anbari2018

Received: 1 August 2018
|
Revised: 9 October 2018
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Accepted: 10 October 2018
DOI: 10.1111/hel.12556
ORIGINAL ARTICLE
Halitosis: Helicobacter pylori or oral factors
Fahimeh Anbari1
| Anahita Ashouri Moghaddam2 | Elham Sabeti3 |
Azin Khodabakhshi1
1
Oral Medicine Department, School of
Dentistry, Shahid Beheshti University of
Medical Sciences, Tehran, Iran
2
Periodontics Department, School of
Dentistry, Guilan University of Medical
Sciences, Rasht, Iran
3
Private Practice, Karaj, Iran
Correspondence
Azin Khodabakhshi, Oral Medicine
Department, School of Dentistry, Shahid
Beheshti University of Medical Sciences,
Tehran, Iran.
Email: [email protected]
Abstract
Introduction: Halitosis is a common complaint among people which has various so‐
cioeconomic effects. The prevalence of halitosis includes a variety of 22% up to 50%
in different societies. According to studies, there have been reports of remarkable
improvements in halitosis after Helicobacter pylori eradication treatment. In studies
on the relationship between H. Pylori and halitosis, the role of oral factors as the most
important cause of halitosis has been neglected. This study was conducted with the
aim of investigating the effect of oral factors on halitosis in patients with H. Pylori.
Materials and Methods: A total of 100 dyspeptic patients who had H. pylori‐positive
serologic test were examined by an organoleptic method for the presence of halito‐
sis. DMFT index was used in order to record the dental status. Oral hygiene was
evaluated using the simplified oral hygiene index (OHI‐S).
Results: The mean DMFT index was 9.09 ± 3.97. The score of simplified oral hygiene
index was 1.79 ± 0.949. There was a direct and significant relationship between hali‐
tosis with DMFT, OHI‐S (P < 0.01). There was no significant relationship between
halitosis and coated tongue (P > 0.01).
Conclusions: According to the results of this study, there is a relation between oral
factors and halitosis in patients with positive H. pylori test. Due to the lower level of
all these indices in patients with halitosis, we cannot attribute halitosis in patients
with H. pylori infection to the presence of this microorganism with certainty.
KEYWORDS
bad breath, halitosis, Helicobacter pylori, oral factors
1 | I NTRO D U C TI O N
Most adults occasionally suffer from halitosis, with this disorder
observed in around 50% of the adult population, especially during
Halitosis is a common complaint among people which has various socio‐
the morning. 2
economic effects. However, unfortunately, it has remained understud‐
Several review studies have indicated that around 80%‐90% of
ied in medical literature. Proper diagnosis and determining the etiology
halitosis cases have an oral origin.3 Although coated tongue and less
of halitosis can contribute to selecting and performing the proper treat‐
frequently periodontitis and gingivitis have been known as the most
ment. Generally, two paths are considered for halitosis: first increased
impotent causes of halitosis so far, the dentist should not neglect
level of special metabolites in the bloodstream (due to a systemic dis‐
the risk of more serious causes and underlying diseases.1 A very few
ease) and second increased bacterial load or elevated levels of the sub‐
number of systemic diseases can also develop special odors in the
strate of these bacteria across the surfaces covering oropharynx cavity,
mouth. They include kidney problems, hepatic disease, diabetes,
respiratory tract, or the esophagus. All types of infections, ulcers, or
oropharyngeal infections, and gastritis.4,5 A small number of studies
tumors that exist in these anatomic regions can cause halitosis.1
have shown a relationship between halitosis and H. Pylori.6
Helicobacter. 2018;e12556.
https://doi.org/10.1111/hel.12556
wileyonlinelibrary.com/journal/hel
© 2018 John Wiley & Sons Ltd
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To record the dental status, DMFT criterion was used. This scale
is obtained by counting decayed (D), missing (M), and filled (F) teeth
and then summing them together.3
To determine coated tongue, 0‐4 scoring was used as follows:
0 = tongue without any coating, 1 = thin coating in less than one‐
third of the tongue, 2 = thin coating between one‐third and two‐
thirds of the tongue, 3 = thin coating in over two‐thirds of the
tongue or thick coating between one‐third and two‐thirds, and
4 = thick coating in over two‐thirds of the tongue.10
The oral hygiene was evaluated using simplified oral hygiene index
(OHI‐S), which is the sum of simplified debris index (DI‐S) and
simplified calculus index (CI‐S). In this method, six surfaces of
FIGURE 1
Mean DMFT in patients with and without halitosis
H. Pylori infection is one of the most common chronic bacte‐
rial infections in the world, especially in developing countries.7
two anterior teeth (upper right central labial surface, lower left
central labial surface), and four posterior teeth (buccal surface of
the top first molars, the lingual surface of the lower primary mo‐
lars are used. If the first molar is missed,then the second (or third)
Currently, not all people with H. Pylori undergo bacterial removal
molar is chosen. The level of debris and calculus is scored on it.11
treatment. The most important indications of treatment include
Debris index = (lingual scores) + (buccal scores)/the total number of
stomach ulcer or duodenal ulcer or low‐grade B‐cell lymphoma as‐
examined buccal and lingual surfaces
sociated with H. Pylori. Treatment is also indicated for functional
dyspepsia.4
The simple calculus index is scored as follows:
Generally, halitosis creates various relationship and social prob‐
lems for the patients, including inability to approach the people
0 = no calculus, 1 = calculus above the gum less than one‐third of
around and speaking to them. Diminished self‐confidence is the
the tooth surface, 2 = calculus above the gum between one‐third
main complaint among halitosis patients.3 In studies on the relation‐
and two‐thirds of the tooth surface or the presence of subgingival
ship between H. Pylori and halitosis, the role of oral factors as the
calculus patches in the cervical region, and 3 = calculus above the
most important cause of halitosis has been neglected. This study
gum more than two‐thirds of the expose surfaces in the mouth
was conducted with the aim of investigating the effect of oral fac‐
or a continual band of subgingival calculus around the cervical
tors on halitosis in patients with H. Pylori.
region.11
Calculus index = (lingual scores) + (buccal scores)/the total number
2 | M ATE R I A L S A N D M E TH O DS
of examined buccal and lingual surfaces)
The study was conducted on 108 dyspeptic patients with positive
H. Pylori serologic test. The diagnosis of H. Pylori was performed
3 | R E S U LT S
through serologic test, which is a simple noninvasive method that
measures IgG levels.4 Then, these patients were examined by a den‐
Out of the 108 participants in this study, eight of them were ex‐
tist. The oral examinations included checking for halitosis, coated
cluded due to incomplete information. From the remaining 100
tongue, oral hygiene, debris index, calculus index, and DMFT as indi‐
patients, 42 were male and 58 were female. The mean age of the
cators of overall oral hygiene.
participants was 38.5 years old (at least 16 and at most 70 years old).
Investigation of halitosis was done by asking the patients about
The mean DMFT index in all of the samples was 9.09 ± 3.97 (at
bad breath in the past three months and then using organolep‐
most 20 and at least 2). For the patients with halitosis, the mean
tic method. For this purpose, a plane (50 × 70 cm) was placed be‐
DMFT was 10.04 ± 3.34 (at most 17 and at least 2; Figure 1).
tween the patient and examiner to prevent them from seeing each
In order to investigate the relationship between halitosis and
other. Then, a clear tube (2.5 cm in diameter and 10 cm in length)
DMFT, Pearson correlation was used, with the results suggesting
was placed in the middle of this plane. The patient was requested to
that there was a direct and significant relationship between halitosis
close their mouth for 60 seconds and not swallow their saliva. After
and DMFT (P < 0.01).
that, they were supposed to exhale their exhaled air through a tube
The mean score of oral hygiene in the entire samples using the
in their mouth.8,9 Accordingly, the positive H. Pylori patients were
simplified oral hygiene index (OHI‐S) was obtained as 1.79 ± 0.949
classified in those with halitosis and without halitosis. A total of 8
(at most 4 and at least 0.4). The mean score obtained from the simpli‐
patients were excluded because of incomplete information or lack
fied debris index (DI‐S) in the entire samples was 1.01 ± 0.56, while
of cooperation.
the maximum and minimum of this index were 2 and 0, respectively.
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TA B L E 1 Maximum, mean, and
minimum scores of CI‐S, DI‐S, and OHI‐S
in patients with and without halitosis
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Group
Without halitosis
Min
With halitosis
Mean
Max
Min
Mean
Max
Index
OHI‐S
0.4
1.09 ± 0.46
2.3
0.5
2.04 ± 0.954
4
DI‐S
0.2
0.615 ± 0.28
1.2
0
1.15 ± 0.57
2
CI‐S
0.08
0.47 ± 0.24
1.3
0.2
0.88 ± 0.47
2.25
CI‐S: simplified calculus index, DI‐S: simplified debris index, OHI‐S: simplified oral hygiene index.
The mean score obtained from the simplified calculus index (CI‐S) in
the entire samples was 0.78 ± 0.46, while the maximum and mini‐
mum of this index were 2.25 and 0, respectively (Table 1).
To study the relationship between halitosis and OHI‐S, Pearson
correlation was used. The results showed that there was a direct and
significant relationship between halitosis and OHI‐S (P < 0.01). This
means that as OHI‐S index grows, which suggests diminished oral
hygiene, halitosis increases.
In order to investigate the relationship between halitosis and de‐
bris index, Spearman correlation was used. The results suggested
that there was a significant and direct relationship between halito‐
sis and debris index (P < 0.01). This means that as debris index in‐
creases, so does halitosis.
To examine the relationship between halitosis and calculus index,
FIGURE 2
Coated tongue in patients with and without halitosis
Spearman correlation was used. The results showed that there was
a direct and significant relationship between halitosis and calculus
90%, specificity: 80%). Serology tests are inexpensive and widely
index (P < 0.01). This means that the higher the calculus index, the
available.14 We chose the serologic test (ELISA) depends on our clin‐
more intense halitosis will be. To inspect the relationship between DI
ical setting, local availability, and cost.
and CI, Spearman correlation was used, based on which there was a
direct and significant relationship between DI and CI (P < 0.01).
In our study, the frequency of halitosis was obtained as 74%
in H. Pylori‐positive patients. This value in the study by Serin et al
To determine coated tongue status, 0‐4 scoring was used. The
was 61.5% among H. Pylori‐positive patients.15 Although currently
patients’ scores are presented in Figure 2. In 57 of patients (40 with
coated tongue (and less frequently) periodontitis and gingivitis are
halitosis and 17 without halitosis), no coating was seen on tongue
known as the most important causes of halitosis, the clinician should
(Figure 2).
not neglect more important and systemic causes that develop hal‐
To investigate the relationship between halitosis and coated
itosis.1 The existence of a possible relationship between H. Pylori
tongue, Spearman correlation was used. Here, no significant relation‐
and halitosis was first proposed by Marshall et al16 In 1992, Timony
ship was observed between halitosis and coated tongue (P = 0.353).
et al reported a considerable improvement in halitosis after re‐
moving H. Pylori.17 In the study by Katsinelos, in patients for whom
4 | D I S CU S S I O N
H. Pylori was eliminated successfully, signs of halitosis diminished
considerably.6
In spite of the results of these studies, there are still questions
The prevalence of halitosis has been examined in different stud‐
about the relationship between halitosis and H. pylori. One question
ies. Nevertheless, due to the different assessment methods and
is that if H. pylori is the cause of halitosis, what is the exact mecha‐
the diversity in cutoff point considered, various values have been
nism? Secondly, why halitosis still remains in many patients in spite
reported, and its prevalence has been stated to be 22%‐50%.3,12,13
of eradication of H. pylori?
Among the methods developed to detect H. pylori infection,
In studies that have examined the relationship between H. pylori
determining the gold standard remains debatable. Several indirect
and halitosis, the role of oral factors as the major cause of halito‐
and direct diagnostic tests have been used for H. pylori detection.
sis has been neglected. Based on the results of the present study,
Guidelines indicated that no single test can be considered as the gold
however, in H. pylori‐positive patients, a direct and significant rela‐
standard for the diagnosis of H. pylori infection.
tionship was observed between halitosis and all oral factors except
Antibody‐based tests, especially serology, are widely available
for coated tongue. It is possible that in the group of patients whose
and relatively sensitive; however, their specificity is low (sensitivity:
halitosis did not improve in spite of eliminating H. pylori, oral factors
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such as calculus, debris, decayed teeth, and defective fillings may
status, no significant relationship was observed between this index
have been the cause of development of halitosis.
and halitosis.3 A plaque is a mix of salivary proteins and bacteria,
Studies have shown that 80%‐90% of halitosis cases have an oral
which can be an important source of sulfur production and halito‐
origin.13,18,19 Various intraoral factors have been known for halitosis
sis. 21 The variety in the results of different studies on the relation‐
including gingivitis, periodontitis, unrepaired caries, improper resto‐
ship between halitosis and hygiene level and extent of plaque can be
13
rations, and local infections inside the mouth.
As a rule, any kind
of restoration in the mouth that prevents hygiene can cause accu‐
mulation of plaques, significantly increasing the potential of halitosis
development. 20
due to the different indices employed and the method of measuring
the oral hygiene level in them.
According to our results, 15 patients with halitosis had good
oral hygiene (OHI‐S index: 0‐1; Figure 3). With the method of the
In our study, the mean DMFT in H. pylori‐positive patients with
present study, the relation between halitosis and H. pylori in indi‐
halitosis was obtained as 9.09 ± 3.97, which had a significant rela‐
viduals with good oral hygiene neither can be confirmed nor can
tionship with halitosis (P = 0.001). The mean DMFT in the H. pylori‐
be refused.
positive patients without halitosis (6.4 ± 4.43) was lower than that of
the group qualifying halitosis (10.04 ± 3.34).
H. pylori was shown to produce hydrogen sulfide and methyl
mercaptan, which may suggest the contribution of this microorgan‐
Although various studies have indicated a significant relationship
ism in the development of halitosis. However, the production of vol‐
between coated tongue and halitosis,19 in the present study, this re‐
atile sulfur compounds by H. pylori is not only very complicated but
lationship was not significant (P > 0.01). Since one of the important
also strain‐specific. 22
causes of development of coated tongue is dry mouth, and in our
To investigate the role of H. Pylori in the development of halito‐
study, the patients with dry mouth and dehydration were excluded,
sis, future studies might include a series of patients with good oral
more than half of the patients (57%) lacked coated tongue.
hygiene who undergo endoscopic examination and pH measure‐
To investigate the level of oral hygiene, simplified oral hygiene
index (OHI‐S), which is the sum of debris index and calculus index,
ment of gastric juice and then treatment of H. pylori infection were
present.
was used. This index alone indicates the level of oral hygiene. In the
present study, a direct and significant relationship was obtained
between OHI‐S and its components with halitosis (DI and halitosis:
5 | CO N C LU S I O N
P = 0.001; CI and halitosis: P < 0.01; OHI‐S and halitosis: P < 0.01).
Furthermore, in the H. pylori‐positive patients without halitosis, CI,
Based on the results of the present study, there is a relation between
DI, and OHI‐S were lower than those of H. pylori‐positive patients
oral factors (debris index, calculus index, oral hygiene index, and
with halitosis, suggesting better oral hygiene in the first group. In
DMFT) and halitosis in H. pylori‐positive patients.
the study by Lu et al who used OHI‐S to investigate the oral hygiene
Considering the lower value of all of these indices in most H. pylori‐positive patients without halitosis, one cannot attribute halitosis
in H. pylori‐positive patients solely to the presence of the gastric mi‐
croorganisms with any certainty.
D I S C LO S U R E S O F I N T E R E S T S
The authors have no disclosures or other conflict of interest to
report.
ORCID
Fahimeh Anbari
Azin Khodabakhshi
https://orcid.org/0000-0002-0601-787X
http://orcid.org/0000-0002-2804-1336
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FIGURE 3
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How to cite this article: Anbari F, Ashouri Moghaddam A,
Sabeti E, Khodabakhshi A. Halitosis: Helicobacter pylori or oral
factors. Helicobacter. 2018;e12556. https://doi.org/10.1111/
hel.12556