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Alimentary Pharmacology & Therapeutics

Systematic review: gastro-oesophageal reflux disease and dental


lesions
F. PACE*, S. PALLOTTA*, M. TONINI , N. VAKILà & G. BIANCHI PORRO*

*Division of Gastroenterology, SUMMARY


Department of Clinical Sciences
‘‘L. Sacco’’, University of Milan, Background
Milan;  Department of Physiological
Dental erosion (DE), which is the irreversible loss of tooth substance
and Pharmacological Sciences,
University of Pavia, Pavia, Italy; that does not involve bacteria ranging from a minimal loss of surface
àUniversity of Wisconsin School of enamel to the partial or complete exposure of dentine by a chemical
Medicine and Public Health, Madison, process, is acknowledged as an established extra-oesophageal manifes-
WI and Marquette University College
tation of gastro-oesophageal reflux disease (GERD). However, the real
of Health Sciences, Milwaukee, WI,
USA impact of GERD in the genesis of this lesion remains unclear.

Correspondence to: Aim


Dr F. Pace, Division of To review the existing literature to assess the relationship between DE
Gastroenterology, ‘‘L. Sacco’’
and GERD.
University Hospital, Via G.B. Grassi,
74, 20157 Milan, Italy.
E-mail: fabio.pace@unimi.it
Methods
Studies that assessed the prevalence of DE in individuals with GERD or
vice versa were identified in Medline and the Cochrane Controlled Trials
Publication data
Register via a systematic research strategy.
Submitted 13 February 2008
First decision 11 March 2008
Resubmitted 20 March 2008
Results
Accepted 20 March 2008 Seventeen studies met the selection criteria. Studies, however, differed
Epub OnlineAccepted 27 March 2008 greatly as far as design, population methods of diagnosing GERD, dura-
tion of follow-up and, consequently, findings. The median prevalence of
DE in GERD patients was 24%, with a large range (5–47.5%), and the med-
ian prevalence of GERD in DE adults patients was 32.5% (range: 21–83%)
and in paediatric population 17% (range: 14–87%). Children with GERD
are found by a majority of studies at increased risk of developing DEs in
comparison with healthy subjects, as are intellectually disabled people.

Conclusions
This systematic review shows that there is a strong association between
GERD and DE. The severity of DEs seems to be correlated with the pres-
ence of GERD symptoms, and also, at least in adults, with the severity
of proximal oesophageal or oral exposure to an acidic pH. The inspec-
tion of the oral cavity in search for DEs should become a routine
manoeuvre in patients with GERD.
Aliment Pharmacol Ther 27, 1179–1186

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doi:10.1111/j.1365-2036.2008.03694.x
1180 F . P A C E et al.

between DEs and GERD to define the size of the prob-


INTRODUCTION
lem; (ii) verify the presumed pathophysiology and (iii)
Dental erosion (DE) is presently recognized as an highlight whether particular subgroups of population
important cause of tooth damage both in children and can have an increased risk of DEs as a consequence of
in adults, occurring in a percentage varying from 2% GERD.
of the general population described in the US1 to 5%
reported in Finland.2 It can be defined as the loss of
MATERIALS AND METHODS
tooth substance by a chemical process that does not
involve bacteria, in contrast to carious tooth dam- The Medline database (from January 1966 to Septem-
age.1, 3 In DEs, the extent of damage may range from ber 2007) and the Cochrane Controlled Trials Register
a barely noticeable loss of surface lustre evident on a were searched. The search terms used were: dental ero-
clean, dry enamel to the partial or complete exposure sion AND gastro esophageal reflux OR esophagitis.
of dentine with its characteristic yellow colour through The only limits employed in this search were English
the thinned overlying enamel.1, 3 and Human studies. Review articles using the same
Dental erosion is caused by the presence of intrinsic search terms were also sought to help identify addi-
or extrinsic acid of non-bacterial origin in the mouth, tional original studies. A careful review of references
or by a combination of them.4 Intrinsic sources of acid was conducted of all retrieved articles. Only studies
include vomiting, regurgitation, gastro-oesophageal published in extenso were included. A data extraction
reflux or rumination. Extrinsic sources of acid are form was developed to standardize the methodological
most commonly dietary acids. Medications, in particu- and quantitative information that was extracted from
lar, some asthma drugs, chewable vitamin C tablets or each study (available from authors on request). This
iron tonics, patient’s lifestyle choices such as unusual consisted of: inclusion criteria of patients in the study,
eating and drinking habits, or socio-economic aspects patient setting (gastrointestinal (GI) vs. dentistry clin-
and environment, can also increase the risk of DE, ics, adult vs. children study), diagnosis of GERD (based
particularly in children.5, 6 on symptoms alone, on upper endoscopy and ⁄ or pH
The first modern description of DEs associated with profile as well), study design, sample size, number of
gastro-oesophageal reflux disease (GERD) is due to dropouts, main outcome measures used to assess effi-
Howden,7 in a case report published more than cacy and study conclusion. Each study was reviewed
35 years ago. In recent years, GERD has been at least by two authors.
described as an important aggravating factor of DEs
and DE is now considered a comorbid syndrome with
RESULTS
an established epidemiological association with GERD.
As an example, the recently published Montreal Crite- The search (final date September 2007) resulted in 19
ria, dealing with a global classification of GERD, state: citations, eight of which were reviews. The Cochrane
‘The prevalence of DEs, especially on the lingual and search and the additional search through cross refer-
palatal tooth surfaces, is increased in patients with ences resulted in six more citations. This left a total of
GERD’.8 This statement (statement no. 48) has been 17 eligible studies.9–24 Of these, five concerned the
approved with 98% of agreement among the Montreal children population10, 20–23 and the remaining the
Group panelists and, reportedly, is based on a high adult one;9, 11–19 furthermore, one study24 was con-
level of evidence, possibly the highest level of evi- ducted on a special population, i.e. institutionalized
dence linking GERD with any extra-oesophageal clini- intellectually disabled individuals.
cal manifestation.8 Thus, it is not surprising that some Because of the marked variation in outcome mea-
authors have advocated that the examination of the sures (see Table 1), it was not possible to perform a
oral cavity, in search for ‘atypical’ DEs, should be an formal meta-analysis, that is a statistical pooling of
integral part of the physical examination of the patient results. Instead, the results were analysed in a qualita-
with suspected GERD.9 On the other hand, other tive fashion. In the following paragraphs, we will first
authors have denied, at least in children, that DEs may consider the results of studies conducted on adult pop-
represent a relevant problem in GERD patients.10 ulations and subsequently those studies conducted on
The aim of this systematic review was to: (i) analyse paediatric patients and finally those conducted on spe-
all the published reports dealing with the association cial populations (i.e. intellectually disabled).

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Table 1. Characteristics of studies included in the review

Author (reference) Type of study No. of subjects, type of population Outcome variable

Munoz et al.11 Case–control 181 GERD patients, 72 HC DE: presence, severity, location.
Periodontal lesions.
Moazzez et al.13 Case–control 31 patients with extra-oesophageal GERD, 7 HC Proximal GER extension

Journal compilation ª 2008 Blackwell Publishing Ltd


Gregory-Head et al.14 Cross-sectional 20 patients with DE % of patients with GERD
Schroeder et al.9 Cross-sectional 12 patients with DE, 30 with GERD referred for 24-h pH % DE in GERD, % GERD in DE

ª 2008 The Authors, Aliment Pharmacol Ther 27, 1179–1186


Loffeld15 Retrospective inventory Patients with reflux oesophagitis No dental prosthesis, % damage of incisors
Jarvinen et al.16 Observational 44 patients with GERD ⁄ DU, 48 postcholecystectomy, % DE
17 with GU
Meurman et al.17 Observational 117 patients with GERD % DE
Bartlett et al.12 Observational 36 patients with DE, 10 HC Oesophageal pH profile
Myklebust et al.18 Questionnaire study General population DEs
Dahshan et al.20 Observational 37 children with possible GERD % DE
O’Sullivan et al.10 Observational 53 children with GERD % DEs
Linnett et al.21 Case–control 52 children with GERD history, 52 healthy sibling % DEs
Aine et al.22 Observational 15 children with GERD % DEs
Ersin et al.23 Case–control 38 children with GERD, 42 HC % DEs
Bohmer et al.24 Case–control Intellectually disabled % DEs, pH profile
Oginni et al.19 Case–control 125 GERD patients, 100 HC % DEs
Gudmundsson et al.25 Observational 14 patients with DE referred for dual 24-h pH Oesophageal and oral pH profile

GERD, gastro-oesophageal reflux disease; DE, dental erosion; DU, duodenal ulcer; GU, gastric ulcer; HC, healthy controls; 24-h pH, 24-hour oesophageal
pH-monitoring.
S Y S T E M A T I C R E V I E W : D E N T A L E R O S I O N S A N D G E R D 1181
1182 F . P A C E et al.

where a control group was used, such as, for example,


Studies conducted on adults
the studies by Munoz et al.,11 Bartlett et al.,12 or Jarvi-
Overall, 11 original studies were found;9, 11–19, 25 of nen et al.16 the prevalence of DEs (or the DE score)
these, seven were conducted on GERD patients (see was statistically greater in GERD subjects than in con-
Table 2). Vice versa, studies by Bartlett et al.,12 trols. No data regarding the prevalence of DEs were
Gregory-Head et al.14 and Gudmundsson et al.25 were provided by two studies, namely Moazzez et al.13 and
conducted on patients with DEs, to investigate the Gregory-Head et al.14 In the former, a score was
presence of GERD (Table 3). The study by Myklebust assessed of teeth with palatal tooth wear, where 0 rep-
et al.18 is a questionnaire survey conducted in Norway, resents no damage and four represents pulpal expo-
but information on the dental status were provided by sure: it was found that the proportion of patients with
the personal dentists only for a minority of respon- a score ‡2 was 70.8% vs. 0% in controls, the propor-
dents, and therefore were not included in the further tion of those with score ‡3 was 8.3% vs. 0%, and none
analysis. Finally, the study by Schroeder et al.9 had had a score ‡4 in either group, whereas the pH-moni-
both a dental group, which was screened for GERD, toring found a higher percentage of time spent in dis-
and a gastroenterological group, referred for dental tal oesophagus with pH < 4 in GERD groups only for
evaluation. the supine period. Interestingly, in this study, a signifi-
Dental erosions were found ranging between 5% cant correlation was found between the proportion of
and 47.5%, with a median value of 32.5%, of the the total time with pharyngeal pH below 5.5 and the
GERD patient samples; the greatest prevalence was proportion of teeth with palatal score 2 (r = 0.44) or 3
found in studies defining GERD patients on the basis (r = 0.44), P < 0.01. In the study by Gregory-Head
of symptoms alone,11 whereas the lowest was found in et al.,14 the Tooth Wear Index (TWI) score was
a study using endoscopic criteria.16 In those studies assessed in GERD patients and in controls; it was

No. of patients GERD diagnostic Table 2. Prevalence of dental


Study (reference) with GERD method Prevalence (%) erosions in adults with
GERD (for abbreviations,
Munoz et al.11 181 Symptoms 47.5 see Table 1)
129 24-h pH-metry
78 Endoscopy
Moazzez et al.13 18 ⁄ 31 24-h dual pH-metry Not stated*
Schroeder et al. 20 ⁄ 30 24-h pH-metry 40
(GI group)9
Loffeld 15 293 Endoscopy 32.5
Jarvinen et al.16 35 Endoscopyà 5
Meurman et al.17 117 Symptoms 24
Oginni et al.19 125 Symptoms 16

* A dental erosion score was used: GERD patients higher score then non-GERD.
  Only the incisor teeth status was assessed.
à Endoscopic oesophagitis and duodenal ulcer were grouped together.

No. of patients Table 3. Prevalence of GERD


with dental Prevalence in adults patients with dental
Study (reference) erosions GERD diagnostic method (%) erosions (for abbreviations, see
Table 1)
Bartlett et al.12 36 24-h oesophageal pH-metry 64
Gregory-Head et al.14 20 24-h dual oesophageal pH-metry 50
Gudmundsson et al.25 14 24-h oesophageal pH-metry 21
Schroeder et al. 12 24-h oesophageal pH-metry 83
(dental group)9

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S Y S T E M A T I C R E V I E W : D E N T A L E R O S I O N S A N D G E R D 1183

found that both the overall score and the maxillary In the study by Aine et al.,22 17 children who
and mandibular surfaces of GERD subjects were signif- attended a university hospital paediatric outpatient
icantly higher than those observed in controls: 0.953 clinic for GERD and who were found to have a patho-
vs. 0.298, 0.941 vs. 0.271 and 0.875 vs. 0.326, respec- logical reflux at 24-h oesophageal pH monitoring were
tively (P < 0.005), suggesting that a relationship exists submitted to dental examination, with teeth erosion
between loss of teeth structure, as measured by the scored according to the previously quoted Aine Index
TWI score and the occurrence of GERD. (from 0 to three); no control group was investigated.
Overall, two patients had score 0, two patients score 1,
six patients score 2 and seven patients score 3, sug-
Studies conducted on children (Table 4)
gesting that only a minority of GERD patients had
A total of five studies were found.10, 20–23 In the study intact teeth.
by Dahshan et al.,20 37 children undergoing elective Finally, in the study by Ersin et al.,23 the effects
upper endoscopy for possible GERD were evaluated for were investigated of GERD on DE vs. caries forma-
the presence, severity and pattern of erosion and stage tion, on salivary function and on salivary microbio-
of dentition of teeth. It was found that 24 of them had logical counts. Thirty-eight GERD patients with a
GERD, 20 of whom had DEs as well, 10 with mild ero- mean age of 6 1 ⁄ 2 years and 42 healthy children of
sion (tooth score £1), six with moderate erosion (at the same age and gender and social background
least one tooth scored 2), and four with severe erosion comprised the study group. All subjects answered a
(at least one tooth scored 3) according to the four- detailed frequency questionnaire related to acidic
point score proposed by Aine et al.22 drinks, foods, and sugar consumption and underwent
In the study by O’Sullivan et al.,10 53 children with a clinical dental examination. The caries experience
moderate to severe GERD as defined by pH monitor- of the children was recorded according to World
ing, were examined for DEs. No control group was Health Organization criteria, and erosions were scored
investigated. according to the Eccles and Jenkins grading scale.26
Results showed that the prevalence of DE was low The children were also investigated for stimulated
when compared with the UK National Survey, with salivary flow rate, buffer capacity, and salivary
only nine (17%) of children showing any sign of mutans streptococci (MS), lactobacilli, and yeast colo-
erosion, and of these only one had erosion involving nization. The results of this rather complicated study
dentine. are the following: the prevalence of DE and the sali-
In the study by Linnett et al.,21 52 children with a vary yeast and MS colonization was found to be sig-
‘definitive’ history of GERD underwent a dental exami- nificantly higher in GERD children than in healthy
nation and were compared on an individual basis with subjects (P < .05); the caries experience, salivary flow
a healthy control sibling without GERD symptoms; the rate, buffering capacities of the children, and fre-
prevalence of teeth erosion was found to be statisti- quency of acidic drinks, foods, and sugar consump-
cally higher in GERD subjects (14%) than in controls tion were found to be similar in both groups. The
(10%), P < 0.05. Furthermore, GERD subjects had ero- authors concluded that GERD children were at an
sion in more permanent teeth compared with controls increased risk of developing erosion and caries com-
(4% vs. 0.8%, P < 0.05), and more severe erosions. pared with healthy subjects.23

Table 4. Prevalence of dental erosions in children with GERD (for abbreviations, see Table 1)

Study (reference) No. patients with GERD Age (range) GERD diagnostic method Prevalence (%)

Dahshan et al.20 24 ⁄ 37 2–18 years Endoscopy 83


O’Sullivan et al.10 53 2–16 years 24-h pH-metry 17
Linnett et al.21 52 17 months–12 years Symptoms + histology 14
Aine et al.22 15 22 months–16 years Symptoms 87
Ersin et al.23 38 6.5 years Symptoms NA

NA, not applicable.

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1184 F . P A C E et al.

novel definition and classification of GERD, referred to


Studies conducted on special groups
as the Montreal global classification, strongly suggested
Only one such study was found, dealing with intellec- causality between reflux and cough, laryngitis, asthma,
tually disabled.24 In this study, authors argued that and DEs, although recognizing the rarity of extra-
not only GERD but also vomiting, rumination and oesophageal syndromes occurring in isolation without
regurgitation are conditions more frequently encoun- a concomitant manifestations of the typical oesopha-
tered in the intellectually disabled population. There- geal syndrome. Furthermore, it emphasizes the fact that
fore, they investigated the presence of DEs in these syndromes are usually multifactorial, with GERD
combination with GERD among intellectually disabled acting as one potential aggravating cofactor.8 For other
inhabitants, arbitrarily defined as having an IQ < 50, syndromes, such as sinusitis, pulmonary fibrosis,
taken from three Dutch institutes. In their study, 63 pharyngitis, or recurrent otitis media, the Montreal
individuals randomly selected underwent an oesopha- Working team concluded that adequate evidence of
geal pH test and dental screening, and possible predis- causal linkage is lacking.8 Among the sufficiently
posing and attributable factors were determined. They proven positive associations with GERD, DE was found
defined an abnormal pH level as a pH < 4, >4.5% of to be a clear-cut one. Studies since the early 1970s7
the measured time. Subjects with DEs were compared have highlighted the injurious role of gastro-duodenal
with those without DEs. The results of this study contents in oral soft-tissue pathology as well as DEs.
showed that in 29 of 63 (46.0%) cases, evidence of The studies we have reviewed are based on a hetero-
DEs was found. In 19 of these 29 subjects with ero- geneous definition of GERD, which is, in some cases,
sions (65.5%), GERD was diagnosed, compared with obtained by the demonstration of endoscopic oeso-
nine (26.5%) of 34 subjects without erosions phagitis,11, 15, 16 in others by a pathological pH
(P = 0.04). In the subjects with erosions, mean dura- metry9, 11–14, 25 or by the presence of GERD symp-
tion of pH <4 was 15.6% (range: 0.5–90.5) compared toms.11, 17, 19 They confirm an prevalence of DEs in
with 6.3% (range 0–40.4) in subjects without erosions adult GERD patients, which is, on average, higher
(P = 0.02). An IQ <35 was found to be predisposing (median value 50%) than that observed in the general
(P < 0.001). Authors concluded that, in this population population (Table 2), where it is estimated to be as high
of 63 institutionalized intellectually disabled persons, as 5%.2 As far as the paediatric population is con-
DEs were diagnosed in 46% and that 65% of them had cerned, we found the prevalence extremely variable,
GERD. Individuals with longer duration of pH < 4 than with a range between 13 and 87%, according to the
6.3% of the measured time and with an IQ < 35 were method used to diagnose GERD. Finally, we explored
at higher risk to develop DEs.24 This study shows that the other way round, i.e. the prevalence of GERD in
DEs in the intellectually disabled population might be patients with DEs, and found an observed prevalence
an oral manifestation of GERD. ranging from 21 to 83%, depending on the method
used to diagnose GERD (Table 3). Finally, we found a
study indicating that intellectually disabled people are
DISCUSSION
at particularly high risk for developing DEs.24
The variety of extra-oesophageal manifestations of As far as the third aim of our systematic review is
GERD is incompletely appreciated. This may be concerned, i.e. the pathophysiology of DEs in patients
because of many factors, including the uncertainty in with GERD, a majority of studies here reviewed con-
classification of GERD patients, and in particular, of firm that DEs may be because of acid reflux damage,
patients with typical GERD symptoms but absence of while on the contrary, dental caries appear to be unre-
oesophagitis. lated or conversely related to GERD;11 in one study, it
Consequently, the published estimates of extra- is even suggested that acid reflux may play a role in
oesophageal disorders vary widely27–31 and symptoms preventing the formation of dental caries by inhibiting
other than heartburn and regurgitation are reported in bacterial growth in the mouth.9 In general, DE appears
up to 50% of patients with endoscopically proven to be a multi-factorial phenomenon in which the pro-
reflux oesophagitis.32 Nevertheless, for some of the tective buffering capacity of the oral cavity is over-
proposed associated manifestations, the evidence link- come by either reduced salivary secretion or increased
ing them with GERD is robust, whereas that for the volume of injurious gastric refluxate. Although GERD
other is less impressive. As an example, the recent may have a noxious effect on other oral structures, it

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S Y S T E M A T I C R E V I E W : D E N T A L E R O S I O N S A N D G E R D 1185

appears to be the most prevalent injury.4 The site of bacterial involvement,9 which may be encountered at
teeth involvement may be universal, but the most different stages, from the very early stages, where the
commonly seen damage occurs on the facial, occlusal, only sign may be a barely noticeable loss of surface
and lingual surfaces. The severity of DEs – according lustre evident on a clean, dry enamel to the typical
to the Eccles and Jenkins26 classification – appears to yellowish areas on the surface of the tooth, because
be correlated with the duration and severity of reflux of the exposition of the underlying dentine through
symptoms.17, 19 While a majority of patients (‡60%) the thinned overlying enamel.1 DE predisposes the
with DE and GERD report typical GERD symptoms, no teeth to attrition (flattening of occlusal surface) and
association has been found between severity of reflux abrasion (wearing away of teeth substance), which
symptoms and subjective symptoms in the mouth.17 A can lead to tooth loss, cosmetic disfigurement and
relationship has also been found between the severity altered facial appearance.33
of DEs and the severity of oesophageal acid exposure In conclusion, from a practical point of view, as DE
as measured by pH-metry; in the study by Schroeder is the predominant oral manifestation of GERD and is
et al.9 conducted in adults, the cumulative erosion highly prevalent in the general population, dental
score correlated with proximal upright reflux (r = examination plays an important role in the evaluation
0.55, P < 0.01), but this association was not found in of patients with typical and atypical symptoms of
the study by Munoz et al.11 or not specifically sought GERD and in the above categories of patients. DE
in the study by Moazzez et al.,13 Gregory-Head might be easily diagnosed by primary care physicians
et al.,14 Gudmundsson et al.25 among the studies con- and gastroenterologists who are familiar with its phys-
ducted in adults and by O’Sullivan et al.10 among the ical characteristics. Early diagnosis and suppression of
ones conducted in children. In the study by Bartlett refluxed acid through lifestyle changes and medica-
et al.,12 the relationship was found between percentage tions have been reported to prevent further damage
of time with distal oesophagus pH <4 and oral acid and tooth loss potentially.33 For patients with signs of
exposure time <6 as measured by oral pH-metry, and erosion, a dental referral is appropriate for evaluation
between the latter and the severity of DE. and restoration of lost tooth structure and institution
The injurious effect of acidic juice of extrinsic of preventive dental measures. Thus, not only is it
(citric fruits and acidic beverages) or intrinsic origin important for the dentist to be familiar with and
(gastro-oesophageal reflux (GER)) on the teeth and inquire about typical and atypical reflux symptoms,
oral tissues has been extensively studied.2, 12, 17 The but also the primary care physician and the gastroen-
direct contact of acid is considered to be the main terologist need to pay more attention to the often
mechanism of injury; GER can result in dental injury neglected oral examination.
by the dissolving of the inorganic material of the
teeth (hydroxyapatite crystals in enamel), which
ACKNOWLEDGEMENT
occurs below the critical pH level of 5.5.25 This leads
to DE, an irreversible loss of tooth substance without Declaration of personal and funding interests: None.

4 Lazarchik DA, Filler SJ. Effects of gas- 8 Vakil N, van Zanten SV, Kahrilas P,
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ª 2008 The Authors, Aliment Pharmacol Ther 27, 1179–1186


Journal compilation ª 2008 Blackwell Publishing Ltd

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