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[Eye Reports 2011; 1:e14] [page 45]

Detection of Helicobacter
Pylori in the lacrimal sac
mucosa of the patients with
primary acquired nasolacrimal
duct obstruction
Naser Owji,1

Seyed Mohammad Bagher Abtahi,2

Negar Azarpira3

1Poostchi Eye Research Center;
2Department of Ophthalmology, Khallili
Hospital; 3Organ Transplant Research
Center, Shiraz University of Medical
Sciences, Shiraz, Iran

Abstract 

Helicobacter pylori have been detected in
sinonasal mucosa in both normal and patho-
logic condition. The nasolacrimal duct is with-
in the medial wall of maxillary sinus and open
into the nasal cavity, so ascending colonization
of nasolacrimal duct and lacrimal sac is possi-
ble. The aim of this study is to investigate the
presence of H. pylori by polymerase chain
(PCR) reaction in the nasal and lacrimal sac
mucosa of the patients with primary acquired
nasolacrimal duct obstruction. Eighty patients
with primary acquired nasolacrimal duct
obstruction who were scheduled for dacryocys-
torhinostomy enrolled in the study. The
patients were asked if they suffered from the
classic symptoms of gastroesophageal reflux
disease (heart burn, regurgitation, and acid
taste). Tissue samples from the lacrimal sac
mucosa and nasal mucosa were obtained dur-
ing dacryocystorhinostomy surgery. The tis-
sues were analyzed for detection of H. pylori
DNA by PCR. The mean age of patients was
41.96±14.7 years (age range, 17-84 Years).
PCR for H. pylori DNA was positive in the nasal
mucosa in 3 patients, in the lacrimal sac
mucosa in 2 patients and in both nasal mucosa
and lacrimal sac mucosa in 1 patient. Classic
symptoms of gastroesophageal reflux disease
were found in 16 patients (20%). It is possible
to detect H. pylori in the lacrimal sac mucosa
of some patients with primary acquired naso-
lacrimal duct obstruction. More comprehen-
sive studies are needed to determine whether
H. pylori plays an etiopathologic role in the
development of primary acquired nasolacrimal
duct obstruction.

Introduction

Helicobacter pylori is a microaerophilic
Gram-negative spiral organism that normally
inhabits the gastric mucus layer. H. pylori is a
major cause of gastritis and peptic ulcer dis-
ease and has been implicated in the develop-
ment of gastric malignancy.1 Colonization of H.
pylori has been found in dental plaques, saliva,
tonsils and adenoids.2,3 Recently this organism
was also detected in the nasal and maxillary
sinus specimens of patients with chronic
sinusitis.4-6 Some believe that the sinonasal
mucosa serves as reservoir for H. pylori infec-
tions.5,6 The nasolacrimal duct is within the
medial wall of the maxillary sinus and opens
into the nasal cavity, so ascending colonization
of nasolacrimal duct and lacrimal sac is possi-
ble. The present investigation was planned to
determine the presence of H. pylori by poly-
merase chain reaction (PCR) in the nasal and
lacrimal sac mucosa in patients with primary
acquired nasolacrimal duct obstruction who
underwent dacryocystorhinostomy. 

Materials and Methods

Eighty consecutive patients with primary
acquired nasolacrimal duct obstruction were
enrolled. They were scheduled for dacryocys-
torhinostomy (DCR) in Khallili Teaching
Hospital (Shiraz, Iran). The study was
approved by the local ethics committee
(Poostchi Eye Research Center). All patients
gave their informed consent before enrolling
in the study. All patients were examined by an
otolaryngologist to rule out possible secondary
causes of nasolacrimal duct obstruction. The
patients were asked whether they had classic
symptoms of gastroesophageal reflux disease
(heart burn, regurgitation, and acid taste) and
whether they had used antibiotics, bismuth
compounds, H2 receptor blockers, antacid
drugs, and proton pump inhibitors before the
surgery. Those who used the above systemic
medications four weeks before the surgery
were excluded from the study. Classic external
DCR was carried out under general anesthe-
sia. Tissue samples from lacrimal sac mucosa
and nasal mucosa were prepared at the time of
lacrimal sac and nasal mucosal flap prepara-
tion. 
Biopsy specimens were fixed in 10%

buffered formalin, embedded in paraffin, sec-
tioned and stained with hematoxylin-eosin to
evaluate the pathological findings. DNA was
extracted from the sample tissues (containing
approximately 10 mg of specimen) by using a
tissue DNA extraction kit (Cinnagen, Tehran,
Iran), following the manufacturer’s instruc-
tions. Great care was taken to avoid contami-

nation both during the sample collection step
and preparation step. 
A polymerase chain reaction assay with the

H. pylori PCR detection kit was performed
according to the manufacturer's protocol. PCR
primers were targeted to an ureC gene seg-
ment of H. pylori. All samples were positive for
b-globin as an internal control. In each run,
positive and negative controls were included.
Culturing of microorganisms and PCR for

other microorganisms was not performed in
this investigation.
The chi-square test and independent t-test

were used for statistical analysis. A P value of
less than 0.05 was considered to be significant. 

Results

The present investigation was performed on
80 patients. There were 21 male (26.25%) and
59 female (73.75%) patients. The mean age of
patients was 41.96±14.7 years (age range, 17-
84 Years). The PCR for H. pylori DNA was pos-
itive in the nasal mucosa in 3 patients, in the
lacrimal sac mucosa in 2 patients and in both

Eye Reports 2011; volume 1:e14

Correspondence: Naser Owji, Department of
Ophthalmology, Khallili Hospital, Oculoplasty
service, Shiraz University of Medical Sciences,
Shiraz, Fars, Iran. Tel./Fax: +98.711.647.1479.
E-mail: dr_oji@yahoo.com

Key words: Helicobacter Pylori, acquired naso-
lacrimal duct obstruction, polymerase chain reac-
tion, nasal mucosa, lacrimal sac mucosa.

Acknowledgements: the authors would like to
thank Soraya Saky, MD for assistance in data col-
lection, and Mohammad Javad Ashraf, MD for
review of pathology specimens. 

Contributions: NO, manuscript conception and
design, revision and final approval; SMBA, NA,
data acquisition, manuscript drafting and final
approval.

Funding: financially, this study is partially sup-
ported by Organ transplant research center,
Shiraz university of medical sciences. There is no
proprietary interest. 

Received for publication: 10 April 2011.
Revision received: 5 December 2011.
Accepted for publication: 6 December 2011.

This work is licensed under a Creative Commons
Attribution NonCommercial 3.0 License (CC BY-
NC 3.0).

©Copyright N. Owji et al., 2011
Licensee PAGEPress, Italy
Eye Reports 2011; 1:e14
doi:10.4081/eye.2011.e14

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[page 46] [Eye Reports 2011; 1:e14]

nasal mucosa and lacrimal sac in 1 patient.
Statistically, there was no significant differ-
ence (P=0.63) between the mean age of
patient with positive PCR (39.16 Years) and
that of the patients with negative PCR (42.18
Years). Classic symptoms of gastroesophageal
reflux disease (GERD) were found in 16
patients (20%). Classic symptoms of GERD
were present in 1 PCR positive patient and in
15 PCR negative patients. There was no statis-
tically significant difference between the two
groups (P=0.65). There was, however, a statis-
tically significant difference between the
mean ages of the patients with and without
classic symptoms of GERD, which were 50.81
years, and 39.75 years, respectively (P=0.007). 

Discussion

H. pylori normally inhabits the gastric
mucosa. H. pylori has been detected in dental
plaque, saliva, tonsils, and adenoids.2,3 The oral
cavity might be considered a reservoir for H.
pylori.7 H. pylori has been found in nasal polyp,
nasal mucosa and maxillary sinus mucosa in
some patients with chronic sinusitis.4-6

The role of H. pylori infection in ophthalmic
diseases such as chronic ocular inflammation,
glaucoma,8 rosacea, and chronic blepharitis9

has been postulated. The complex interaction
between H. pylori and ocular disease is a field
of ongoing research. Gastric colonization by H.
pylori infection is associated with release of
variable proinflammatory and vasoactive sub-
stances such as interleukins, tumor necrosis
factor α, interferon g, prostaglandins, and C-
reactive protein. In addition, in peptic ulcer
disease associated with H. pylori infection,
nitric oxide and endothelin-1 (constrictor of
arterioles and venules) are increased. These
substances may influence, for example, the
pathophysiology of glaucoma by microvascular
disturbance of anterior optic nerve vessels and
the ophthalmic artery.10 Production of oxida-
tive stress and circulating lipid peroxides by H.
pylori infection could affect pathophysiology of
glaucoma as well.11 Similar mechanisms have
been proposed for a possible association
between H. pylori infection and choroido -
retinopathy.12 Gastrin (a potent vasodilator)
level in the serum is elevated in patients with
H. pylori associated gastric disease.
Circulating gastrin may cause vasodilation of
the skin and ocular surface vessels leads to
rosacea manifestations.13

To the best of our knowledge, this is the first
study reporting the presence of H. pylori in the
lacrimal sac mucosa. The detection of H. pylori
in the lacrimal sac mucosa shows that colo-
nization is not restricted to the nasal cavity,
but ascending colonization via nasolacrimal
duct is possible. The postulated mechanisms

by which H. pylori reaches the nasal cavity are
as follows. First, H. pylori may come from the
stomach by gastroesophageal reflux (GER).
Second, the oral cavity may act as a reservoir of
H. pylori, and the microorganism may come to
the nasal cavity directly through oronasal
reflux.4,6 In our study, the prevalence of subjec-
tive signs of GERD was similar in both PCR
positive and negative patients. We did not
investigate GER objectively. In addition, we did
not investigate the presence of H. pylori in the
stomach or oral cavity, so we do not know about
the source of infection in these cases. 
The role of H. pylori infection in the patho-

genesis of upper respiratory system diseases
has been evaluated by some investigators.14 It
is speculated that there is a relationship
between GERD and chronic rhinopharyngitis
and rhinosinusitis in both children and
adult.15-17 It is suggested that direct reflux of
gastric juice into nasopharynx may cause
mucosal edema and inflammation, leading to
obstruction of sinus ostia.18 Recently focus has
been on the possible direct role of H. pylori in
tissue injury of the sinonasal mucosa and
development of chronic rhinosinusitis.4,6

However, the causality has not been estab-
lished yet. 
Primary acquired nasolacrimal duct obstruc-

tion (PANDO) occurs in the absence of an
obvious precipitating cause.19 Pathologic stud-
ies of lacrimal passages have indicated that
PANDO results from fibrous obstruction sec-
ondary to chronic inflammation. The first
event in nasolacrimal duct obstruction is
unknown but dacryostenosis develop as a
result of inflammation and fibrosis.
Dacryostenosis with stasis and secondary
infection may lead to complete nasolacrimal
duct obstruction.20,21 Descending infection
from the conjunctiva has been considered a
causative factor in dacryostenosis. In addition
to the descending infection from the eye,
ascending infection from nasal mucosa could
be the starting point of dacryostenosis.22

Bacteria, fungi, and parasites have been impli-
cated as underlying causes of lacrimal
drainage obstruction.19

In our series, those who used systemic
antibiotics or bismuth during the four weeks
before the surgery were excluded, as the treat-
ment may eradicate or decrease H. pylori pres-
ence. The lacrimal sac mucosa of three
patients was positive for H. pylori. Retrograde
colonization of nasolacrimal duct and hence
lacrimal sac mucosa from the nasal cavity is
possible. It may be transient colonization but
infection of the nasolacrimal duct and lacrimal
sac could not be ruled out. It is highly specula-
tive, but in some patients with PANDO, H.
pylori may cause direct nasolacrimal duct
mucosa injury and chronic inflammation, lead-
ing to nasolacrimal duct stenosis. If it is true,
treatment of H. pylori in these patients is war-

ranted to prevent complete nasolacrimal duct
obstruction.
Limitations of the present case series sug-

gest several areas for further research. One of
the drawbacks of our study is the lack of con-
trol group. Secondly, the small group of partic-
ipants limits the ability to make generaliza-
tions and requires one to view the results with
caution. Hence, there is a need for further
research to evaluate the presence of H. pylori
in larger series with a control group and to
evaluate the effect of treatment for H. pylori in
patients with positive PCR.

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