RESEARCH ARTICLE


The Magnitude and associated factors of Helicobacter Pylori Infection among Dyspeptic Patients at the Arba Minch General Hospital in Southern Ethiopia



Dagninet Alelign1, *, Goshu Furo1, Maykil Degu1, Dagimawie Tadesse1, Gebre Kayta1, Aschalew Kidanewold1
1 Department of Medical Laboratory Sciences, College of Medicine and Health Sciences, Arba Minch University, Arba Minch, Ethiopia


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Creative Commons License
© 2023 Alelign et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

* Address correspondence to this author at the Department of Medical Laboratory Sciences, College of Medicine and Health Sciences, Arba Minch University, Arba Minch, Ethiopia; Tel: +251-964-428-118; E-mail: dagninet.alelign@gmail.com


Abstract

Background:

Infection with Helicobacter pylori (H. pylori) is a major public health problem, with a higher prevalence reported in developing countries, including Ethiopia. Persistent H. pylori infection could result in chronic gastritis, duodenal ulcers, and subsequently gastric carcinoma. However, the burden of the infection varies within and between countries.

Methods:

An institution-based cross-sectional study was carried out on 422 adult dyspeptic patients attended at Arba Minch General Hospital from March 1st to June 30th, 2022. Pretested structured questionnaires were used to collect socio-demographic characteristics, clinical information, and other related factors for H. pylori infection. Stool samples were analyzed using the H. pylori fecal antigen rapid test kit. The data was analyzed using SPSS version 25. The p-value < 0.05 was considered statistically significant.

Results:

The overall magnitude of H. pylori was found to be 32.2% (136/422), with a 95% CI = (27.7-36.5). The highest proportion of H. pylori occurred in male study participants (55.1%) and in participants aged 31-40 years (42.6%). H. pylori stool antigen positivity was significantly associated with alcohol consumption [AOR = 1.87, 95% CI: (1.06-3.29)], smoking cigarettes [AOR = 2.75, 95% CI: (1.43-5.27)], and hand washing practice after the toilet [AOR = 3.02, 95% CI: (1.41-6.48)].

Conclusion:

Overall, a considerable magnitude of H. pylori was identified in the setting. Alcohol consumption, smoking cigarettes, and hand washing practice after using the toilet were found to be statistically significantly associated with H. pylori infection. Health education is therefore essential, particularly regarding societal lifestyle changes and knowledge of the potential sources of infection and H. pylori transmission.

Keywords: Helicobacter pylori, Stool antigen, Dyspeptic, Arba Minch, Ethiopia, Alcohol consumption, Cigarettes, Stool samples.



1. INTRODUCTION

Infection with Helicobacter pylori (H. pylori) is a major public health problem both in developed and developing countries, with varying levels of prevalence. The global systematic review shows that approximately 4.4 billion people worldwide are estimated to be positive for H. pylori, with a high burden in developing countries [1, 2]. According to epidemiologic studies, approximately 20-50% of developed-country populations and 70-90% of developing-country populations (nearly 80% among the elderly) are H. pylori positive, while only 10-20% of infected individuals experience symptoms [3-5].

H. pylori is the principal species of the genus Helicobacter, which is a Gram-negative bacillus that is tiny, curved, highly mobile, and biochemically positive for urease, catalase, and oxidase and is known to repeatedly colonize the human stomach [1, 5-7]. The pathogen is acquired via the fecal-oral, or oral-oral, route, though the exact route of transmission is unknown, and if left untreated, it can persist throughout life [2-6]. H. pylori infection is clinically characterized by stomach aches or burning pain, stomach pain that may be worse when your stomach is empty, nausea, loss of appetite, frequent burping, bloating, and unintentional weight loss [2-10].

H. pylori plays a significant role in the pathogenesis of chronic gastritis, peptic ulcer disease (PUD), mucosa-associated lymphoid tissue (MALT) lymphoma, and gastric adenocarcinoma, which is the third most deadly cancer in the world [5-10]. In Africa, H. pylori infection is thought to be the root cause of about 70% of stomach ulcers and 90% of duodenal ulcers, respectively [5, 11-14]. Additionally, numerous extra-gastric disorders have been studied for the potential involvement of H. pylori, including neuro- degeneration, nonalcoholic fatty liver disease, iron deficiency anemia, idiopathic thrombocytopenic purpura, and vitamin B12 insufficiency [5, 7, 13, 14]. However, differences in virulence and the ensuing interactions with host and environmental variables result in variations in disease expression [3, 4, 11, 12].

The prevalence of H. pylori varies from one geographical location to another; within a country, it is possible to have a different prevalence considering age, ethnicity, level of literacy, socioeconomic status, environmental factors, and diagnostic techniques [4-7]. Statistical studies have also revealed the burden of H. pylori infection in continental terms as 69.4% in South America, 37.1% in North America, 34.3%-47.0% in Western Europe, 24.4% in Oceania, 54.6% in Asia, and 79.1% in Africa [2-5, 15, 16]. Infection rates are higher in developing countries due to low socioeconomic status, overcrowding, poor housing, poor sanitation (both personal and environmental hygiene), contaminated water supplies, animal feces accumulation, and food contamination [6, 7, 17-20].

The prevalence of H. pylori in Ethiopia shows remarkable variations from place to place as well as from study to study, even in the same setting [2, 4]. In dyspeptic Ethiopian patients, the prevalence of H. pylori infection varies from 17.7% to 91% across the country [4, 11, 12, 17-25]. However, the majority of the previous prevalence research was conducted using antibody rapid tests, which have questionable performance in detecting acute infection and distinguishing active infection from previous exposure. Besides, there is a paucity of data, particularly in the study setting, about the prevalence of H. pylori infection and its associated factors. Hence, the current study aimed to determine the prevalence and associated factors of H. pylori infection using a stool antigen test among dyspeptic patients at Arba Minch General Hospital in southern Ethiopia.

2. MATERIALS AND METHODS

2.1. Study Design and Area

An institution-based cross-sectional study was conducted at the outpatient department of Arba Minch General Hospital, Southern Ethiopia, from March 1st to June 30th, 2022. The hospital is located in Arba Minch town in Gamo Zone, Southern Nations, Nationalities, and Peoples (SNNP), Southern Ethiopia. Arba Minch is the seat of administration for the Gamo zone, which is located 454 km from the capital city of Ethiopia (Addis Ababa). Arba Minch General Hospital was established in 1961 E.C. during Empierer Hailesilasie and provides preventive, curative, and rehabilitative care for more than 1.5 million people from the Gamo zone and other nearby zones.

2.2. Population and Eligibility Criteria

The study population consisted of all adult dyspeptic patients who provided stool samples in the outpatient department during the study period; patients who had taken antibiotics within the previous two weeks and those who were unable to reply were excluded.

2.3. Sample Size Determination and Sampling Technique

The sample size was computed by using the single population proportion formula, taking the 51.4% prevalence of H. pylori infection in adult dyspeptic patients from a previous study done in Hadiya Zone, Southern Ethiopia [2], and by considering a 95% confidence interval (Zα/2= 1.96), and a 5% margin of error. The total of 422 sample sizes were determined using a consecutive sampling technique after accounting for the 10% non-response rate.

2.4. Data Collection

Data on the socio-demographic (gender, age, marital status, residence, occupational status, and educational status) and personal habit (smoking, alcohol intake, and coffee consumption) characteristics of the study participants were gathered at the outpatient department (OPD) using a pretested structured questionnaire through face-to-face interviews.

2.5. Sample Collection and Processing

Following instructions on collecting quality fecal samples, every study participant provided approximately two grams of stool in a clean, leak-proof, screw-capped plastic container. The stool samples were subsequently transferred to a vial with diluents, rapidly agitated, and after two minutes of resting the tube, two to three drops (80µL) were dropped into the round window of the test kit. The presence of H. pylori stool antigen was detected using a HENSO Medical (Hangez HOUS, O.Ltd.) rapid test kit with a monoclonal anti-H. pylori antibody conjugated with a colloid gold nitrocellulose membrane based on a lateral flow chromatographic immunoassay technique with 96.9% sensitivity and 99.2% specificity [2, 21, 22].

2.6. Data Quality Assurance

To ensure data quality, pre-testing on 5% of the sample size was performed at Arba Minch Dilfana Primary Hospital, and appropriate precautions were taken throughout the data collecting and laboratory work processes. Standard Operating Procedures (SOPs) were meticulously followed at every step in accordance with the manufacturer's guidelines.

2.7. Ethical Clearances

The study was conducted after it was ethically reviewed and approved by the Ethical Committee of the Department of Medical Laboratory Sciences at Arba Minch University (Ref. No. MeLT/06/14). Permission was obtained from Arba Minch General Hospital. Informed written consent was obtained from each participant before data collection. All conventional safety measures were taken to prevent COVID-19, including wearing a mask and using personal protective equipment when collecting and processing the sample. All the information obtained from the study subjects was coded to be maintained confidentially. Positive laboratory results were reported to the respective patients’ physicians to receive proper treatment and counseling.

2.8. Data Processing and Analysis

Data processing and analysis were done using the Statistical Package for the Social Sciences, version 25. Descriptive statistics like frequency, mean, and percentage were calculated. Logistic regression analysis was applied to identify predictor variables associated with H. pylori infection. A bivariate logistic regression analysis was used to assess associated factors. Variables with a p-value less than 0.25 in the bivariable analysis were jointly entered into a multivariable analysis. The presence of associations and statistical significance was determined at a p-value less than or equal to 0.05.

3. RESULTS

3.1. Socio-demographic Characteristics of the Study Participants

A total of 422 suspected adult patients participated in the study. About 235 (55.7%) patients were male. The mean (±SD) age of the study population was 31 ± 11.4 years, with a range of 18 to 63 years. Among the age distribution, 173 (41% of the study participants) were in the 31-40 age group. The majority of the study participants (57.1%) lived in rural areas, and more than half (58.9%) had more than four family members (Table 1).

The overall magnitude of H. pylori infection was 32.2% (136/422). The prevalence was higher among males (55.1%) than females (44.9%). Participants aged 31-40 years had the highest frequency of H. pylori infection (42.6%). In terms of marital status, it was discovered that married people had the highest prevalence of the infection (50.7%), followed by unmarried (33.8%), whereas 52.2% of H. pylori infections were identified in rural residents. However, none of the socio-demographic characteristics were statistically significant (P > 0.05) (Table 1).

3.2. Environmental and Behavioral Characteristics

Among the total number of study participants, 20.1% of them had an unprotected drinking water source. A total of 34.6% of study participants had the habit of drinking alcohol three or more times per week, while 20.9% of participants were habitual of smoking cigarettes, and 81% of the participants had the habit of drinking coffee more than two cups per day. Moreover, 17.1% of the study participants did not wash their hands after toilet visits (Table 2).

Among the study participants with a habit of alcohol drinking, coffee drinking, and cigarette smoking, the H. pylori infection rate was 55.9%, 77.1%, and 40.4%, respectively. Participants in the study who drank from unprotected water sources and those who never washed their hands after visiting the toilet were found to have infection rates of 25.7% and 26.5% of H. pylori, respectively. Moreover, patients who had alcohol three or more times per week, regardless of type or dose, were 1.87 times more likely to develop H. pylori infection [AOR = 1.87, 95% CI: (1.06-3.29), p = 0.030], whereas cigarette smokers were 2.75 times more likely [AOR = 2.75, 95% CI: (1.43-5.27), p = 0.002]. Likewise, being unable to wash hands after a toilet visit increased the chance of H. pylori infection by 3.02 times [AOR = 3.02, 95% CI: 1.41-6.48), p = 0.005] (Table 2).

Table 1. Magnitude of H. pylori infection in relation to socio-demographic characteristics among dyspeptic patients at Arba Minch general hospital, 2022.
Variables Categories H. pylori Infection (%) COR (95% CI) AOR (95% CI) P-value
Positive (%) Negative (%)
Gender Male 75 (55.1) 160 (55.9) 0.97 (0.64-1.46) 1.305 (0.51-3.37) 0.582
Female 61 (44.9) 126 (44.1) 1 1 -
Age (year) 18-30 43 (31.6) 63 (22.0) 0.74 (0.45-1.22) - -
31-40 58 (42.6) 115 (40.2) 0.48 (0.26-0.86) - -
41-50 24 (17.6) 74 (25.9) 0.47 (0.22-1.03) - -
>51 11 (8.1) 34 (11.9) 1 - -
Residence Urban 65 (47.8) 116 (40.6) 1 - -
Rural 71 (52.2) 170 (59.4) 0.75 (0.49-1.12) - -
Marital Status Single 46 (33.8) 101 (35.3) 0.85 (0.34-2.16) - -
Married 69 (50.7) 144 (50.3) 0.89 (0.36-2.22) - -
Divorced 13 (9.6) 26 (9.1) 0.94 (0.32-2.78) - -
Widowed 8 (5.9) 15 (5.2) 1 - -
Occupation Farmer 14 (10.3) 34 (11.9) 0.94 (0.45-2.00) 0.96 (0.37-2.45) 0.925
Daily labour 23 (16.9) 35 (12.2) 1.51 (0.77-2.95) 1.85 (0.74-4.56) 0.184
Merchant 41 (30.1) 76 (26.6) 1.24 (0.70-2.18) 0.92 (0.25-3.33) 0.897
Student 27 (19.9) 70 (24.5) 0.88 (0.48-1.63) 0.37 (0.10-1.32) 0.126
Employee 31 (22.8) 71 (24.8) 1 1 -
Educational Status Illiterate 10 (7.4) 12 (4.2) 1.17 (0.47-2.91) 0.48 (0.13-1.78) 0.271
Primary school 23 (16.9) 75 (26.2) 0.43 (0.24-0.78) 0.24 (0.08-0.71) 0.011
Secondary school 53 (39.0) 129 (45.1) 0.58 (0.36-0.93) 0.39 (0.19-0.85) 0.018
College & above 50 (36.8) 70 (24.5) 1 1 -
Family Size < 4 52 (38.2) 121 (42.3) 1 - -
> 4 84 (61.8) 165 (57.7) 1.19 (0.78-1.79) - -
Note: *Statistically Significant Variables Abbreviations: AOR: Adjusted Odds Ratio; CI: Confidence Interval; COR: Crude Odds Ratio.
Table 2. The magnitude of H. pylori infection in relation to environmental factors and behavioral habits among dyspeptic patients at arba minch general hospital, 2022.
Variables Categories H. pylori Infection COR (95% CI) AOR (95% CI) P-value
Positive (%) Negative (%)
Drinking water source Pipe water 101 (74.3) 236 (82.5) 1 1 -
Unprotected water 35 (25.7) 50 (17.5) 1.64 (1.00-2.67) 1.03 (0.49-2.16) 0.934
Alcohol drinking Yes 76 (55.9) 70 (24.5) 3.91 (2.54-6.03) 1.87 (1.06-3.29) 0.030*
No 60 (44.1) 216 (75.5) 1 1 -
Coffee drinking Yes 106 (77.9) 236 (82.5) 1.34 (0.80-2.21) - -
No 30 (22.1) 50 (17.5) 1 - -
Cigarette smoking Yes 55 (40.4) 33 (11.5) 5.21 (3.16-8.57) 2.75 (1.43-5.27) 0.002*
No 81 (59.6) 253 (88.5) 1 1 -
Defecation practice Toilet 118 (86.8) 254 (88.8) 1 1 -
Open FD 18 (13.2) 32 (11.2) 0.83 (0.45-1.53) 1.45 (0.68-3.06) 0.33
Hand washing practice after toilet Yes 100 (73.5) 250 (87.4) 1 1 -
No 36 (26.5) 36 (12.6) 2.50 (1.49-4.19) 3.02 (1.41-6.48) 0.005*
Note: Open FD = Open field defecation; Unprotected water = underground, river, and ponds. Abbreviations: *Statistically Significant; AOR: Adjusted Odds Ratio; CI: Confidence Interval; COR: Crude Odds Ratio.

4. DISCUSSION

There has been a lot of variation in the prevalence of H. pylori infection reported across Ethiopia, even within the same geographic area, because of things like processing sample and method deference, geographic location, and socioeconomic, behavioral, environmental, and clinical factors, all of which have a big impact [2, 4, 26-28]. The current study determined an overall magnitude of H. pylori stool antigen positivity in adults (≥18 years old) with dyspepsia of 32.2% with a 95% CI of (27.7-36.5). This magnitude was comparable with studies in Dessie 30.4% [19], Addis Ababa 36.8% [26], Gonder, Ethiopia 37.6% [23], Canada 29.4% [27], and Uganda 35.7% [7]. On the contrary, a lower rate of H. pylori infection was reported in Yirga Cheffe, Southern Ethiopia, at 7.7% [17]. However, our finding was lower than those of studies conducted in various parts of Ethiopia, with prevalence rates ranging from 49.2% to 91% [2, 4, 24, 25, 28], and studies conducted in different parts of the world, with prevalence rates ranging from 40.9% to 87.7% [6, 29-33]. The disparity could be explained by a difference in the study area, sample size, study population, personal hygienic conditions, socioeconomic status, and lifestyle, as well as behavioral factors of study participants. Despite these factors, the difference in testing methodology as well as the sensitivity and specificity of the employed serological tests may affect the detection rate of H. pylori. In fact, antibody tests do not differentiate between current and past infections.

In this study, the prevalence of H. pylori infection in male participants (55.1%) was higher than that in females. In line with previous studies done in Ethiopia [12, 19], the difference was not statistically significant. In contrast, previous studies done in Ethiopia [2, 11, 21, 22, 34] and in Nakuru, Kenya [35] reported that the rate of H. pylori infection should be statistically associated with sex, although the exact preferences for sex are not well documented. The variation in prevalence between males and females could probably be due to the difference in lifestyles, exposure to potential environmental sources, and habits such as smoking and alcohol consumption.

In this study, age had no significant association with H. pylori infection (p > 0.05), which is in line with previous reports from Ethiopia [2, 4, 19]. In contrast, there are studies in Ethiopia that show a significant association between age and H. pylori infection [12, 21, 34]. These differences might be influenced by the participants’ age range. In our study, it ranged from 18 to 63 years old. Likewise, in this study, there was no statistically significant difference in the prevalence of H. pylori with respect to family size in the household, which is contrary to previous studies done in Ethiopia [19, 21]. All these findings are consistent with the concept that the most important factors influencing the transmission of infection may differ with socio-demographic features, geographical location, and study population.

In this study, drinking alcohol was shown to be significantly associated with the rate of H. pylori stool antigen positivity (P = 0.030). This result agrees with studies done in different areas of Ethiopia [2, 19, 4, 12, 34]. The reason might be that frequent alcohol consumption affects the contribution of the intestinal microbial populations by disturbing the balance of intestinal homeostasis as well as by damaging gastric mucosa with a significant alteration of the immune system, which facilitates the colonization of H. pylori [4, 12, 36]. Besides, heavy drinking can possibly predispose consumers to social contacts that favor transmission of the H. pylori infection [4, 12]. However, there are studies that support a preventive effect of alcohol consumption against active H. pylori infection on the assumption that (a) alcohol may have a protective anti-bactericidal effect against new H. pylori infection; (b) alcohol may be bactericidal against existing H. pylori; and (c) alcohol causes repeated local damage to the gastric mucosa, which accelerates atrophic changes and causes H. pylori auto-eradication [2, 36, 37].

Cigarette smoking was another behavioral factor associated with H. pylori stool antigen positivity (P = 0.002), which is consistent with a previous study conducted in Butajira, Ethiopia [12]. This could possibly be due to using nicotine, which promotes chronic stomach inflammation, reduces mucosal blood flow, reduces mucus and epidermal growth factor secretion, and impairs the immune system. This, in turn, facilitates H. pylori colonization and makes infection difficult to eradicate [12, 38]. However, this contradicts the assumption hypothesized by studies done in Tokyo [36] and Porto, Portugal [39], which is that the elevated acid and pepsin secretion caused by smoking protect the gastric mucosa from H. pylori infections.

On the other hand, study participants who did not wash their hands after visiting the toilet had a higher chance of having an H. pylori infection (P = 0.005). This is in agreement with previous studies done in Ethiopia [4, 21, 34]. The assumption is that poor personal and environmental hygiene plays a great role in the transmission of H. pylori bacteria, and this finding supports the notion of an oral-oral or fecal-oral route with or without intermediate vectors of transmission, which is thought to be the primary route of transmission [1, 2, 4, 5]. Lack of proper sanitation and basic hygiene after using the toilet, therefore, can be a source of infection and increase the chance of acquiring H. pylori.

5. LIMITATIONS OF THE STUDY

The limitations of the present study include the cross-sectional study design with consecutive sampling technique and the fact that it was limited to only adult patients with dyspepsia in a single institution, which may not infer the prevalence of H. pylori infection in the general population. In addition, alcohol consumption data with regard to type, amount, and duration was not gathered. Moreover, body mass index (BMI), ABO blood grouping, and anemia status of dyspeptic patients as well as the prognosis of the patient were not considered in this study due to budget and resource constraints.

CONCLUSION

This study demonstrated that the magnitude of H. pylori among our study population was less as compared to the findings quoted in previous studies. Lifestyle factors such as alcohol consumption, cigarette smoking, and hand washing practice after toilet visits were found to be risk factors for H. pylori infection. However, no significant association was observed between other socio-demographic variables and H. pylori stool antigen detection. However, the given magnitude of H. pylori that we identified, it is essential to develop and implement intervention strategies, particularly those that focus on modifying social lifestyles to prevent transmission and, in turn, lessen the clinical effects of infection. Moreover, large-scale cohort-type community-based studies are needed to better characterize and formulate a cause-and-effect relationship between the risk factors and H. pylori infection.

AUTHORS’ CONTRIBUTIONS

Dagninet Alelign conceived, designed, and drafted the manuscript; all other authors made substantial contributions to conception and design; acquisition of data, or analysis and interpretation of data; agreed to submit to the current journal; gave final approval of the version to be published; and agreed to be accountable for all aspects of the work.

LIST OF ABBREVIATIONS

AOR = Adjusted Odds Ratio
CI = Confidence Interval
COR = Crude Odds Ratio

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study was conducted after it was ethically reviewed and approved by the Ethical Committee of the Department of Medical Laboratory Sciences at Arba Minch University (Ref. No. MeLT/06/14).

HUMAN AND ANIMAL RIGHTS

No animals were used in this research. All procedures performed in studies involving human participants were in accordance with the ethical standards of institutional and/or research committees and with the 1975 Declaration of Helsinki, as revised in 2013.

CONSENT FOR PUBLICATION

Informed written consent was obtained from each participant before data collection.

STANDARDS OF REPORTING

STROBE guidelines were followed.

AVAILABILITY OF DATA AND MATERIALS

The datasets analyzed during the current study are only available from the corresponding author [D.A] upon reasonable request.

CONFLICT OF INTEREST

The authors declare no conflict of interest financial or otherwise.

FUNDING

The project was supported by the Department of Medical Laboratory Sciences of Arba Minch University College of Medicine and Health Sciences.

ACKNOWLEDGEMENTS

We acknowledge the involvement of Abenezer Dugo, Zerubbabel Tesfaye, and Abubeker Ali as well as health professionals at Arba Minch General, in data collection. We appreciate the technical and financial support provided by the Department of Medical Laboratory Sciences of Arba Minch University College of Medicine and Health Sciences. Our gratitude also goes out to the study participants for agreeing to take part in the research.

REFERENCES

[1] Hooi JKY, Lai WY, Ng WK, et al. Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 2017; 153(2): 420-9.
[2] Kahase D, Haile K. Helicobacter pylori infection and predictors among dyspeptic adult patients in southwest ethiopia: Cross-sectional study. Res Rep Trop Med 2020; 11: 141-7.
[3] Smith S, Fowora M, Pellicano R. Infections with Helicobacter pylori and challenges encountered in Africa. World J Gastroenterol 2019; 25(25): 3183-95.
[4] Melese A, Genet C, Zeleke B, Andualem T. Helicobacter pylori infections in Ethiopia; prevalence and associated factors: a systematic review and meta-analysis. BMC Gastroenterol 2019; 19(1): 8.
[5] Smith SI, Ajayi A, Jolaiya T, et al. Helicobacter pylori infection in Africa: update of the current situation and challenges. Dig Dis 2022; 40(4): 535-44.
[6] Kouitcheu Mabeku LB, Noundjeu Ngamga ML, Leundji H. Potential risk factors and prevalence of Helicobacter pylori infection among adult patients with dyspepsia symptoms in Cameroon. BMC Infect Dis 2018; 18(1): 278.
[7] Namyalo E, Nyakarahuka L, Afayoa M, et al. Prevalence of helicobacter pylori among patients with gastrointestinal tract (git) symptoms: a retrospective study at selected Africa air rescue (AAR) Clinics in Kampala, Uganda, from 2015 to 2019. J Trop Med 2021; 2021: 9935142.
[8] Alharbi R, Ghoraba M. Prevalence and patient characteristics of Helicobacter pylori among adult in primary health care of security forces hospital Riyadh, Saudi Arabia, 2018. J Family Med Prim Care 2019; 8(7): 2202-6.
[9] Adlekha S, Chadha T, Krishnan P, Sumangala B. Prevalence of helicobacter pylori infection among patients undergoing upper gastrointestinal endoscopy in a medical college hospital in Kerala, India. Ann Med Health Sci Res 2013; 3(4): 559-63.
[10] Zamani M, Ebrahimtabar F, Zamani V, et al. Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 2018; 47(7): 868-76.
[11] Alebie G, Kaba D. Prevalence of Helicobacter pylori infection and associated factors among gastritis students in Jigjiga University, Jigjiga, Somali regional state of Ethiopia. J Bacteriol Mycol (Monroe Township) 2016; 3(3): 00060.
[12] Kibru D, Gelaw B, Alemu A, Addis Z. Helicobacter pylori infection and its association with anemia among adult dyspeptic patients attending Butajira Hospital, Ethiopia. BMC Infect Dis 2014; 14(1): 656.
[13] Durazzo M, Adriani A, Fagoonee S, Saracco GM, Pellicano R. Helicobacter pylori and respiratory diseases: 2021 update. Microorganisms 2021; 9(10): 2033.
[14] Doulberis M, Kotronis G, Gialamprinou D, et al. Alzheimer’s disease and gastrointestinal microbiota; impact of Helicobacter pylori infection involvement. Int J Neurosci 2021; 131(3): 289-301.
[15] Hunt RH, Xiao SD, Megraud F, et al. World Gastroenterology Organisation Global Guideline: Helicobacter pylori in developing countries. J Clin Gastroenterol 2011; 45(5): 383-8.
[16] Archampong TN, Asmah RH, Wiredu EK, Gyasi RK, Nkrumah KN, Rajakumar K. Epidemiology of Helicobacter pylori infection in dyspeptic Ghanaian patients. Pan Afr Med J 2015; 20(1): 178.
[17] Ayele B, Molla E. Dyspepsia and Associated Risk Factors at Yirga Cheffe Primary Hospital, Southern Ethiopia. Clin Microbiol 2017; 6(3): 3.
[18] Asrat D, Nilsson I, Mengistu Y, et al. Prevalence of Helicobacter pylori infection among adult dyspeptic patients in Ethiopia. Ann Trop Med Parasitol 2004; 98(2): 181-9.
[19] Seid A, Demsiss W. Feco-prevalence and risk factors of Helicobacter pylori infection among symptomatic patients at Dessie Referral Hospital, Ethiopia. BMC Infect Dis 2018; 18(1): 260.
[20] Negash M, Wondifraw Baynes H, Geremew D. Helicobacter pylori infection and its risk factors: a prospective cross-sectional study in resource-limited settings of Northwest Ethiopia. Canadian J Infect Dis Med Microbiol 2018; 2018: 9463710.
[21] Hailu G, Desta K, Tadesse F. Prevalence and risk factors of Helicobacter pylori among adults at Jinka Zonal hospital, Debub Omo Zone, Southwest Ethiopia. Autoimmune Infect Dis 2016; 2(2): 1-8.
[22] Dilnessa T, Amentie M. Prevalence of Helicobacter pylori and risk factors among dyspepsia and non-dyspepsia adults at Assosa General Hospital, West Ethiopia: A comparative study. Ethiop J Health Dev 2017; 31(1): 4-12.
[23] Kasew D, Abebe A, Munea U, et al. Magnitude of Helicobacter pylori among dyspeptic patients attending at University of Gondar Hospital, Gondar, Northwest Ethiopia. Ethiop J Health Sci 2017; 27(6): 571-80.
[24] Taddesse G, Habteselassie A, Desta K, Esayas S, Bane A. Association of dyspepsia symptoms and Helicobacter pylori infections in private higher clinic, Addis Ababa, Ethiopia. Ethiop Med J 2011; 49(2): 109-16.
[25] Kebede W, Abebe G. H. Pylori Prevalence and Its Effect on CD4+ Lymphocyte Count in Active Pulmonary Tuberculosis Patients at Hospitals in Jimma, Southwest Ethiopia. Int J Immunol 2015; 3(1): 7.
[26] Shiferaw G, Abera D. Magnitude of Helicobacter pylori and associated risk factors among symptomatic patients attending at Jasmin internal medicine and pediatrics specialized private clinic in Addis Ababa city, Ethiopia. BMC Infect Dis 2019; 19(1): 118.
[27] Naja F, Kreiger N, Sullivan T. Helicobacter pylori infection in Ontario: prevalence and risk factors. Can J Gastroenterol 2007; 21(8): 501-6.
[28] Birru Haile T, Gelana Tiki T. Trends in the occurrence of Helicobacter pylori infection in Arada Sub-City: A 5-year retrospective study. Sinet Ethiop J Sci 2022; 45(1): 61-8.
[29] Mwangi CN, Njoroge S, Rajula A, et al. Prevalence and endoscopic findings of Helicobacter pylori infection among dyspeptic patients in Kenya. Open J Med Microbiol 2020; 10(4): 233-42.
[30] Mbang KA, Uchenna O, Emmanuel U, et al. Prevalence of Helicobacter pylori infection among dyspepsia patients in Calabar. Glob J Pure Appl Sci 2019; 25(2): 145-51.
[31] Akeel M, Elmakki E, Shehata A, et al. Prevalence and factors associated with H. pylori infection in Saudi patients with dyspepsia. Electron Physician 2018; 10(9): 7279-86.
[32] Wang W, Jiang W, Zhu S, et al. Assessment of prevalence and risk factors of helicobacter pylori infection in an oilfield Community in Hebei, China. BMC Gastroenterol 2019; 19(1): 186.
[33] Kharel S, Bist A, Shrestha S, Homagain S. Helicobacter pylori healthy South Asians. JGH Open 2020; 4(6): 1037-46.
[34] Abebaw W, Kibret M, Abera B. Prevalence and risk factors of H. pylori from dyspeptic patients in northwest Ethiopia: a hospital based cross-sectional study. Asian Pac J Cancer Prev 2014; 15(11): 4459-63.
[35] Shmuely H, Obure S, Passaro DJ, et al. Dyspepsia symptoms and Helicobacter pylori infection, Nakuru, Kenya. Emerg Infect Dis 2003; 9(9): 1103-7.
[36] Ogihara A, Kikuchi S, Hasegawa A, et al. Relationship between Helicobacter pylori infection and smoking and drinking habits. J Gastroenterol Hepatol 2000; 15(3): 271-6.
[37] Du P, Zhang C, Wang A, Ma Z, Shen S, Li X. Association of alcohol drinking and Helicobacter pylori infection: A meta-analysis. J Clin Gastroenterol 2021.
[38] Camargo MC, Piazuelo MB, Mera RM, et al. Effect of smoking on failure of H. pylori therapy and gastric histology in a high gastric cancer risk area of Colombia. Acta Gastroenterol Latinoam 2007; 37(4): 238-45.
[39] Ferro A, Morais S, Pelucchi C, et al. Smoking and Helicobacter pylori infection: an individual participant pooled analysis (Stomach Cancer Pooling- StoP Project). Eur J Cancer Prev 2019; 28(5): 390-6.