









































Pa
ge

 
1



Pa
ge

 
47

American Journal of  Medical 
Science and Innovation (AJMSI) 

Prevalence of  Helicobacter Pylori (H. Pylori) Infection among Patients Undergoing 
Upper Gastrointestinal Endoscopy: An Institution Based Study

Prabhat Pradhan1, Gyan Prasad Bajgai2*

Volume 2 Issue 1, Year 2023 
ISSN: 2836-8509 (Online) 

DOI: https://doi.org/10.54536/ajmsi.v2i1.1320
https://journals.e-palli.com/home/index.php/ajmsi

Article Information ABSTRACT

Received: February 19, 2023

Accepted: March 20, 2023

Published: March 30, 2023

Several studies have established region-based prevalence rate of  H. pylori infection and its 
association with clinical outcomes in Bhutan. However, this study attempts to determine 
hospital-based prevalence rate of  H. pylori and its association with clinical outcomes. A 
total of  347 volunteers (159 females and 188 males; mean age of  49.8 ± 15.5 years) were 
enrolled from Central Regional Referral Hospital (CRRH) in Gelephu.  Upper gastro-intestinal 
endoscopy (UGIE) was performed among the dyspeptics and H. pylori infection was 
determined by Histology examination. The histological prevalence of  H. pylori among 
347 patients who went upper gastro-intestinal endoscopy was 55.6%. The prevalence of  
H. pylori infection increased with age but it was statistically insignificant (P > 0.05). 
Gastritis was the most common endoscopic finding, present in 309 (89%) patients followed 
by normal upper endoscopy results in 24 (6.9%) patients. The prevalence of  H. pylori 
among patients with gastritis and a duodenal ulcer was significantly higher than in patients 
with gastric cancer (P < 0.05). The high incidence of  gastritis in the hospital may be 
attributed to the high prevalence of  H. pylori infection among the individuals with dyspepsia. 

Keywords
Endoscopy, Gelephu, 
Helicobacter Pylori, 
Prevalence 

1  Department of  Surgery, Jigme Dorji Wangchuck National Referral Hospital, Thimphu Bhutan
2 Department of  Dentistry, Jigme Dorji Wangchuck National Referral Hospital, Thimphu Bhutan
* Corresponding author’s e-mail: gpbajgai@jdwnrh.gov.bt

INTRODUCTION
Helicobacter pylori infection is well known to be the most 
common human infection affecting more than 50% of  
the world’s population (Salih, B.A. (2009). There is a 
variation in the prevalence of  infection between different 
countries and, among different societies and ethnic 
groups within the same country (Van D. et al. 2009; Kaur 
et al.2003; Malaty et al. 1996). Chronic infection with H. 
pylori is typically acquired early in life, especially among 
those in poor socio-economic status and over-crowded 
conditions (Bardhan PK, 1997; McColl KE 2010). 
Bhutan is a small country with an estimated population 
of  8, 00,000. The incidence of  gastric cancer in Bhutan 
is reported to be quite high (with 24.2 cases per 100,000 
populations per years) as compared to other neighboring 
countries like Thailand, India and Bangladesh (Shiota et 
al, 2013; Dendup et al. 2015). The previous studies have 
showed association of  high incidence of  gastric cancer 
with high prevalence of  H. pylori among Bhutanese 
population (Dorji et al. 2014; Vilaichone et al. 2013). 
However, there has not been a study conducted as to 
determine the hospital-based prevalence rate of  H. pylori 
infection and its association with clinical outcomes among 
the patients regularly visiting the concerned hospital. 
Helicobacter pylori infection is quite rampant in Bhutan at 
66.2%. Punakha district disclosed the highest prevalence of  
H. pylori infection (85.6%), followed by Wangduephodrang 
district (75.4%), while Haa had the lowest prevalence 
(57.7%) (18). The reason why Haa and other districts had 
lower prevalence could be due to low residing population 
and seasonal migration during summer and winter months 
(Ratha-korn et al. 2020).
Therefore, we conducted a retrospective hospital-based 

study over two years (August 2014 to December 2016) 
to determine the prevalence of  H. pylori infection among 
the dyspeptic patients visiting CRRH and to assess 
association among clinical outcomes, gender and age with 
H. pylori infection. 

METHODS
Gelephu is one of  the sub-districts located in the Southern 
part of  Bhutan. The region shares border with India. The 
Central Regional Referral Hospital (CRRH), located in 
Gelephu, provides healthcare services to the local people 
residing in Sarpang district, as well as to those patients 
referred from four other districts which include Trongsa, 
Tsirang, Dagana and Zhemgang within the Central 
Region. Patients are referred to CRRH to avail endoscopy 
service from all five districts as the district hospitals lack 
such facility. 
This was a cross-sectional study was carried out among 
Bhutanese population who attended CRRH between 
August 2014 and December 2016. The study population 
included individuals who had undergone UGIE for 

Figure 1: Central Regional Referral Hospital, Bhutan

https://doi.org/10.54536/ajmsi.v2i1.1320
https://journals.e-palli.com/home/index.php/ajmsi


Pa
ge

 
48

https://journals.e-palli.com/home/index.php/ajmsi

Am. J. Med. Sci. Innov. 2(1) 47-50, 2023

evaluation of  dyspeptic symptoms. The information on 
age, gender, biopsy report and presence or absence of  
H. pylori infection was reviewed from the medical record 
maintained in the outpatient registry. Subjects with age 
below 14 years were excluded from the study. This study 
was approved by Research Ethics Board of  Health 
(REBH), Ministry of  Health. 

Procedure for Endoscopy and Histology
Endoscopy was performed after an overnight fasting of  
the patients. Scope was inserted through the mouth after 
lignocaine spray in the throat to make the pharynx numb. 
Detailed examination of  esophagus, stomach and upper 
part of  duodenum was performed. Gastric biopsies 
were taken randomly from at least two sites. All biopsies 
were fixed in formalin prior to shipment to Pathology 
laboratory in Thimphu for Hematoxylin and Eosin (H 
& E) staining. 

Statistical Analysis
Frequency and percentage were used to describe the 
characteristics of  the study population. The prevalence of  
H. pylori infection was presented in terms of  percentage 
(%) and Z-test was used to assess whether this prevalence 
was significantly different from the prevalence of  
previous studies. The association between age and gender 
with H. pylori infection was analyzed using Pearson Chi-
Square. P value less than 0.05 was considered statistically 
significant in this study.

RESULTS
Endoscopic Findings and Prevalence of  H. Pylori 
infection
A total of  347 subjects were enrolled for the study of  
which, 159 (45.82%) were females and 188 (54.18%) were 
males. The mean age of  the study population was 49.8±15.5 
years (range: 15 – 83 years). The most common endoscopic 
finding among the patients with dyspepsia was gastritis 
(309, 89.05%), followed by normal endoscopy results (24, 
6.9%). Gastric cancer, duodenal ulcer and gastric ulcer 
were less common, present only in eight patients (2.31%), 
five (1.44%) and, one (0.29%) respectively.
A study subject was considered H. pylori positive when the 
biopsy specimen showed positive in H & E staining. The 
overall prevalence of  H. pylori among the study subjects 
was 55.6% (95% CI: 50.367 – 60.873). We also tested 
whether the prevalence in this study was significantly 
different from previous studies using Z-test (Ha: p < 86% 
and Ha: p < 73.4%). The prevalence of  H. pylori infection 
among the study population in CRRH was significantly 
lower as compared to previous prevalence of  H. pylori 
infection found in other Regions (p<0.001).

Association of  H. Pylori Infection with Age and 
Gender
109 (57.98%) of  the males were H. pylori positive as 
compared to 84 (52.83%) of  the females. In our study, 
older patients were more likely to be H. pylori positive 
than the younger ones. The positivity of  H. pylori was 

Table 1: Association of  H. pylori infection with age and gender.

Characteristics Total number (n) H. pylori P-value
Positive (%) Negative (%)

Gender
Male 188 109(57.98) 79 (42.02) 0.336#

Female 159 84 (52.83) 75 (47.17)
Age
15 - 29 38 19 (9.87) 19 (12.34) 0.124#

30 - 39 62 38 (19.69) 24 (15.58)
40 - 49 63 42 (21.76) 21 (13.64)
50 - 59 71 40 (20.73) 31 (21.13)
> 60 113 54 (27.98) 59 (38.31)

observed highest among subjects with age higher than 
60 years (27.98%) followed by 40-49 years (21.76%) and 
50-59 years (20.73%). 15-29 years subjects had the least 
H. pylori infection with 9.87%. However, there was no 
statistically significant association of  H. pylori infection 
with both gender and age (p>0.05) (Table 1). 

Association between H. pylori infection and clinical 
outcomes
The clinical presentations of  the subjects were considered 
for assessing the association with H. pylori infection 
(Table 2). Patients with gastritis are more likely to have H. 
pylori infection (61.8%) than those without it (38.2%; p < 

Table 2: Association between H. pylori infection and clinical findings.

Clinical Findings Total number (%) H. pylori P-value
Positive (%) Negative (%)

Gastritis 309 (89.0) 191 (61.8) 118 (38.2) < 0.001#

Gastric ulcer 5 (1.4) 1 (20.0) 4 (80.0) < 0.001*

https://journals.e-palli.com/home/index.php/ajmsi


Pa
ge

 
49

https://journals.e-palli.com/home/index.php/ajmsi

Am. J. Med. Sci. Innov. 2(1) 47-50, 2023

Duodenal ulcer 1 (0.3) 0 (0.0) 1 (100.0) 0.444*

Gastric cancer 8 (2.3) 1 (12.5) 7 (87.5) 0.030*

Normal 24 (6.9) 0 (0.0) 24 (100.0) < 0.001#

0.001). In contrary, cases with gastric ulcer, gastric cancer 
and normal endoscopic findings are less likely to have H. 
pylori infection (p < 0.05).

DISCUSSION
This study was endoscopy-based and histological 
examination was performed to detect H. pylori among 
patients with dyspepsia. The study revealed high 
prevalence rate of  H. pylori 55.6% among Bhutanese 
population with dyspepsia. This is in contrast to the 
previous studies conducted by Vilaichone et al 2014; 
Dorji et al. 2013) in Bhutan where the prevalence rates 
ranging from 73.4% to as high as 96% were found among 
Bhutanese population residing in different districts and 
regions with dyspepsia. The lower prevalence rate of  H. 
pylori, as revealed by our study compared to the previous 
studies, possibly could have been due to the sensitivity 
of  histological detection, which was the only method of  
detection used in this study. The sensitivity of  this method 
depends not only on density of  H. pylori biopsy sites but 
also on expertise of  pathologists (el-Zimaity HM, 2000). 
Many studies have showed several factors such as age 
of  patient, socio-cultural practices, living conditions, 
environment and geographic location play important 
roles in H. pylori infection in different population. 
Therefore, one of  the factors contributing to the lower 
prevalence of  H. pylori, as compared to the previous 
studies, could also be due to the location of  the hospital, 
Southern part of  Bhutan where socio-cultural practices 
are different from the mainstream Bhutanese tradition 
and cultural practices. The same study conducted by 
Dorji and his colleagues has revealed the similar trend in 
the prevalence of  H. pylori in Southern Bhutan compared 
to Western and Central regions. However, it is difficult to 
compare the H. pylori detection rate since different studies 
have used different methods. Dorji et al has used serology 
to determine IgG antibody against H. pylori which does 
not differentiate past and present infection, therefore, 
this could have also contributed in higher prevalence rate 
than this study. 
Although there is no significant difference in prevalence 
of  H. pylori among the age groups, there is an increasing 
trend in prevalence with increase in age groups, which is 
in contrast to the previous studies. The similar trend has 
also been seen in other studies conducted by (Rodrigo 
et al 1997; Koch et al 2005)in Spain and Greenland 
respectively.
The most common cause of  dyspepsia was found to be 
gastritis through histological examination which was in 
concurrence with endoscopic results. Furthermore, this 
study showed that 61.8% of  patients with gastritis had H. 
pylori infection and this is in consistent with other studies 
conducted in Nigeria (Jemilohun et al. 2010; Ndububa et 

al. 2001). Unlike other studies, this study showed gastric 
and duodenal ulcers have lesser association with H. 
pylori compared to gastritis which was comparable with 
the study conducted by Olubuyide and his colleagues in 
Nigeria (Olubuyide et al. 1989).
One of  the key limitations of  this study is that it 
was hospital-based setting and may not be a true 
representation of  the prevalence of  H. pylori among 
dyspeptics in the general population of  the Central region 
of  Bhutan. Further, the study was carried out only in one 
centre, therefore, this study calls for a community-based 
which would be more representative. Also since this study 
was also a retrospective cohort study, data collection was 
limited to the information available in hospital records. 
The records did not include information on risk factors 
for H pylori infection such as social, economic and other 
determinants.

Conflict of  Interest
There is no conflict of  interest among authors

Acknowledgement
We would like to acknowledge and thank Mr Tsheten, Mr 
Binay Thapa, the staff  of  CRRH rendering full support 
during the whole study period and staff  of  JDWNRH 
involved in the study in any way.  

CONCLUSION
In conclusion, this study found high prevalence of  H. 
pylori infection in concurrence and comparable with other 
developing countries. Also, there is a strong association 
between gastritis and H. Pylori infection which suggests 
treatment of  H. pylori infection may be a priority choice 
while managing gastritis in the hospital set up.

Limitation of  The Study
Some of  the limitations were: only ambulant population 
who visited the hospital for UGIE were performed 
endoscopy. Other patients from other districts who 
were not referred to the Gelephu Regional Referral 
hospital were missed. Moreover, patients refusing or not 
consenting for UGIE were also missed for the procedures. 

REFERENCES
Salih, B.A. (2009). Helicobacter pylori infection in developing 

countries: the burden for how long? Saudi journal 
of  gastroenterology. Official Journal of  the Saudi 
Gastroenterology Association,15(3), 201-7. 

Van Duynhoven, Y. T., & de Jonge, R. (2001). Transmission 
of  Helicobacter pylori: a role for food? Bulletin of  the 
World Health Organization, 79(5), 455-60. 

Kaur G, Naing NN. (2003). Prevalence and ethnic 
distribution of  helicobacter pylori infection among 

https://journals.e-palli.com/home/index.php/ajmsi


Pa
ge

 
50

https://journals.e-palli.com/home/index.php/ajmsi

Am. J. Med. Sci. Innov. 2(1) 47-50, 2023

endoscoped patients in north eastern peninsular 
malaysia. The Malaysian journal of  medical sciences: 
MJMS., 10(2), 66-70. 

Malaty, H. M., Kim, J. G., Kim, S. D., & Graham, D. Y. 
(1996). Prevalence of  Helicobacter pylori infection in 
Korean children: inverse relation to socioeconomic 
status despite a uniformly high prevalence in adults. 
American Journal of  Epidemiology, 143(3), 257-62. 

Bardhan PK. (1997). Epidemiological features of  
Helicobacter pylori infection in developing countries. 
Clinical infectious diseases : An official publication of  the 
Infectious Diseases Society of  America., 25(5), 973-8. 

McColl KE. (2010). Clinical practice. Helicobacter pylori 
infection. The New England journal of  medicine., 362(17), 
1597-604. 

Shiota S, Mahachai V, Vilaichone RK, Ratanachu-ek T, 
Tshering L, Uchida T, et al. (2013). Seroprevalence of  
Helicobacter pylori infection and gastric mucosal atrophy 
in Bhutan, a country with a high prevalence of  gastric 
cancer. J Med Microbiol., 62(10), 1571-8. 

Dendup T, Richter JM, Yamaoka Y, Wangchuk K, 
Malaty HM. (2015). Geographical distribution of  
the incidence of  gastric cancer in Bhutan. World J 
Gastroenterol., 21(38), 10883-9. 

Dorji D, Dendup T, Malaty HM, Wangchuk K, Yangzom 
D, Richter JM. (2014). Epidemiology of  Helicobacter 
pylori in Bhutan: the role of  environment and 
Geographic location. Helicobacter. 19(1), 69-73. 

Vilaichone RK, Mahachai V, Shiota S, Uchida T, 
Ratanachu-ek T, Tshering L, et al. (2013). Extremely 
high prevalence of  Helicobacter pylori infection in 
Bhutan. World J Gastroenterol., 19(18), 2806-10. 

El-Zimaity HM. (2000).  Accurate diagnosis of  Helicobacter 

pylori with biopsy. Gastroenterol Clin North Am., 29(4), 
863-9. 

Megraud F, Brassens-Rabbe MP, Denis F, Belbouri A, Hoa 
DQ. (1989). Seroepidemiology of  Campylobacter 
pylori infection in various populations. Journal of  
clinical microbiology., 27(8), 1870-3. 

Rodrigo Saez L, Riestra Menendez S, Fernandez 
Rodriguez E, Fernandez Velazquez MR, Garcia 
Alonso S, Lauret Brana ME. (1997).  Epidemiological 
study of  the prevalence of  Helicobacter pylori infection 
in the general population in Asturias, Spain. Rev Esp 
Enferm Dig., 89(7), 511-22.

Koch A, Krause TG, Krogfelt K, Olsen OR, Fischer 
TK, Melbye M. (2005). Seroprevalence and risk 
factors for Helicobacter pylori infection in Greenlanders. 
Helicobacter., 10(5), 433-42. 

Jemilohun AC, Otegbayo JA, Ola SO, Oluwasola OA, 
Akere A. (2010). Prevalence of  Helicobacter pylori 
among Nigerian patients with dyspepsia in Ibadan. 
Pan Afr Med J., 6(18). 

Ndububa DA, Agbakwuru AE, Adebayo RA, Olasode 
BJ, Olaomi OO, Adeosun OA, et  al. (2001). Upper 
gastrointestinal findings and incidence of  Helicobacter 
pylori infection among Nigerian patients with 
dyspepsia. West Afr J Med., 20(2), 140-5. 

Olubuyide IO, Atoba MA, Ayoola EA. (1989). Dyspepsia 
in Ibadan. Trop Geogr Med., 41(4), 337-40. 

Ratha-korn vilaichone, Natsuda Aumpan, Thawee 
Ratanachu-ek, (2020). Lotay Tshering……
Population-based study of  Helicobacter pylori infection 
and antibiotic resistance in Bhutan. International Journal 
of  Infectious Diseases.

https://journals.e-palli.com/home/index.php/ajmsi

