relieving GERD symptoms in infants, and controlled trials in older children were lacking.67 Another review article found that the effectiveness of PPIs in relieving regurgitation symptoms in adults was modest and lower than that for heartburn, pointing to the need for a more effective treatment.68 This finding is supported by another Cochrane review confirming the more effective relief of symptoms (heartburn, reflux and bloating) by surgical intervention (laparoscopic fundoplication) compared with pharmacologic management, although surgical intervention carries the risk of rare but serious complications.69 With the recent development of novel techniques for the diagnosis and management of GERD, researchers are now realizing the true complexity of the GERD diagnosis, and the much lower effectiveness of PPIs in adults than was originally believed.70 Thus, the complete cessation of nocturnal acid regurgitation in particular may be difficult to achieve by pharmacologic treatment.

Salivary flow rates are usually reduced considerably while asleep,71 and several of the drugs commonly prescribed for GERD and other extra-esophageal conditions may lead to a further reduction in the quantity and quality of stimulated salivary secretions.62,73 Physicians should be aware of any drugs or medicines consumed by patients that may cause or exacerbate hyposalivation and lead to xerostomia. In some instances, saliva substitutes may be prescribed or recommended.

Patients often consume many exogenous dietary acids, which will exacerbate any tooth erosion associated with acid regurgitation. Patients with xerostomia may eat acidic fruits, chew or suck acidic sour-tasting candies and gums, use citric acid candy sprays, and rinse their mouths with acidic cola-type beverages to stimulate saliva production and to remove the remnants and taste of regurgitated stomach contents. Patients should be advised to avoid such acidic foods and beverages and instead rinse their mouths either with water, milk, sodium bicarbonate solutions or sodium fluoride mouth rinses. Tooth brushing and chewing hard foods and sugar-free gums should be avoided for approximately 2 h after a regurgitation episode to allow for the re-establishment of salivary pellicle and subsequent tooth surface remineralization. Recurrent acid regurgitation and partial remineralization of exposed root surfaces of maxillary posterior teeth, particularly in older persons, may result in dark, softened, sensitive dentin that is susceptible to abrasion. Tooth brushing should be done carefully, using a soft multitufted tooth brush and a low-abrasive high sodium fluoride-containing dentifrice.

Patients with GERD should be referred for dental consultations for the collaborative management of any associated oral manifestations. Erosive tooth wear may be accelerated by parafunctional habits and abrasive diets, and wear rates should be monitored periodically to evaluate tooth wear progression. Prevention of further tooth wear is a priority involving local preventive, restorative and maintenance phases.74 Preventive measures may involve the stimulation or substitution of salivary secretions (after assessing their quantity and quality), neutralizing the effects of endogenous and exogenous acids, reducing tooth sensitivity, providing dietary advice (regarding dental erosion, dental caries and oral mucosal sensitivity), enhancing tooth surface integrity (using acidulated phosphate fluoride, metallic ions), and placing adhesive physical barriers on susceptible tooth surfaces.58 Oral discomfort and malodor caused by xerostomia should be alleviated both by home and professional dental care. The importance of adequate fluid intake should be reinforced in GERD sufferers, especially in the elderly living in hot and dry conditions. As saliva flow decreases during sleep, a humidifier may be required to relieve symptoms of sleep-related xerostomia.58

Conclusions

According to many research publications, the association of tooth erosion and GERD is stronger than generally perceived by physicians. Tooth erosion usually progresses slowly, and its signs are often subtle and not readily observed during a cursory oral examination under less-than-ideal conditions. Failure to diagnose early signs of erosive tooth wear can result in significant damage to the dentition and the masticatory system before treatment is sought. Therefore, early diagnosis and preventive management is important to prevent a lifetime of debilitating dentition and the need for complex restorative therapy. Preventive management should involve restoration of the host defense, including salivary parameters. The quality and quantity of saliva should also be monitored by physicians during treatment of GERD with PPIs. Collaboration between physicians and dentists during the management of patients with GERD is also strongly advocated.

Acknowledgment

We gratefully acknowledge financial assistance from the Australian Dental Research Foundation and Dentsply Australia Pty Ltd in support of our research projects on dental erosion.

Ancillary