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Abstract

Objective

The association between Helicobacter pylori and hypertension is unclear. Herein, we aimed to investigate the association between H. pylori and hypertension among adults in Sudan.

Methods

We conducted a community-based case–control study (175 participants in each arm) in the Wad Hamid district in northern Sudan. Cases comprised adults with hypertension and controls were non-hypertensive adults. We assessed participants' data using a questionnaire. We also conducted rapid H. pylori antibody tests and binary and linear regression analyses.

Results

Multivariable logistic regression revealed age (adjusted odds ratio [AOR] 1.05, 95% confidence interval [CI] 1.03–1.07), female sex (AOR 5.50, 95% CI 2.36–12.80), and body mass index (AOR 1.12, 95% CI 1.07–1.17) were significantly associated with hypertension. Moreover, compared with controls, a significantly higher number of patients with hypertension were positive for H. pylori (82/175, 46.9% vs. 46/175, 26.3%). H. pylori seropositivity was associated with systolic blood pressure (coefficient 3.811), diastolic blood pressure (coefficient 3.492), mean blood pressure (coefficient 3.599), and hypertension (AOR 3.15, 95% CI 1.82–5.46).

Conclusion

Our study revealed a significant positive association between H. pylori seropositivity and hypertension. This finding supports literature recommending the eradication of H. pylori to prevent hypertension and its complications.

Keywords

Hypertension systolic blood pressure diastolic blood pressure case–control study seropositive

Introduction

Hypertension is a worldwide health problem among adults (31.1% of those aged ≥20 years) and is one of the main causes of global morbidity and mortality.¹ The burden of hypertension is much higher in resource-limited settings such as Sub-Saharan Africa, where approximately 30% of the population has hypertension.² Several factors such as age, sex, obesity, and alcohol intake are risk factors for hypertension.³ Recently, greater attention has been paid to the role of Helicobacter pylori in the development of several diseases including hypertension, cardiovascular diseases, and metabolic disorders.^4–7 H. pylori is a gram-negative bacterium with a helical or spiral shape, which has been isolated from the human stomach.⁸ Researchers have called for increased awareness and appropriate management on a global scale to combat the association of H. pylori infection with hypertension and metabolic syndrome, as this triad represents a crucial global health problem on a pandemic scale with high morbidity and mortality.⁹

Some studies have found a significant association between H. pylori and hypertension,^5,6,10,11 but others have failed to show any such association.^4,12–15 Moreover, few studies have been conducted in Sub-Saharan Africa.^4,16 Although the pathological relationship between hypertension and H. pylori infection is not fully understood, the evidence shows that H. pylori influences blood pressure through various mechanisms including dietary, inflammatory, dyslipidemia, and metabolic pathways.^9,10,17,18

The practical steps for tackling H. pylori and its complications at a global scale require a thorough understanding of the local context. First, the prevalence of H. pylori in the community, as well as its association with blood pressure level, must be assessed. Then, appropriate health care measures should be applied accordingly. Among adults, there is a high prevalence of H. pylori infection (45.8%) in western Sudan¹⁹ and eastern Sudan (65.8%)²⁰ and a high prevalence of hypertension (40.8%) in eastern Sudan.³ However, the association between H. pylori and hypertension has not been assessed in Sudan. Such an association must be explored to minimize hypertension and its complications (morbidity and mortality) in the country. In the current study, we aimed to investigate the association between H. pylori and hypertension among adults in Almatamah, River Nile state, Northern Sudan.

Methods

Study area

River Nile state is one of 18 states in Sudan. Based on the 2008 census, its total population was 1,120,441.²¹ There are seven localities (lowest administrative units in Sudan) in River Nile state.

Case and control definitions

The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines were strictly followed in this study.²² Participants were considered hypertensive with systolic blood pressure ≥140 mmHg, diastolic blood pressure was ≥90 mmHg, or with both criteria met in repeated measurements, or with use of anti-hypertensive medication for high blood pressure.²³ Any participant with systolic/diastolic blood pressure <140/<90 mmHg and not reporting the use of anti-hypertensive medications was considered a control.

Study population and design

This community-based case–control study was conducted from July to September 2021 in four villages in Wad Hamid district, Almatamah locality, River Nile state, Northern Sudan. Wad Hamid district is adjacent to Khartoum state and approximately 100 km from Khartoum, the capital of Sudan.

Initially, one locality (i.e., Almatamah) was randomly selected from among the seven in River Nile. From the three districts of Almatamah locality, one was randomly selected (i.e., Wad Hamid). Four villages (i.e., Hajer Alteer, Athawra Kabota, Alkoumer, and Wadi Alshohda) were chosen from the randomly selected district using a systematic sampling method. Then, 20 to 40 households from each village were selected based on population density, from which we recruited adults with hypertension and healthy non-hypertensive controls. The first member in each household who agreed to participate and met the study inclusion criteria was selected. If the selected house was uninhabited or the inhabitants refused to participate, the next house was selected until the target number of study participants was reached. The investigators trained two medical officers in data collection methods to standardize the data collection procedure so as to maintain data quality.

After signing an informed consent form, all adult (aged ≥18 years) Sudanese residents (including both men and women) with no symptoms were enrolled from households chosen using the lottery method. Participants aged less than 18 years, pregnant women, patients with poor cognitive function, and severely ill patients were excluded from this study.

Data collection

For the current data collection, we used the World Health Organization (WHO) three-level STEPwise approach questionnaire.²⁴ The questionnaire was used to gather data on sociodemographic characteristics including age in years, sex, employment status (employed/unemployed), marital status (married/unmarried), education level (<secondary and ≥secondary), cigarette smoking (never and former/current), alcohol consumption (never and former/current), and family history of hypertension.

Procedures

Blood pressure was measured for each participant using a standard mercury sphygmomanometer (model no. 19160027; Jiangsu Yuwell Medical Equipment & Supply Co., Ltd, China) after at least a 10-minute rest and while in a sitting position, with the arm maintained at heart level. Using an appropriately sized cuff, the mean of two blood pressure readings (taken at an interval of 1–2 minutes) was calculated. If the difference between the two readings was >5 mmHg, measurements were retaken until the reading stabilized.

Each participant's weight was measured in kg using standard procedures and well-calibrated scales adjusted to zero before each measurement. Each participant was asked to stand with minimal movement and hands by their sides. Shoes and excess clothing were removed. Then, height was measured in cm with each participant standing upright with their back against the wall and feet together. Body mass index (BMI) was computed as weight in kg divided by the square of height in meters (kg/m²). BMI was categorized according to the WHO classification as underweight (<18.5 kg/m²), normal weight (18.5–24.9 kg/m²), overweight (25.0–29.9 (kg/m²), and obese (≥30.0 kg/m²).²⁵

A 3- to 5-mL blood sample was collected from each participant for H. pylori serological testing. Blood samples were centrifuged at 1500 rpm for 15 minutes, and an H. pylori antibody test was performed according to the manufacturer's instructions (Hangzhou AllTest Biotech Co., Ltd.; Hangzhou, China). The H. pylori antibody rapid test is a rapid visual immunoassay for the qualitative detection of specific immunoglobulin M (IgM) and IgG antibodies against H. pylori. The test is widely used and has high sensitivity and specificity.²⁶ In this work, we defined the test results as positive or negative for H. pylori infection.

Sample size calculation

The sample size was calculated, assuming an H. pylori prevalence of 45% and 30% among hypertensive and non-hypertensive participants, respectively. This assumption was based on reports of H. pylori in Cameroon (45.0% among hypertensive vs. 30.0% among non-hypertensive participants).¹⁶ The sample size in each arm was calculated to detect a difference of 5% at α = 0.05 with a power of 80%. It was assumed that 10% of individuals might not respond or would have incomplete data.

Ethical considerations

The current work was conducted according to the principles laid down in the Declaration of Helsinki. Almatamah Health Authority, Sudan approved the study (#9, 2021). All participants provided their written informed consent to participate in the study. The authors followed all measures to ensure the privacy and confidentiality of participants, such as excluding personal identifiers during data collection.

Statistical analysis

Data were analyzed using IBM SPSS for Windows, version 22.0 (IBM Corp., Armonk, NY, USA). The proportions are expressed as frequency (%). Continuous data were evaluated for normality using the Shapiro–Wilk test and were non-normally distributed. Non-normally distributed data are expressed as median (interquartile range). Adjusted regression analysis (binary and linear) was performed with hypertension (for binary regression) and systolic, diastolic, and mean blood pressure (for linear regression) as dependent variables; sociodemographic data (age, sex, BMI, educational level, occupation, marital status, smoking, alcohol consumption, and family history of hypertension) as clinical parameters; and H. pylori as the independent variable. Adjusted odds ratios (AORs), 95% confidence intervals (CIs), coefficients, and standard error were calculated, as appropriate. A two-sided P-value of <0.05 was considered statistically significant.

Results

A total of 175 participants were included in each arm of the study (hypertensive and non-hypertensive participants) at a ratio of 1:1. Among the total, 41.7%, 70.8%, 26.5%, and 41.1% were male, more highly educated, married, and employed, respectively (data not shown). Compared with controls, patients with hypertension were older, had a higher BMI, included more women, had lower education levels, were unemployed, unmarried, and had a family history of hypertension, as shown in Table 1. The results of multivariable logistic regression revealed that age (AOR 1.05, 95% CI 1.03–1.07), female sex (AOR 5.50, 95% CI 2.36–12.80), and BMI (AOR 1.12, 95% CI 1.07–1.17) were associated with hypertension. Occupational status, marital status, family history of hypertension, smoking, and alcohol consumption did not differ significantly between the two groups (Table 1). Moreover, age and BMI were significantly associated with systolic, diastolic, and mean blood pressure (Table 2).

Table 1.

Univariate and multivariate analysis of factors associated with hypertension.

Variable	Participants with hypertension (N-175)	Participants without hypertension (N-175)	Univariate analysis		Multivariate analysis
	Median (interquartile range)		OR (95% CI)	P	OR (95% CI)	P
Age, years	50.0 (39.0‒60.0)	38.0 (28.0‒50.0)	1.04 (1.03‒1.06)	<0.001	1.05 (1.03‒1.07)	<0.001
Body mass index, kg/m²	28.4 (24.8‒31.6)	24.2 (19.4‒28.2)	1.12 (1.08‒1.17)	<0.001	1.12 (1.07‒1.17)	<0.001
Sex
Male	47 (26.9)	99 (56.6)	Reference			<0.001
Female	128 (73.1)	76 (43.4)	3.55 (2.27‒5.56)	<0.001	5.50 (2.36‒12.80)	<0.001
Education level
≥Secondary	128 (73.1)	120 (68.6)	Reference		‒	–
<Secondary	47 (26.9)	55 (31.4)	0.80 (0.51‒1.27	0.347	‒	–
Occupational status
Employed	58 (33.1)	86 (49.1)	Reference			0.358
Unemployed	117 (66.9)	89 (50.9)	1.95 (1.27‒3.00)	0.002	0.71 (0.34‒1.48)	0.358
Marital status
Married	39 (22.3)	54 (30.9)	Reference			0.642
Unmarried	136 (77.7)	121 (69.1)	1.56 (0.96‒2.51)	0.07	0.86 (0.45‒1.64)	0.642
Family history of hypertension
No	75 (42.9)	109 (62.3)	Reference			0.104
Yes	100 (57.1)	66 (37.7)	2.20 (1.44‒3.38)	<0.001	1.54 (0.92‒2.60)	0.104
Cigarette smoking
Never	154 (88.0)	132 (75.4)	Reference			0.406
Current/former	21 (12.0)	43 (24.6)	2.39 (1.35‒4.23)	0.003	1.49 (0.58‒3.79)	0.406
Alcohol consumption
Never	169 (96.6)	155 (88.5)	Reference			0.106
Current/former	6 (3.4)	20 (11.5)	3.64 (1.42‒9.29)	0.007	0.33 (0.09‒1.26)	0.106
H. pylori seropositivity
No	93 (53.1)	129 (73.7)	Reference			<0.001
Yes	82 (46.9)	46 (26.3)	2.47 (1.58‒3.87)	<0.001	3.15 (1.82‒5.46)	<0.001

Values in the table are median (interquartile range) or frequency (percentage).

H. pylori, Helicobacter pylori; OR, odds ratio; CI, confidence interval.

Table 2.

Linear regression analysis of factors associated with systolic, diastolic, and mean blood pressure.

Variable	Systolic blood pressure		Diastolic blood pressure		Mean blood pressure
Variable	Coefficient (standard error)	P	Coefficient (standard error)	P	Coefficient (standard error)	P
Age, years	0.31 (0.06)	<0.001	0.16 (0.05)	0.001	0.21 (0.04)	<0.001
Body mass index, kg/m²	0.17 (0.15)	0.251	0.50 (0.11)	<0.001	0.39 (0.10)	<0.001
Sex
Male	Reference
Female	3.39 (2.81)	0.229	2.64 (2.11)	0.210	2.89 (1.88)	0.125
Education level
≥Secondary	Reference
<Secondary	−5.26 (2.03)	0.010	1.21 (1.52)	0.428	−0.95 (1.36)	0.486
Occupational status
Employed	Reference
Unemployed	0.23 (2.54)	0.929	−1.85 (1.90)	0.331	−1.16 (1.70)	0.496
Marital status
Married	Reference
Unmarried	2.02 (2.20)	0.358	1.60 (1.64)	0.331	1.74 (1.47)	0.237
Family history of hypertension
No	Reference
Yes	3.59 (1.90)	0.060	1.52 (1.42)	0.286	2.21 (1.27)	0.083
Cigarette smoking
Never	Reference
Current/former	−1.47 (3.02)	0.628	2.46 (2.26)	0.278	1.15 (2.02)	0.569
Alcohol consumption
Never	Reference
Current/former	4.43 (3.96)	0.264	−6.04 (2.96)	0.042	−2.55 (2.65)	0.336
H. pylori seropositivity
No	Reference
Yes	3.81 (1.88)	0.044	3.49 (1.41)	0.014	3.60 (1.26)	0.005

H. pylori, Helicobacter pylori.

Compared with the controls, a significantly higher number of patients with hypertension were H. pylori positive (82/175, 46.9% vs. 46/175, 26.3%, P < 0.001]. H. pylori was associated with systolic blood pressure (coefficient 3.811, P = 0.044), diastolic blood pressure (coefficient 3.492, P = 0.014), mean blood pressure (coefficient 3.599, P = 0.004), and hypertension (AOR 3.15, 95% CI =1.82–5.46) (Tables 1 and 2).

Discussion

The main finding of the current study was that H. pylori seropositivity was associated with systolic blood pressure, diastolic blood pressure, mean blood pressure, and hypertension. We previously showed that pregnant Sudanese women with H. pylori seropositivity had a 4.9 times higher risk of having preeclampsia.²⁷ As mentioned above, several previous studies have reported a significant association between H. pylori and systolic, diastolic, and mean blood pressures and hypertension.^5,6,10,11 In Cameroon, Tamokou et al. reported that adults with H. pylori infection had a 2.04 times higher risk of having hypertension.¹⁶ In a recent large cross-sectional study enrolling 17,100 Chinese adults, H. pylori infection was associated with diastolic blood pressure and hypertension.¹¹ Interestingly, in a recent study, only diastolic blood pressure (no association with systolic blood pressure) was associated with H. pylori infection.¹⁰ In a recent meta-analysis (2021) that included six studies enrolling 11,317 patients with hypertension and 12,765 controls, H. pylori infection was associated with hypertension (OR 1.34, 95% CI 1.10–1.63).⁵ In their meta-analysis in 2022 that included 55 studies with 198,750 participants, Yue et al. reported that H. pylori infection was associated with hypertension (OR 1.32, 95% CI 1.15–1.52). Moreover, those authors reported that participants with H. pylori infection had elevated levels of systolic as well as diastolic blood pressure.⁶

Among 363 symptomatic patients with dyspepsia in a health facility in Cameroon, H. pylori infection was not associated with systolic blood pressure, diastolic blood pressure, mean blood pressure, or hypertension.⁴ Likewise, a general health survey among adults in Amsterdam (Netherlands) reported that seropositivity for H. pylori was not associated with hypertension.¹² Interestingly, in a large cross-sectional study of healthy participants (37,263), H. pylori infection was not associated with systolic blood pressure.¹⁰ In the Czech population (1818 individuals aged 5–98 years), H. pylori infection was not found to be associated with blood pressure.¹⁵

We urge caution in comparing our results with the findings of the above studies. First, our study was conducted among asymptomatic participants in the community and some results of past studies were from symptomatic participants or facility-based studies. Second, differences in the sociodemographic characteristics of different settings have to be considered, e.g., alcohol consumption. Third, different methods, such as enzyme-linked immunosorbent assay, rapid urease breath test, stool antigen test, and histology were used in different studies.

The exact mechanism by which H. pylori might influence blood pressure is not well known; however, different theories might explain the association between H. pylori and hypertension. Several components of H. pylori infection-related metabolic syndrome present important risk factors for the development of arterial hypertension.^9,10 H. pylori infection is reported to be associated with dyslipidemia in the form of higher total cholesterol level, higher low-density lipoprotein, and lower low-density lipoprotein level.¹⁰ A recent systematic review and meta-analysis showed a significant association between obesity and H. pylori infection.²⁸ Moreover, H. pylori influences blood pressure via various mechanisms including dietary, inflammatory and metabolic pathways.^9,17,18

The current study was conducted mainly to assess the association between H. pylori and hypertension. Several factors might act as confounders such as age, sex, BMI, and marital status. As shown in regression analysis, many of these factors are associated with hypertension; we have previously discussed these in our previous work in eastern Sudan.³ Discussion of these factors might extend beyond the scope of this manuscript.

Limitations

The design of the present study was an unmatched case–control study, in which there was a difference in age and sex between cases and controls; hence, the element of bias could not be eliminated. A longitudinal study would provide greater clarification regarding the association between H. pylori and hypertension. H. pylori infection status was determined via serology only; the presence of anti-H. pylori antibodies does not necessarily indicate an active infection. All participants were adults, thus limiting generalization of the findings to populations of all ages. Lipid profile and inflammatory biomarkers were not assessed. Moreover, there was no information regarding the virulence or genetic characteristics of the infecting m H. pylori strains.

Conclusion

Footnotes

Acknowledgements

The authors would like to thank all individuals who participated in this study.

Authors’ contributions

AAH and IA conceived the study. BEA and OEO supervised the work, guided the analysis, and critically reviewed the manuscript. AAH, BEA, and IA prepared the analysis plan, performed the data analysis, and wrote the first draft of the paper. BE and OEO supervised data collection. All authors reviewed and approved the final manuscript.

Availability of data and material

The datasets generated and/or analyzed during the current study are not publicly available because the manuscript is still under the peer review process but are available from the corresponding author on reasonable request.

Declaration of conflicting interests

The authors declare that there is no conflict of interest.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

ORCID iD

Ahmed A Hassan

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Association between Helicobacter pylori seropositivity and hypertension among adults in Northern Sudan: a community-based case–control study

Abstract

Objective

Methods

Results

Conclusion

Keywords

Introduction

Methods

Study area

Case and control definitions

Study population and design

Data collection

Procedures

Sample size calculation

Ethical considerations

Statistical analysis

Results

Discussion

Limitations

Conclusion

Footnotes

Acknowledgements

Authors’ contributions

Availability of data and material

Declaration of conflicting interests

Funding

ORCID iD

References