International Dental Journal (2002)

Gastrointestinal diseases and

halitosis: association of gastric
Helicobacter pylorii nfection
K. Hoshi, Y. Yamano, A. Mitsunaga, S. Shimizu, J. Kagawa
and H. Ogiuchi
Tokyo, Japan

The relationship between gastrointestinal conditions and halitosis is Recently, halitosis research has
discussed. Few reports have suggested that gastrointestinal diseases may received considerable attention
cause halitosis. H. pylori infection, which causes gastric ulcers, is consid- from patients, clinicians, and
ered as a possible cause for halitosis. Intensity of malodour of mouth air researchers 1- 3 . Halitosis (oral
was found to be higher in H. pylori-positive patients than in negative malodour or 'bad breath') is caused
patients. The levels of hydrogen sulphide and dimethyl sulphide in mouth air mainly by tongue coating and peri-
were also significantly higher in the positive patients than in the negative odontal disease 4•5 • Volatile sulphur
patients (P<0.05). When odour strength in exhaled breath was compared compounds (VSC; hydrogen
between the two groups, no significant difference was found. Hence, sulphide, methyl mercaptan, and
H. pylori infection might not cause a systemic condition producing breath dimethyl sulphide) are claimed to
odour. Although there were no significant differences in periodontal param-
be the principal aetiological agents
eters or tongue coating between the positive and negative groups, H. pylori
for such halitosis 6 • Gastrointestinal
may be a frequent contributor to the production of malodour even though its
diseases are also generally believed
role had not been suspected before. Further study would be necessary to
to cause halitosis 7- 9 . A survey
clarify the reason for the increase of volatile sulphur compounds (VSCs)
level in H. pylori infection.
showed that people assumed hali-
tosis as originating from the
Key words: Halitosis, Helicobacter pylori, gastrointestinal disease gastrointestinal tract rather than
from the lungs or bronchi 10 .
Moreover, many patients had
previously visited a gastroenterolo-
gist before visiting our Breath
Odour Clinic. Not only patients
but also physicians and dentists
often attribute halitosis to gastric
problems, and advise patients to
undergo gastrointestinal examina-
tions11.
Breath analysis data have
clearly demonstrated that odorous
compounds produced by a
systemic disease such as hepatic
cirrhosis travel through the blood-
stream and diffuse into the lung
air 12- 15 . At present there is a lack of
critical evidence that would associ-
ate gastrointestinal diseases with
halitosis. However it has been
Correspondence to: Dr. K. Hoshi , Depart ment of Oral an d Maxi llofaci al Su rgery, Toky o
Women 's Medical University, School of Med icine, 8-1 Kawada-cho , Shinju ku -ku, Tokyo, demonstrated that gastric Helicobacter
162-8666 Japan. E-mail: keikah @ta2 .so-net.ne .jp pylori (H. pylon) infection, which is
© 2002 FDI/World Dental Press
0020-6539/02/03207-05
208
a risk factor for duodenal/ gastric
ulceration16 and gastric cancer17 , may
cause halitosis. In this paper, the
relationship between gastrointes-
tinal conditions and halitosis are
discussed.
Halitosis and gastrointestinal
diseases
There are some case reports of
halitosis caused by gastrointestinal
diseases 7- 9 • Pyloric stenosis is one
of the conditions discussed.
Obstruction of the gastric tract in
infants, such as congenital pyloric
stenosis, causes halitosis because of
the vomited food or gastric juice 18 .
Acquired pyloric stenosis is caused
by tumours, scars from gastric or
duodenal ulcers, as well as other
mechanisms. It has been described
that the malodour resulting from
this condition smells like rotten eggs,
and it has been reported that CO?,
H 2, CH 4 , and air were found in the
gas from the stomach7 • Foul odour
caused by pyloric stenosis was
improved with gastric lavage 7 , and
a tetracycline regimen improved
halitosis 8
A few cases of extrinsic duode-
nal obstruction with halitosis were
reported 19 . The peritoneal bands
pass across from the colon to the
duodenum, gallbladder, liver, and
kidney. These bands rarely obstruct
the duodenum. After correcting
duodenal obstruction 19 and aorta-
enteric fistula 20 , postoperatively the
patient's breath was no longer foul.
Based on these findings, it was
suggested that bacteria produced
volatiles in the gastrointestinal tract,
which are then expelled orally by
regurgitation or leaking. It is also
possible that the compounds might
diffuse into lung air after being
carried to the lungs by blood.
Although physiologic and oral
pathologic halitosis were not
differentially examined in these
studies, vomiting that accompanies
these conditions may also lead to
poor oral hygiene that may cause
oral malodour. For these patients,
Treatment Need- P, which is based
International Dental Journal (2002) Vol. 52/No.3 (Supplement)
on oral hygiene instructions, is
always required.
The oesophagus is normally
collapsed and closed tightly and as
a result gases originating in the
gastrointestinal tract are not released
through the mouth 12 • In pathologi-
cal conditions, such as gastric
retention, gastric and oesophageal
tumours or oesophageal diverticu-
lum, foul eructation or odour
leaking may occur. The sites of
lesions that produce the odour may
correlate to the odour intensity.
A lesion close to the oral cavity,
for example, pharyngoesophageal
(Zenker's) diverticulum 21 , may be
the main reason for the halitosis
associated with this condition.
The incidence of halitosis related
to intestinal diseases was found to
be less than 1 per cent of these
cases complaining of halitosis 11 •
Moreover, it is not simple for
dental practitioners to diagnose
extra-oral conditions, such as
gastrointestinal conditions. There-
fore, practitioners must employ the
classification of halitosis in order
to screen the conditions and avoid
mismanagement.
Halitosis in H. pylori positive
patients
Background of halitosis study
in H. pylori infections
Marshall et aiY reported halitosis
in subjects experimentally infected
with H. pylori, although the meas-
urement of malodour was not well
organised. Consequently, H. pylori
infection is considered as a cause
of halitosis 23- 27 . Hoshi 24 and Ierardi
et a/. 25 determined VSC concentra-
tion and organoleptic score in
mouth air from H. p]lori-positive
and -negative patients. Although
no significant differences were
observed between the groups 2\ an
association between H. pylori and
halitosis was suggested. Therefore,
these studies could not confirm the
'Helicobacter halitosis' correlation.
Recently, a well organised study has
been reported by Hoshi et a/. 28 , which
revealed the effect of H. PJilori
infection on oral malodou r
production.
Diagnosis of H. pylori
infection
Diagnosis of H. p]lori infection
includes invasive and/ or non-inva-
sive procedures. Invasive methods
utilising endoscopy involve the
culture of the microorganisms from
the tissue biopsy, the histological
evaluation, and the urease activity
test for high activity of the enzyme
in H. pylori. Non-endoscopic meth-
ods involve the serological assay of
antibody to H. pylori and the
[ 13 C]urea breath test. The antibody
assay is preferred by physicians, but
the method needs improvement.
The [13 C]urea breath test is a prac-
tical, simple, and very accurate
procedure to determine H. PJilori
infection. This procedure is consid-
ered as a readily available alternative
to the invasive method and involves
[ 13 C]urea being administered to
patients. H. PJilori metabolises
[ 13 C]urea to [13 C]CO? which then
appears in the breath air via the
lungs. High concentration of
[ 13 C]CO? in the breath air suggests
that H. fJ'Iori infection exists. This
procedure was employed by Hoshi
et al. 28 and Ierardi et al. 25 to deter-
mine the association between H.
pylori infection and halitosis.
Oral environment and H.
pylori infection
After the urea breath tests, 80
patients were divided into H.
pylori-positive (N = 31) and -nega-
tive groups (N = 49) 27 . The mean
ages were 44.7 and 33.8 years in
the gastric H. pylori-positive and
-negative groups (P<0.01) respec-
tively. As previously elucidated, the
prevalence of H. pylori infection
increases with age 29 •30 • The oral
health status of patients with and
without H. pylori infection is shown
in Table 1. No significant differ-
ence was found between the two
groups.
The occurrence of H. pylori
 209

Table 1 Age, gender and oral health status in H. pylori positive and negative groups

Variables H. pylori infection Significance

Positive (n=31) Negative (n=49)
Ag e, Mean(range)years 44 .7(21-77) 33.8( 18- 67) P<0.0 1"
Gender, Male/Female 14/17 20/29 NS
Plaque index 1.74 ± 0.53* 1.72 ± 0.47 NS
Gingival index 1.00 ± 0.56 1.16 ± 0.47 NS
Number of pockets 4mm or deeper 33.23 ± 21 .04 39.35 ± 24.11 NS
Number of pockets bleeding on probing 45.50 ± 26.2 1 59 .41 ± 28.72 NS
Tongue coating weight (mg) 17.50 ± 16.20b 15.00 ± 16.20C NS
*Mean ± SO
• Mean values were compared by unpai red t-test.
bn=23, cn=24

infection via the oral r oute is an

established theory, and the H. pylori
infection rate is high in th e
populations exposed to unsanitary
environments31 . T h e oral health
status of such a population is 8
presumed to b e generally p oor. 0 666
0
0 66 6
Poor oral h ygiene practices might 666
h ave a potential to relate with H. o8g 6 0 ~6
§ ~
pylori infection in individuals.
~ 66
66 ~0 6
0 6
0§~ 6~6 8o

-+
oo8 M~ 6
oo
Oral rna/odour and VSC in H. ~~~ 00
pylori-positive subjects
o8 6~ 0 ~
666 08o 8o 666

A gas chrom atograph (GC)

~~6 666
666
~ 6£,6~666
00 0 :SM
66 0 6~6
66 6
equipped with a flame photomet- 6 a ~66
Lib.

~~66
0
ric detector (GC-1 7A, Shimadzu,
J apan) was used to measure VSC 0 ~ 0

concentration in mouth air23 • Mean 10 8 ~ 0

values of hydrogen sulp h ide,
methyl mercaptan, and dimethyl
sulphide concentrations in mouth
air from the H. pylori positive
patients were determined 28 . T h e
mean co m mon logarithm s of
hydrogen sulphide, methyl mercaptan,
and dimethyl sulp hide levels o f the
H. pylori-positive and the H. pylori-
negative patients were - 0.59, - 0.84,
- 0.90, and - 1.16, - 1.36, - 1.57,
respectivelf 8 . Significant differences
were found in hydrogen sulphide
and dimethyl sulphide concentra-
tions between the H. pylori-posi-
tive and -negative groups (P<0.05),
but no significant difference was
observed in m ethyl m ercaptan
concen tration s 28 (Figure 1). The
reason for the absence of signifi-
cant difference in methyl mercaptan
may be that th e groups' periodon-
tal status was similar (Methyl
mercaptan level is strongly correlated
with the severity of periodontitis 4) .
666
~6
0
0 6
~ ~~~~-----------------------
H.p (+) H.p (-) H.p (+) H.p (-) H.p (+) H.p (-)
H2S CH3SH (CH3)2S
Figure 1. Distribution of concentrations of hydrogen sulphide, methyl mercaptan and
dimethyl sulphide in Helicobacter pylori-positive patients and -negative patients. All data
were logarithmically transformed to approximate them to normal distribution. H2 S: P=0.033,
CH3 SH: not significant, (CH3) 2 S: P=0.023 (Student's t-test based on arithmetic mean and
SD).
Results from organoleptic judg- might leak into the oesophagus or
ments of mouth air, exhaled breath, travel to the lungs via blood and
an d tongue coating odour are eventually diffuse into ltmg air. These
shown in Table 2 and T able J2 8 . A events would result in a significant
significant difference between H . increase in the organoleptic score
pylori-positive and -negative groups of exhaled breath, but no signifi-
was found only in mouth air (Table cant difference was reported 28 .
4) 28• H. pjilon· has high urease activ- Therefore, it was implied that H.
ity; urea is catalysed to ammonia pylori might not relate with extraoral
and carbon dioxide. Ammonia pathologic halitosis.
Hoshi eta/.: Gastrointestinal diseases and halitosis
210

Table 2 Oral malodour scores in H.pylori positive and negative groups

Number~su~ects(%)
Odour judgement• H. pylori
Pos itive Negative

Mouth air
Malodour Positive (Score 2,3,4, or 5) 23 (74.2%) 25 (51.0%)
Malodour Negative (Score 0,1) 8 (25 .8%) 24 (49.0%)
Total 31 (100.0%) 49 (100.0%)

Exhaling breath
Malodour Positive (Score 2,3,4, or 5) 22 (71 .0%) 30 (61 .2%)
Malodour Negative (Score 0,1) 9 (29.0%) 19 (38.8%)
Total 31 (1 00.0%) 49 (100.0%)

•oral malodour score was judged as previously described 3 ·5 .

Table 3 Tongue coating odour scores in H.pylori pos itive and

negative groups

Number of subjects (%)

Tongue coating odour score• H. pylori
Positive Negative

High (Score 3, 4, or 5) 7 (25 0%) 15 (33.3%)

Low (Score 0, 1, or 2) 21 (75 .0%) 30 (66.7%)
Total 28 (1 OO.O%)b 45 (1 OO.O%)b

•oral malodour score was judged as previously described 3 ·5

bThree and four measurements were missed from positive and
negative groups, respectively.

Table 4 Odds ratio, chi-square and confidence interval between oral/tongue coating
malodour and H. pylori infection

Odds ratio 95% Cl• chi -square

Oral malodour in mouth airc 2.76 1.78to3.74 4.248b

Oral malodour in exhaling breathe 1.55 0.58 to 2.52 0.792
Tongue coating malodourd 1.50 0.44 to 2.56 0.569
aCl:confidence interval.
bP<0.05
csee Table 2 for the results by organoleptic measurement.
dSee Table 3 for the results by organoleptic measurements

It is not yet confirmed whether to be a degenerated morphologic microorganism effectively reduced

H. pylori produces VSC. If H. pylori
contributes to the production of
VSC in gastrointestinal tracts,
hydrogen sulphide in the intestine
would be quickly oxidised before
being absorbed into the blood
stream. Methyl mercaptan would
be methylated to dimethyl sulphide
as previously reported 32 . Then
dimethyl sulphide would diffuse
into the lung air after being carried
to the lungs via blood. However
dimethyl sulphide in the lung air
from H. pylori positive patients has
not yet been determined.
H. pylori is present in the oral
cavity as the coccoid form. Culture
supernatant of oral microorganisms
inhibits growth and biochemical
activities of the H. pylori strain, and
generates the coccal form; suggested
International Dental Journal (2002) Vol. 52/No.3 (Supplement)
phase 33 •34 • It was found that odour
intensity and VSC concentration
were higher in the mouth air of the
H. pylori-positive subjects than in
H. pylori-negative subjects (P<O.OS).
Although H. pylori infection may
not be the principal cause of hali-
tosis, since 50 per cent of the
world's population is believed to
carry this microoraganism 31 , H.
pylori might be a common contribu-
tor to the production of malodour.
Is it possible to eliminate oral
rna/odour associated with H.
pylori?
It has been reported that H. pylori
disappeared after treatment but
halitosis persisted2 . Other findings
suggested that eradication of the
oral malodour 25 •26 . In these latter
studies, the patients were not
examined for physiologic, oral
pathologic, or extraoral pathologic
halitosis by accurate odour assess -
ment. Antibiotics, which are used
for eradication of H. pylori in the
former studies 2•25 •26 , appear prom-
ising in the treatment of physiologic
halitosis 35 • It has not yet been eluci-
dated whether or not oral malodour
associated with H. pylori can be
eliminated through the eradication
of H. pylori.
It has been suggested that chlor-
hexidine mouthrinse may not reduce
oral malodour of H. pylori-positive
dyspeptic patients following omera-
zole and amoxicillin treatments,
although antiseptic mouthrinses
improve oral malodour 25 • In our

clinic, oral m alo dour m easured by
gas chromatography was reduced
in H. pylori-positive patients o nly
with oral hygiene including to ngue
cleaning and without eradicating H.
pylori (data are n o t shown). T h ere-
fore, oral hygiene practices, such as
tongue cleaning (that is, Treatment
N eeds-13•5), should be adopted for
reducing oral malodour associated
with H. pjilori.
Conclusions
Gastrointestinal condition s, which
m ay cause halitosis, are very rare in
occurrence; and as such, are not
considered to be the common
causes of halitosis. H. PJ'Iori-posi-
tive patients demonstrated more
severe malodour in their mouth air
than did the H. pji/ori-negative
patients. However, no significant
difference was observed in the
exhaled breaths of the two groups.
H. pylori infection, on its own, may
not induce extraoral pathologic hali-
tosis except in the conditions with
complications.
References
1 . van Steenberghe D . Breath malodor.
Curr Opin Periodonto/1997 4: 137-143 .
2 . Delanghe G, Ghyselen J, van
Steenberghe D, eta!. Multidisciplinary
breath-odour clinic. Lancet 1997 350:
187 .
3. Yaegaki k, Coil J M. Examination,
classification, and treatment of hali-
tosis; clinical perspectiVes. J Can Dwt
Assoc 2000 66: 257- 261.
4 . Yaegaki K, Sanada K . Biochemical and
clinical fac tors influencing oral
malodor in periodontal patients. J
Peridontol 1992 63: 783-789 .
5 . Miyazaki H, Sakao S, Katoh Y, eta!.
Correlation between volatile sulphur
components and certain oral health
measurements in general population. J
Pe1iodontol 1995 66: 679- 684.
6. Tonzetich J. Direct gas chromato-
graphic analysis of sulphur compounds
in mouth air in man. Arch Oral Bioi
1971 16: 587- 597 .
7 . Eas t T. An explosive eructation. Lancet
1934 4: 252- 253 .
8. Tydd T F, Dyer N H . Pyloric stenosis
presen ti ng with h ali tosis. Br Med J
1974 3: 321.
9 . Attia E L, Marsh all K G . Halitosis
CMAJ 1982 126: 1281- 1285 .
10 . Hoshi K . Evaluation and perception
of oral malodor among students in
denti stry thro ugh a standard question-
naire. In the ThesiJ of 'Master of Dental
Sciences' pp14- 22, Leuven: Catholic
University Le uven, 1996.
11 . Delanghe G . G hyselen J, Bollen C, et
a!. An invento ry of patients' response
to tr eatment at amultidi sciplinary
breath odor clinic. Q11intesswce Int
1999 30: 307- 310 .
12 . Beers M H, Berkow R. Halitosis. In
The i\lferck 111anua/ of Diag11osis and
Tberapy (17th ed) pp 239-240, West
Point: Merck, 1999 .
13 . Roo th G, Ostenson S. Acetone in al-
veolar air, and the control of diabe tes.
Lancet 1966 2: 1102- 1105.
14 . Simenhoff M L, Burke J F, Saukkonen
J J, eta!. Biochemical profile of uremic
breath. N Eng! J Med 1977 297: 132-
135 .
15 . Tangerman A, Meuwese-Arends M T,
van Tongeren J H M. A new sensitive
assay fo r measuring volatile sulphur
compounds in human breath by Ten ax
trapping and gas chromatography and
its application in liver cirrhosis. Clinica
Chimica Acta 1983 130: 103- 110.
16 . Nomura A, Stemmermann G N, Chyou
P-H, et a!. H elicobacter pyl01i infection
and the risk for duodenal and gastric
ulceration . Ann Intem iVIed 1994 120:
977- 981.
17 . Uemura N, Okamoto S, Yamamoto S,
et a!. H elicobacter pylori infection and
the development of gastric cancer. N
Eng/ J i\!Ied 2001 345: 784-789 .
18 . Madarikan BA. Halitosis and gastric
outlet obstruction in infants. Br J Clin
Pract 1990 44: 419.
1 9 . Stephenson B M, Rees B I. Extrinsic
duodenal obstruction and halitosis.
Postgrad Med J 1990 66: 568-5 70.
20. Mosimann F . Faecaloid breath herald-
ing secondary aorto -enteric fistula.
Vasa 1995 24: 77- 78 .
21 . Crescenzo D G, Transtek V F, Allen
M S, et a/. Zenker's diverticulum in
the elderly: Is operation justified? Ann
Thorac S11rg 1998 66: 347-350.
22 . Marshall B J, Armstrong] A, McGechie
D B, et a!. Attempt to fulfil Koch's
./
211
postulates for pyloric campylobacter.
Med J A11st 1985 142: 436-439 .
23 . Greenspan J S. Halitosis. In Braunwald
E, Fa uci AS, Kasper D L, et a!. (eds)
Harrison's principles of intemal medicin.
15'" ed. pp194-198 . Washington, DC:
McGraw-Hill, 2001 .
24. Hoshi K, Possible link of Helicobacter
pylori infection to oral malodor. In the
Thesis of 'Master of Dwta/ Scie11ces'
pp36- 54, Leuven : Catholic Univer-
sity Leuven, 1996.
25 . Ierardi E, Amoruso A, La Notte T, et
a/. Halitosis and Helicobacter pylori a
possible relationship. Dig Dis Sci 1998
43: 2733-2737.
26. Tiomny E, Arber N, Moshkowitz M,
et a!. Halitosis and Helicobacter pylo1i -
a possible link? J Clin Gastrowterol
1992 15: 236- 237.
2 7 . Norfleet R G. Helicobacter halitosis.
J Clin Gastroenterol 1993 16: 274.
28 . Hoshi K, Yamano Y, Mitsunaga A, et
a/. Association between halitosis and
gastric Helicobacter PJ'Iori infection. J
Tokyo Tf;7olll Med Uni1> 2001 71: 787-
797.
29. Asaka M, I<..imura T, Kudo M, eta/.
Relationship of Helicobacter pylori to
serum pepsinogens in an asymptomatic
Japanese population. Gastroenterology
1992 102: 760- 766.
30 . Leodolter A, Wolle K, Malfertheiner
P. Current standards in the diagnosis
of Helicobacter pylori infection. Dzg
Dis 2001 19: 116- 122.
31 . Brown L M. Helicobacter pylmi: epide-
miology and routes of transmission.
Epidemiol R ev 2000 22: 283-297.
32 . Kaji H , Hisamura M, Saito N, et a/.
Gas chromatographic determination
of volatile sulfur compounds in the
expired alveolar air in hepatopathic
subjects. J Cbrolllatograplry 1978 145:
464- 468.
33. Eaton K A, Catrenich C E, Makin K
M, et a/. Virulence of coccoid and
bacillary forms of Helicobacter PJ'I01i in
gnotobiotic piglets. J Infect Dis 1995
171: 459- 62.
34 . Okuda K, Ishihara K, Miura T, eta!.
Helicobacter pylori may have only a
transient presence in the oral cavity
and on the surface of oral cancer.
Microbiol Imlllllllol 2000 44: 385-388.
35. Fujimaki I, Yamaguchi H , Obata J, et
a!. Deodorant effects of flagyl by dou-
ble-blind method. J ]p11 Soc Pe1iodontol
1973 15: 271-275.
Hoshi et a/: Gastrointesti nal diseases and halitosis