Seroprevalence of Helicobacter pylori Infection and Associated Factors Among Adult Dyspeptic Patients in Public Health Facilities, Mizan Aman Town, Southwest, Ethiopia: Institutional-Based Cross-Sectional Study.

BACKGROUND: Helicobacter pylori infection is a public health problem associated with chronic gastritis, peptic ulcer, and gastric cancer. It is endemic in developing countries like Ethiopia. This study was aimed to assess seroprevalence of H. pylori infection and associated factors among adults' dyspeptic patients in public health facilities of Mizan Aman Town, Southwest Ethiopia.
METHODS: Cross-sectional study was conducted in public health facilities of Mizan Aman Town, from April 1, 2018, to June 30, 2018. A total of 208 adult dyspeptic patients were included in the study. A structured questionnaire was used to collect data. Serum was tested for anti-H. pylori antibody using a commercial test strip. Data were entered using Epi info 6.04 and exported to SPSS 21 for analysis. Bivariate and multivariate logistic regression was employed and OR with 95% CI was retrieved. P-value of less than 0.05 was considered as statistically significant.
RESULTS: A total of 208 participants were interviewed. The mean age of respondents was 31.70 (SD ±9.123) years. Seroprevalence of H. pylori infection was 89 (42.8%). Presence of domestic animals (AOR = 13.33, 95% CI = (2.203-80.692)), sources of drinking water (AOR = 0.011, 95% CI = (0.001-0.110)), toilet type (AOR = 11.236, 95% CI = (1.921-65.73)), shared beds with siblings (AOR = 7.775, 95% CI = (1.676-36.082)), family size (AOR = 0.015, 95% CI = (0.003, 0.089)), storing and reusing water (AOR =0.014, 95% CI = (0.002-0.103)) and occupational status (AOR = 23.33, 95% CI = (2.034-67.661)) were variables significantly associated with seroprevalence of H. pylori.
CONCLUSION: Seroprevalence of H. pylori infection is relatively high in Ethiopia. Family size, shared bed, presences of domestic animals, storage and reuse of water, toilet type, sources of drinking water, and occupation were significant factors associated with H. pylori infection. The possible identified modifiable risk factors should be addressed through effective health education.

Introduction

Helicobacter pylori infection is a global public health problem and associated with chronic gastritis, and strongly linked to peptic ulcer diseases and gastric cancer. The bacterium is endemic in Africa and Asia.1 Its prevalence is highly variable in relation to geographical area, age, and socioeconomic factors; which is high in developing countries. Globally, different strains of H. pylori appear to be associated with differences in virulence, and the resulting interplay with host and environmental factors leads to subsequent differences in the epidemiology of infection.2,3

It has been well established that H. pylori is the cause of almost all duodenal ulcers and chronic benign gastric ulcers.4 The infection is found to be associated with gastritis, non-ulcer dyspepsia, duodenal ulcer, gastric ulcer, gastric cancer, and gastric lymphoma of mucosa-associated lymphoid tissue.5 Gastric cancer is a major global health threat and is the third leading cause of cancer deaths worldwide causing an estimated >720,000 deaths per year globally.6,7 Chronic H. pylori infection can also contribute to gastric mucosal instability by reducing gastric acid secretion.8

An epidemiological survey reveals that H. pylori infection is significantly higher in developing countries where the prevalence rate ranges between 70% and 90%, as compared to 20–50% in developed countries. The association between H. pylori infection and dyspeptic symptoms has long been established with H. pylori infection having high population attributable risk for dyspepsia.9 In Nigeria, various studies on H. pylori show prevalence rates between 73.0% and 94.5% among patients with dyspepsia10–12.

In developing countries, 70–90% of the population harbor H. pylori, which is mostly acquired during childhood.13 Transmission of H. pylori is largely through oral–oral or fecal-oral routes. A lack of proper sanitation, safe drinking water, basic hygiene, as well as poor diets and overcrowding, play a role in determining the overall prevalence of infection. Transmission of the bacterium is pronounced through poor environmental sanitation and crowding conditions including fecal contamination of water sources.2,14 In addition, the continuing emergence of resistance to the conventional anti-bacterial drugs used to treat H. pylori infections is challenging the eradication of H. pylori in developing countries.15,16

In Ethiopia, studies documented a high prevalence of H. pylori infection among adults in various localities.17,18 Planning and prevention measures that reduce the public health impact of H. pylori infection are critically needed. In this regard, investigating the epidemiology of the infection among the different segments of population is required to design effective intervention measures. Hence, the current study was aimed at the assessment of seroprevalence of H. pylori infection and associated factors among patients with dyspepsia in selected public health facilities in southwest Ethiopia.

Methods

Study Design and Setting

An institutional-based cross-sectional study was conducted in Mizan Tepi University Teaching Hospital (MTUTH) and Mizan health center, Bench Maji Zone, Southwest Ethiopia. The health facilities are located in Southwestern part of Ethiopia, Mizan Aman town, 561 km far from the capital city Addis Ababa. The town has a latitude and longitude of 7°0ʹN 35°35ʹE/7.000°N35.583°E, respectively, with an elevation of 1451 meters above sea level. The health facilities are expected to provide medical services for about 1 million people in Southwest Ethiopia and surroundings. The study was conducted from April 1, 2018 to June 30, 2018.

Source and Study Population

Adult dyspeptic patients aged ≥18 years based on ROME III criteria were included in the study. Patients with history of gastrectomy and who were critically ill and unable to give responses were excluded.

Sample Size Determination and Procedure

The minimum sample size (n) was determined by using single population proportion formula [n = (Z α/2)2 P (1-P)/d2], where Zα/2 = the value under standard normal table at 95% level of confidence which is 1.96, expected prevalence P, set at 85.6%, a previous study conducted in Gondar hospital, Ethiopia,19 d= precision which was set at 5%. Including 10% non-response rate, the final sample size was 208 dyspeptic patients.

The sample size was proportionally allocated to the two health facilities based on previous flow of dyspeptic patients through six months record review. Proportionally, a total of 139 dyspeptic patients from MTUTH and 69 dyspeptic patients from Mizan health center were selected consecutively.

Data Collection Tool and Procedure

Structured questionnaire which was adopted and modified from different reviewed literatures was used.19–21 Socio-demographic data included sex, age, ethnicity, and socio-economic factors and data on risk factors of H. pylori included smoking, diet, and alcohol consumption. The questionnaire was pretested among 5% of the sample size in other health institution before the actual data collection period. The coherence and skipping pattern of the questionnaire were corrected after the pretest.

Specimen Collection and Laboratory Procedure

Upon completion of the questionnaire, 3–5 mL of the venous blood sample was aseptically collected by trained laboratory professionals and serum sample was tested for anti-H. pylori antibody using a commercially available H. pylori serology test strip (HEXAGON H. PYLORI, Germany), following manufacturer’s instructions and interpreted accordingly. The kit has 97% sensitivity and 95% specificity compared with ELISA (HEXAGON H. PYLORI, Germany). Those participants tested positive results for the H. pylori serology test were asked to produce the stool when coming for the H. pylori serology test and the results were confirmed by the stool antigen test. The questionnaire was pre-tested and adequate supervision during data collection was made. The quality of the laboratory results was guaranteed by applying quality control measures during specimen collection and testing.

Operational Definitions

H. pylori Positive: Those participants whose serum result was reactive for the anti-H. pylori antibody test.

H. pylori Negative: Those participants whose serum result was non-reactive for an anti-H. pylori antibody test.

Adult: a human being whose age is 18 years and above who is expected to become sexually mature (According to Ethiopian National law).

Dyspepsia: Pain or discomfort centered in the central portion of the upper abdomen associated with a variety of symptoms such as fullness in the upper abdomen, early satiety, bloating or nausea or vomiting (ROME III criteria).

Educational status: refers to the highest level of education attended by the respondent during the time of the survey.

Income: for rural study participants calculated in kind the crop and cattle changed into monetary forms.

Data Processing and Analysis

Data were entered by using Epi info version 6.04 and exported into SPSS version 21 for cleaning, categorization, and analysis. The results were summarized using descriptive statistics including frequencies and proportions. Bivariate analysis was conducted to identify the association between each independent variable with the outcome variables. Multivariate analysis was employed to identify independent predictors associated with the outcome variables. In the multivariate analysis, adjusted odds ratio (AOR) and corresponding 95% confidence intervals were retrieved. Those variables with a p-value of less than 0.05 were considered as statistically significant.

Results

Socio-Demographic Characteristics of the Respondents

A total of 208 eligible participants were included in the study from selected public health institutions. The mean age of the respondents was 31.70 (SD ±9.123) years. Most of the participants, 87 (41.8%) were in the age range of 25–34 years. Of the total respondents, 123 (59.1%) were rural residents. Eighty-three (39.9%) of participants were not able to read and write (Table 1).

Table 1

Socio-Demographic Characteristics of the Respondents (n=208), Southwest Ethiopia, 2018

Variables	N (%)
Place of residence
Urban	85 (40.9)
Rural	123 (59.1)
Age of respondents
18–24	48 (23.1)
25–34	87 (41.8)
35–44	49 (23.6)
≥45	24 (11.5)
Mean ± SD	31.70 ±9.123
Sex
Male	95 (45.7)
Female	113 (54.3)
Marital status
Married	148 (71.2)
Single	30 (14.4)
Divorced	16 (7.7)
Separated	9 (4.3)
Widowed	5 (2.4)
Religion
Protestant	92 (44.2)
Orthodox	75 (36.1)
Muslim	41 (19.7)
Ethnicity
Bench	68 (32.7)
Kefa	64 (30.8)
Sheka	24 (11.5)
Amhara	20 (9.6)
Oromo	20 (9.6)
Others*	12 (5.8)
Respondent’s educational status
Unable to write and read	83 (39.9)
Able to read and write	36 (17.3)
Primary	32 (15.4)
Secondary	27 (13.0)
Certificate	15 (7.2)
Diploma and above	15 (7.2)
Respondent’s occupational status
Farmer	54 (26.0)
Housewife	48 (23.1)
Merchant	37 (17.8)
Student	22 (10.6)
Daily worker	23 (11.1)
Government employee	24 (11.5)
Monthly household income in Ethiopian Birr (ETB)
≤750	60 (28.8)
751–1000	59 (28.4)
1001–2000	39 (18.8)
≥2001	50 (24.0)
Mean ±SD	1400.1±1012.27
Household family size
≤3	30 (14.4)
4–5	89 (42.8)
≥6	89 (42.8)
Total	208 (100%)

Note: Others* represents Tigre, Me’anit, Surma.

Seroprevalence of Helicobacter pylori Infection

The overall seroprevalence of H. pylori infection was 89 (42.8%) through antibody detection. Of the positives, 24/89 (26.96%) and 19/89 (21.34%) were occupational housewives and farmers, respectively. A high proportion of H. pylori seropositive cases, 49/89 (55.05%), 59/89 (66.29%), and 82/89 (92.13%) were reported among participants with a household family size of ≥6, who have domestic animals, and who does not treat water before use, respectively (Table 2).

Table 2

Distribution of Seroprevalence of H. pylori Infection (n=208), Southwest Ethiopia, 2018

Variables	Anti-H. pylori Antibody Serostatus
	Negative, N (%)	Positive, N (%)
Occupational status
Farmer	35 (64.8)	19 (35.2)
Housewife	24 (50.0)	24 (50.0)
Merchant	19 (51.4)	18 (48.6)
Student	13 (59.1)	9 (40.9)
Daily worker	10 (43.5)	13 (56.5)
Government employee	18 (75.0)	6 (25.0)
Household family size
≤3	10 (33.3)	20 (66.7)
4–5	69 (77.5)	20 (22.5)
≥6	40 (44.9)	49 (55.1)
Shared bed with siblings
Yes	57 (50.9)	55 (49.1)
No	62 (64.6)	34 (35.4)
Domestic animals
Yes	49 (45.4)	59 (54.6)
No	70 (70.0)	30 (30.0)
Boiling water before drinking
Consistently boiling water before drinking	28 (80.0)	7 (20.0)
Sometimes boiling water before drinking	9 (31.0)	20 (69.0)
Never boiling water before drinking	82 (56.9)	62 (43.1)
Storing and reusing water
Never storing or reusing water	11 (52.4)	10 (47.6)
Sometimes storing and reusing water	49 (71.0)	20 (29.0)
Always storing and reusing water	59 (50.0)	59 (50.0)
Frequency of bathing and showering
At least 2–3 times/week	17 (70.8)	7 (29.2)
Less than 2–3 but more than once/week	40 (66.7)	20 (33.3)
Once/week or less	62 (50.0)	62 (50.0)
Toilet type
Water-closet	17 (77.3)	5 (22.7)
Pit-latrine	43 (65.2)	23 (34.8)
Open-field	59 (49.2)	61 (50.8)
Hand washing with soap after toileting
Yes	49 (75.4)	16 (24.6)
No	70 (49.0)	73 (51.0)
Sources of drinking water
Tap Water	20 (44.4)	25 (55.6)
Bore-hole/well	69 (69.7)	30 (30.3)
River Water	30 (46.9)	34 (53.1)
Water treatment
Yes	21 (75.0)	7 (25.0)
No	98 (54.4)	82 (45.6)
Garbage collecting system in the compound
Yes	33 (71.7)	13 (28.3)
No	86 (53.1)	76 (46.9)

Risk Factors of H. pylori Infection

A number of variables like; occupational status, household family size, shared bed with siblings, presence of domestic animals, boiling water before drinking, storing and reusing water, frequency of bathing and showering, toilet type, hand washing with soap after toileting, sources of drinking water, water treatment and garbage collecting system in the compound were the factors found to be significantly associated with the participants' current serostatus of anti-H. pylori antibody by bivariate analysis. However, after adjusting for possible confounders with multivariate analysis, only variables like; occupational status, household family size, shared a bed with siblings, presence of domestic animals, storing and reusing water, toilet type, and sources of drinking water were found to be significantly associated.

Those participants whose family size was 4 to 5 per household were less likely to be positive for anti-H. pylori antibody than those whose family size was ≥6 members per household (AOR = 0.015, 95% CI = (0.003, 0.089)). Respondents who shared a bed with siblings were 7 times more likely to be positive for anti-H. pylori antibody than their counterparts (AOR = 7.775, 95% CI = (1.676–36.082)) and participants who respond for the presence of domestic animals were 13 times more likely to be positive for anti-H. pylori antibody than their counterparts (AOR = 13.33, 95% CI = (2.203–80.692)). Participants whose sources of drinking water were bore-hole/well were less likely to be positive for the current status of anti-H. pylori antibody than those who used river water (AOR = 0.011, 95% CI = (0.001–0.110)).

Those whose educational status were students were more likely to be positive for the current status of anti-H. pylori antibody than government worker (AOR =23.33, 95% CI= (2.034–67.661)). Those who sometimes store, and reuse water were less likely to be positive for the current status of anti-H. pylori antibody that those who always store and reuse the water (AOR =0.014, 95% CI= (0.002–0.103)).

Participants who use the open field for toilet were 11 times more likely to be positive for the current status of anti-H. pylori antibody than those who use water pit toilet (AOR =11.236, 95% CI= (1.921–65.73)). Respondents who use well water were less likely to be positive for the current status of anti-H. pylori antibody than those who use river water (AOR =0.011, 95% CI= (0.001–0.110)) (Table 3).

Table 3

Determinant Factors for Participant’s Current Status of Anti-H. pylori Antibody (n=208), Southwest Ethiopia, 2018

Variables	Anti-H. pylori Antibody Serostatus		COR (95% CI)	AOR (95% CI)
	Negative, N (%)	Positive, N (%)
Occupational status
Farmer	35 (64.8)	19 (35.2)	1.629 (0.553–4.794)	4.127 (0.376–45.351)
Housewife	24 (50.0)	24 (50.0)	3.000 (1.015–8.864)*	7.868 (0.746–83.008)
Merchant	19 (51.4)	18 (48.6)	2.842 (0.921–8.768)	4.023 (0.368–43.939)
Student	13 (59.1)	9 (40.9)	2.077 (0.592–7.288)	23.334 (2.034–67.661)*
Daily worker	10 (43.5)	13 (56.5)	3.900 (1.131–13.45)*	3.995 (0.348–45.832)
Government employee	18 (75.0)	6 (25.0)	1.00+	1.00+
Household family size
≤3	10 (33.3)	20 (66.7)	1.633 (0.686–3.883)	0.329 (0.019–5.815)
4–5	69 (77.5)	20 (22.5)	0.237 (0.124–0.453)*	0.015 (0.003–0.089)*
≥6	40 (44.9)	49 (55.1)	1.00+	1.00+
Shared bed with siblings
Yes	57 (50.9)	55 (49.1)	1.760 (1.006–3.076)*	7.775 (1.676–36.082)*
No	62 (64.6)	34 (35.4)	1.00+	1.00+
Domestic animals
Yes	49 (45.4)	59 (54.6)	2.810 (1.587–4.975)*	13.334 (2.203–80.692)*
No	70 (70.0)	30 (30.0)	1.00+	1.00+
Boiling water before drinking
Consistently boiling water before drinking	28 (80.0)	7 (20.0)	1.00+	1.00+
Sometimes boiling water before drinking	9 (31.0)	20 (69.0)	8.889 (2.836–27.86)*	9.292 (0.890–97.006)
Never boiling water before drinking	82 (56.9)	62 (43.1)	3.024 (1.240–7.376)*	3.875 (0.736–20.408)
Storing and reusing water
Never storing or reusing water	11 (52.4)	10 (47.6)	0.909 (0.359–2.302)	5.212 (0.828–32.799)
Sometimes storing and reusing water	49 (71.0)	20 (29.0)	0.408 (0.217–0.769)*	0.014 (0.002–0.103)*
Always storing and reusing water	59 (50.0)	59 (50.0)	1.00+	1.00+
Frequency of bathing and showering
At least 2–3 times/week	17 (70.8)	7 (29.2)	0.412 (0.160–1.063)	0.222 (0.024–2.082)
Less than 2–3 but more than once/week	40 (66.7)	20 (33.3)	0.500 (0.263–0.950)*	0.525 (0.086–3.203)
Once/week or less	62 (50.0)	62 (50.0)	1.00+	1.00+
Toilet type
Water-closet	17 (77.3)	5 (22.7)	1.00+	1.00+
Pit-latrine	43 (65.2)	23 (34.8)	1.819 (0.594–5.564)	1.423 (0.289–7.004)
Open-field	59 (49.2)	61 (50.8)	3.515 (1.219–10.14)*	11.236 (1.921–65.73)*
Hand washing with soap after toileting
Yes	49 (75.4)	16 (24.6)	0.313 (0.163–0.601)*	1.459 (0.358–5.950)
No	70 (49.0)	73 (51.0)	1.00+	1.00+
Sources of drinking water
Tap Water	20 (44.4)	25 (55.6)	1.103 (0.513–2.373)	6.151 (0.104–34.283)
Bore-hole/well	69 (69.7)	30 (30.3)	0.384 (0.200–0.736)*	0.011 (0.001–-0.110)*
River Water	30 (46.9)	34 (53.1)	1.00+	1.00+
Water treatment
Yes	21 (75.0)	7 (25.0)	0.398 (0.161–0.984)*	0.394 (0.059–2.620)
No	98 (54.4)	82 (45.6)	1.00+	1.00+
Garbage collecting system in the compound
Yes	33 (71.7)	13 (28.3)	0.446 (0.219–0.909)*	0.378 (0.101–1.416)
No	86 (53.1)	76 (46.9)	1.00+	1.00+

Notes: *Adjusted for all significant variables p <0.05. +Reference Category.

Abbreviation: CI, confidence interval.

Discussion

In the current study, the seroprevalence of H. pylori infection was 42.8% (95% CI (36%; 50%)) through the detection of anti-H. pylori antibody in the serum samples. More than half of the world’s populations in developing countries are infected with H. pylori infection.

In this study, the seroprevalence of H. pylori infection was much higher than a study conducted in North Jakarta 22.5%20 and comparable with a study conducted in Tanzania, 39% (95% CI: 32.3 −45.7).22 Whereas the result is lower compared to the studies done in Kano Nigeria, 81.7%,23 Bahrain, 54%,24 Nigeria, 73.6%,21 South Africa, 66.1%,25 and in Northwest Ethiopia, 85.6%19 and Addis Ababa St. Paul hospital, 64.2%.26 In comparison with the other studies conducted in different areas of the world, it was also found to be lower as compared with the systematic review and meta-analysis conducted in Ethiopia from 1990–2017, where the overall pooled prevalence of H. pylori infection was 52.2%.27 The difference could be attributed due to the socioeconomic difference, study period difference, and laboratory methods used by the individual studies, in which some of the above studies used histological technique, and urea breath test to determine the prevalence of H. pylori infection. Another reason could be due to the difference in sample size as that of this study is relatively lower.

Different predictor variables were found to be significant with serostatus of H. pylori infection.

In the current study, having high family size per household is significantly associated with H. pylori infection. The condition related to crowdedness which favors the transmission of the bacterium between individuals. Similar studies from Iraq,28 North Jakarta,29 Isreal30 and in Nigeria,21,31 documented high crowding index was a significant predictor H. pylori infection. Furthermore, this result is supported by the studies conducted in China32 and Sweden,33 documented that family size is a predictor variable for H. pylori infection in which high family members per household will play a significant role for interfamilial transmission of the bacterium during childhood which results in high seroprevalence of H. pylori in the general population too. In addition, a shared bed with siblings is a predictor variable associated with high prevalence of H. pylori infection in the current study. A similar study reported that the prevalence of H. pylori infection increased with the increment of sibling number (20% in those with none sibling versus 63% with eight or more siblings) in a household.34

The presence of domestic animals was found to be significantly associated with serostatus of H. pylori infection. A similar finding was documented from a study in Butajira, Ethiopia.35 The probability of acquiring the bacterium could be increased due to the presence of domestic animals like cats, dogs, and cattle’s which could contribute to the contamination of food and drinking utensils and could also directly or indirectly contaminate food items and water as well.36

In the current study, sources of drinking water from the river and storing and reusing water frequently were significantly associated with seroprevalence of H. pylori infection compared to those who use tap water. In addition, the toilet type of participants was a factor associated with seroprevalence of H. pylori infection. A similar related finding was reported from a study done in Sana’a,37 and North Jakarta20 which reported poor hand hygiene, hand washing habit, low clean water, and low sanitation index as factors significantly associated with seroprevalence of H. pylori infection. This indicated that poor personal hygiene and environmental sanitation are the source of transmission for infectious diseases causative agents including H. pylori. Whereas, a contradicted finding was reported from a study conducted in Rural Beninase,38 which indicated seroprevalence of H. pylori infection does not have an association with the source of drinking water. This difference with the current study could be attributed to the difference in sources of water used because nearly one-third of the participants of this study were used river water whereas the study subjects in Benine used tap water and well water only. River water is easily contaminated by animal and human waste products, and drinking such water was a high-risk factor for H. pylori infection.39

The result of the current study needs to be interpreted cautiously in which the study has some limitations. The first limitation is, we only studied people aged 18 years or above and did not assess the prevalence in children. Secondly, the inclusion of patients receiving antibiotics for other infections or who have been treated for H. pylori infection in the past may affect the diagnostic accuracy of the test result. Thirdly, it was conducted in a health institution setting and may not be a true representative of the prevalence of H. pylori among dyspeptics in the general population of South-West Ethiopia. A community-based study including all age group therefore needs to be considered by future researchers.

Conclusions

In conclusion, the observed seroprevalence of H. pylori infection among adult dyspeptic patients is relatively high in the study area. Family size shared a bed with siblings, presence of domestic animals, frequent storage and reuse of water, toilet type, and sources of drinking water were significant factors associated with the overall seroprevalence of H. pylori infection. The result can further suggest that the bacterium is still a public health problem that requires further study and effective interventions. Hence, the possible modifiable risk factors should be addressed through effective health education on personal hygiene and sanitation, water handling, toilet usage, handling of domestic animals. Dyspeptic patients should be tested for H. pylori serologically and future broad studies with advanced laboratory procedures should be conducted to identify further associated factors and socioeconomic impact of H. pylori infection.