Epidemiology of Helicobacter pylori infection in dyspeptic Ghanaian patients

Epidemiology of Helicobacter pylori infection in dyspeptic Ghanaian patients

 

Timothy Nii Akushe Archampong^1,&, Richard Harry Asmah², Edwin Kwame Wiredu³, Richard Kwasi Gyasi³, Kofi Nyaako Nkrumah¹, Kumar Rajakumar^4,5

 

¹Department of Medicine, University of Ghana Medical School, College of Health Sciences, University of Ghana, Legon Boundary, Accra, Ghana, ²Department of Medical Laboratory Sciences, School of Allied Health Sciences, College of Health Sciences, University of Ghana, Legon Boundary, Accra, Ghana, ³Department of Pathology, University of Ghana Medical School, College of Health Sciences, University of Ghana, Legon Boundary, Accra, Ghana, ⁴Department of Infection, Immunity and Inflammation, University of Leicester Medical School, Leicester LE1 9HN, United Kingdom, ⁵Department of Clinical Microbiology, University Hospitals of Leicester NHS Trust, Leicester LE1 5WW, United Kingdom

 

 

^&Corresponding author
Timothy Nii Akushe Archampong, Department of Medicine, University of Ghana Medical School, College of Health Sciences, University of Ghana, Legon Boundary, Accra, Ghana

 

 

 

 

Helicobacter pylori is a spiral-shaped gram-negative urease-producing bacterium [1]. It is the most common chronic bacterial infection known to humans [2, 3]. It is found in the gastric antrum and in areas of gastric metaplasia in the duodenum [4]. It has also been established as the main aetiological agent in the development of chronic gastritis, gastric and duodenal ulceration, gastric B-cell lymphoma and distal gastric cancer [4]. H. Pylori has been demonstrated worldwide and in individuals of all ages with conservative estimates suggesting 50 % of the world´s population is affected [3]. Infection is more frequent and acquired at an earlier age in developing countries compared to European populations where evidence of H. Pylori is rarely found before age 10 but increases to 10 % in those between 18 and 30 years of age and to 50 % in those older than age 60 [3]. In many developing countries, the infection has a high prevalence rate (80 -- 95%) [5]. More than 50% of children are infected by the age of 10 years with the prevalence of infection rising to over 80% in young adults [6]. The incidence of H. pylori infection in Ghanaian patients with dyspeptic symptoms referred for upper gastrointestinal endoscopy at the Korle-Bu Teaching Hospital (KBTH) has previously been found to be 75.4% [7]. The exact mode of transmission is unclear but intra-familial clustering suggests person-to-person spread mainly in childhood [4]. The risk of infection with H. Pylori is related to socioeconomic status and living conditions in early life. Overcrowded conditions associated with childhood poverty lead to increased transmission and higher prevalence rates [8]. Potential dietary associations with H. pylori have been investigated in humans and chronic excessive salt intake has been shown to enhance H. pylori colonization in mice and in humans [9].This study investigated the epidemiological characteristics of H. pylori infection in a West African country with a known high prevalence of the condition.

 

 

Ethical approval was granted by the Protocol and Ethical Review Committee of the University of Ghana Medical School, College of Health Sciences, Accra, Ghana. This study was conducted in accordance with the Helsinki Declaration.It used a cross-sectional design to consecutively sample dyspeptic patients at the Endoscopy Unit of the KBTH, Accra between April, 2010 and August, 2012. Korle-Bu Teaching Hospital has 2,500 beds and is the main tertiary referral center in the capital, Accra serving the majority of the southern half of Ghana. The Endoscopy Unit runs two four-hour sessions per day on four days of the week. Approximately five patients attend each endoscopy session for upper gastro-intestinal (GI) endoscopy. Sampling was conducted during three such sessions per week. All patients were taken through the explanatory statement of the project before endoscopy. Patients with priorH. pylori eradication treatment or proton-pump inhibitor-use two weeks preceding endoscopic analysis were excluded from the study. Consenting patients were subsequently recruited into the study and administered the study questionnaire which elicited patients’ demographics, household, environmental characteristics, associated symptoms and relevant background history.This included occupation, alcohol intake, dietary preferences and herbal remedies. Household structure was defined as follows: detached (a single house in an enclosed compound); semi-detached (two houses built side by side and sharing a common wall); compound structure (more than two separate houses enclosed in the same compound). Urban residences were categorized into class 1 –- 3 based on the Accra Metropolitan Assembly (AMA) classification of Accra with tax imposition rates of Ghana Cedi (GHC) 100, GHC 60 and GHC 40 respectively. These reflect relative wealth and housing density in the Metropolis with class 1 corresponding to the most affluent and class 3 the most densely populated regions. Rural regions were geographical areas in Ghana not within an urban area and outside cities and towns.

 

H. pylori infection was confirmed by rapid-urease Campylobacter-like-organism (CLO) examination of antral biopsies at upper GI endoscopy (CLO testing kit: Cambridge Life Sciences Ltd, Cambridge, UK). Data was analyzedusing the SPSS 16 Program. Categorical data was expressed as proportions and presented in tables. Chi-square was used to demonstrate the differences between observed variables with a p-value of <0.05 used to indicate statistical significance. Logistic regression analysis was used to demonstrate the relative risk of H. pylori infection in patients with specific predictor variables.

 

 

The sample population of dyspeptic patients attending the Endoscopy Unit for upper GI endoscopy yielded 242 patients of which 47.5% were females, 52.5 % males. The overall prevalence of H. pylori obtained by immediate CLO-testing of gastric antral biopsies was74.8%. The age distribution of H. pylori-CLO-positive cases was even across most age - groups as illustrated by Figure 1. Agegroup 21-– 30 years had the highest H. pylori prevalence, 80.0% (n=24) while agegroup (61-–70) had the lowest, 69.2% (n=27). There was no statistically significant difference in H. pylori prevalence between agegroups, (p = 0.957). Table 1 illustrates the relationship between housing characteristics and H. pylori prevalence including number in household, type of household and residential location. There was a statistically significant difference between residential classes in relation to H. pylori prevalence (p=0.046) with rural areas having the highest prevalence (88.6%, n=39). However, H pylori prevalence decreased across areas mapping to the three residential classes in accordance with increasing affluence (Table 1). Consistent with this theme, all nine patients with a household size over 30 individuals had H. pylori infection in comparison to 67.9%, (n=55) of patients living in households with 1 -– 5 members. By contrast, there was nostatistical difference in H. pylori prevalence between household structural types; detached, semi-detached or compound house-structure, (p = 0.469).

 

Table 2 shows the distribution of H. pylori cases by occupation, p = 0.107; the unemployed and patients involved in farming/agriculture had relatively high H. pylori infection rates of 92.3% and 91.7% respectively. Potential associations were also sought between consumption of alcohol, herbal remedies,dietary preference (spice, fat, smoked fish, salt) and H. pylori infection prevalence. However, none achieved statistical significance, Table 3. Table 4 demonstrates the relative risk of H. pylori infection with specific predictor variables after logistic regression analysis. Residential class was the most significant risk factor for the presence of H. pylori infection following multi-variate analysis (OR 1.86; 95 % CI 1.27-2.73). Household size (OR 1.78; 95 % CI 0.71-4.34) and structure (OR 2.37; 95 % CI 0.92-6.09) were however potential risk factors for H. pylori infection.

 

 

The prevalence of H. pylori infection in this study was 74.8% comparable to previous studies in Ghana [7], Nigeria [10] and other developing countries [8]. The uniformly high age-related H. pylori prevalence demonstrated supports the notion that the rate of acquisition of infection is predominantly highest in early life [11]. Indeed, it is widely believed that once acquired colonization persists throughout life unless otherwise eradicated [11]. Re-infection with H. pylori following successful bacterial cure is not uncommon in developing countries,occurring in approximately ~ 12% of individuals shown to have been originally cleared of this bacterium. By contrast, in developed countries~1% such individuals are subsequently re-infected. Additionally, when re-infection occurs this has most commonly been shown to represent recrudescence of the original bacterial strain [12]. Studies based in Peru and Mexico showed re-infection rates of 3-– 7% [13, 14], while in comparison a European-based study elicited a rate of only 0.4% [15]. Re-infection from multiple sources of infection in developing countries, particularly in endemic areas has also been suggestedas important in maintaining the presence of this organism during adulthood [8, 13, 14].

 

Rising numbers of household membership and household structure were not significantly associated with H. pylori infection. However, all nine patients with a household size of over 30 members had H. pylori infection in comparison to 67.9% of patients living in households with only 1 -– 5 individuals.A studyhas shown that in UK adults, aged 50-- 59 years, sibling number was independently associated with prevalence of H. pylori infection [16]. Similarly, in a Cambodian study the number of children in the household was more significant than number of adults in predicting the presence of H. pylori infection [17, 18]. Specific characteristics of children may enhance the spread of H. pylori among contacts and household members. For example, a child may have an enhanced susceptibility to H. pylori through increased exposure and a possible lowered immune response [17].

 

In this study, occupation was used as a surrogate marker of socio-economic status of patients. Those who were classified as unemployed or students had a relatively high infection prevalence of 96.2%. Given the frequent correlation between employment status and wealth, these data would appear to be consistent with the finding that children from low-income families havesignificantly higher infection rates than those from high-income families [19]. The H. pylori prevalence in Black and Hispanic people was also inversely related to the social class during childhood. In support of the notion that childhood environment was critical, this relationship remained even after adjusting for the present social class and age of study participants [20]. More affluent and less densely populated urban areas (residential classes) also demonstrated lower infection rates (Table 1). Smaller family size, less crowding, improved sanitation and clean water help explain the decline in H. pylori prevalence in developed countries [17] as well as some developing countries [21]. This may be as a result of the reported presence of H. pylori in vomitus, human faeces and unclean water, all potentially serving as sources of infection of vulnerable residents in over-crowded and densely populated accommodations [16].

 

Farming and agriculture was associated with an infection prevalence of 91.7% suggesting possible zoonotic transmission. In Ghana, poultry, cows, sheep and goats are some of the common animals frequently reared in farming communities. Many animals such as cats, monkeys have been successfully infected with H. pylori strains and an increased risk of infection with exposure to sheep has also been reported in a number of studies [18, 22]. Since other Helicobacter species also strongly produce urease, the CLO test would not be able to differentiate H. Pylori from other species such as H. Heilmannii [23]. The large spiral gastric Helicobacter-like organisms (GHLOs), commonly noted in dogs and cats, often infect patients who own pets suggesting a zoonotic link. However, they are associated with approximately 0.08-1% of gastritis in humans [24]. Laboratory studies have experienced difficulty in isolating H. Pylori from material other than gastric tissue which has made identification of portals of entry and exit problematic [25]. Reports using whole-cell enzyme-linked immune-absorbent assay (ELISA) sonicate to monitor infection serologically, have cited a high incidence of H. pylori in abattoir workers [24]. Theseresults have been thought to be confounded by potential antigenic cross-reactivity in workers´ sera due to the constant exposure to other gastrointestinal flora of animals [24]. Thus, the isolation of H. pylori from the inflamed gastric lining of commercially reared animals [26], and the ability to experimentally infect cats with H. pylori [24], continues to raise the possibility of zoonotic H. pylori transmission from infected animals who have close human contact.

 

 

H. pylori is endemic in Ghana but the persistently high prevalence across age groups despite significant community anti-microbial use and abuse [27], suggests likely re-crudescence or re-infection from multiple sources in a developing country. Socio-cultural factors such as residential class and farming may be facilitating factors for its continued prevalence. Further study will evaluate the impact of these epidemiological factors, broader host traits and microbial determinants in the transmission and persistence of H. pylori in Ghana.

 

 

The authors declare no competing interests.

 

 

Timothy Archampong, the principal investigator of the project, was involved in concept design, patient recruitment,data analysis and drafted the manuscript. Harry Asmah, Prof. E.K. Wiredu and Prof. R.K. Gyasi assisted the principal investigator in procurement of consumables, analysis and interpretation of the data, critically revised the article and provided final approval of the article. Dr. K.N. Nkrumah and Dr. K. Rajakumar guided the principal investigator in concept design, critically revised the article and provided final approval of the article.

 

 

This study was fundedby the Danish Universities-Platform for Human Health (PHH) Pilot Grant and the University of Ghana Office of Research,Innovation and Development (ORID) Grant during patient recruitment, procurement of consumables, sample collection, data analysis and manuscript development. I would like to acknowledge Rev. Tom Ndanu, University of Ghana Dental School, for his assistance during analysis of project data. I am grateful to Rita Adu, Research Assistant, Department of Medicine, University of Ghana Medical School, and staff of the Endoscopy Unit, Korle-Bu Teaching Hospital for assistance during patient recruitment and rapid-urease H. pylori-CLO-testing.

 

 

Table 1: housing characteristics and Helicobacter pylori prevalence

Table 2: distribution of Helicobacter pylori cases by occupation

Table 3: dietary preference, alcohol consumption and Helicobacter pylori infection

Table 4: predictor variables and H. pylori risk – multi-variate analysis

Figure 1: age distribution of Helicobacter pylori cases

 

 

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