Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Open Access

Peer-reviewed

Research Article

Comparison of hematologic parameters, serum electrolytes, and lipid profiles among dyspeptic patients with and without Helicobacter pylori infection attending Jimma Medical Center, Jimma, South West Ethiopia

  • Negussie Sarbecha ,

    Roles Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

    nafyadsarbecha@gmail.com

    Affiliation Department of Biomedical Sciences, School of Medicine, Madda Walabu University, Robe, Ethiopia

    ⨯
  • Minale Fikade,

    Roles Conceptualization, Data curation, Methodology, Supervision, Visualization, Writing – review & editing

    Affiliation Department of Biochemistry, School of Biomedical Sciences, Jimma University, Jimma, Ethiopia

    ⨯
  • Tesaka Wondimnew,

    Roles Conceptualization, Data curation, Methodology, Writing – review & editing

    Affiliation Department of Biochemistry, School of Biomedical Sciences, Jimma University, Jimma, Ethiopia

    ⨯
  • Kumsa Kene,

    Roles Conceptualization, Data curation, Methodology, Writing – review & editing

    Affiliation Department of Biochemistry, School of Biomedical Sciences, Jimma University, Jimma, Ethiopia

    ⨯
  • Negawo Kebede,

    Roles Conceptualization, Data curation, Formal analysis, Writing – review & editing

    Affiliation Department of Biomedical Sciences, School of Medicine, Madda Walabu University, Robe, Ethiopia

    ⨯
  • Habtemariam Gebresillasie,

    Roles Conceptualization, Data curation, Software, Writing – review & editing

    Affiliation Department of Biomedical Sciences, School of Medicine, Madda Walabu University, Robe, Ethiopia

    ⨯
  • Zerihun Assefa

    Roles Conceptualization, Methodology, Writing – review & editing

    Affiliation Department of Biochemistry, School of Biomedical Sciences, Jimma University, Jimma, Ethiopia

    ⨯

Abstract

Background

About half of the world’s populations are infected with Helicobacter pylori, which may create atherogenic lipid profiles and contribute to atherosclerosis and related cardiovascular disease. Furthermore, it has been connected to hematological symptoms like anemia. Even though the high prevalence of H.pylori and its associated complications, including cardiovascular disease and anemia, in Ethiopia, there is little data regarding the risk factors associated with H.pylori infection, such as hematologic parameters, electrolyte imbalances, and lipid profiles.

Methods

A comparative cross-sectional study design with a consecutive sampling technique was employed at Jimma Medical Center among 108 dyspeptic patients. Five (5) ml of blood samples were collected from each participant, and serum was extracted and analyzed using a COBAS 6000 core for the lipid and electrolyte, and whole blood was used with a SYSMEX XN 550 to determine hematological parameters. Data were entered in to Epi-data version 4.6 and exported to SPSS version 25 for analysis. Simple descriptive statistics and chi-square test were used to present the socio-demographic characteristics of the study subjects. Student t-test was used for data comparison and p-value < 0.05 was considered statistically significant.

Results

H.pylori infected patients had significantly decreased levels of red blood cell count (p = 0.002), hemoglobin (p = 0.012), mean corpuscular hemoglobin concentration (p < 0.001), platelet count (p = 0.001), and sodium level (p = 0.006) when compared to the uninfected group. However, total cholesterol (p = 0.001), and low density lipoprotein (p = 0.021) were increased in H.pylori infected patients when compared to the uninfected group.

Conclusions

This study revealed that H.pylori infection can cause derangements of hematologic parameters, electrolyte imbalances, and alterations of lipid parameters which considered as risk factors for anemia and cardiovascular diseases.

Citation: Sarbecha N, Fikade M, Wondimnew T, Kene K, Kebede N, Gebresillasie H, et al. (2024) Comparison of hematologic parameters, serum electrolytes, and lipid profiles among dyspeptic patients with and without Helicobacter pylori infection attending Jimma Medical Center, Jimma, South West Ethiopia. PLoS ONE 19(11): e0310047. https://doi.org/10.1371/journal.pone.0310047

Editor: Mihret Tilahun, Wollo University, ETHIOPIA

Received: April 29, 2024; Accepted: August 15, 2024; Published: November 4, 2024

Copyright: © 2024 Sarbecha et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

List of abbreviations: CagA, Cytotoxin associated gene A; Hct, Hematocrit; Hgb, Haemoglobin; H.pylori, Helicobacter pylori; HDL-C, High Density Lipoprotein- Cholesterol; LDL-C, Low Density Lipoprotein-Cholesterol; MCHC, Mean Corpuscular Haemoglobin Concentration); RBC, Red Blood Cell); TG, Triglyceride; TC, Total Cholesterol; VacA, Vacuolating cytotoxin gene A; WBC, White Blood Cell

Introduction

Dyspepsia is typically used to describe upper abdominal discomfort that is believed to be caused by the upper gastrointestinal tract and may include symptoms such as abdominal bloating, belching, epigastric pain, heartburn, acid regurgitation, early satiety, nausea, and a sense of slow or abnormal digestion [1, 2]. The main causes of dyspepsia are functional dyspepsia (70%), peptic ulcer disease (PUD) (10%), gastroesophageal reflux disease (GERD) (5%), and gastric cancer (1%) [3]. Functional dyspepsia is caused by H.pylori infection, delayed gastric emptying, impaired stomach accommodation, diet, lifestyle factors like chewing khat, drinking alcohol, and smoking, as well as psychosocial factors like depression, stress, and anxiety [4].

H.pylori is a spiral-shaped gram-negative commensal bacterium that inhabits the human stomach [5]. For almost 40 years, H.pylori has been recognized as a serious and widespread human bacterial pathogen [6]. Factors like socioeconomic status, poverty, crowded living conditions, sanitation, ethnicity, and unsafe water and food can contribute to the incidence of H.pylori infection [7]. Infection rates vary by region, but over the past three decades, the number of infected people has maintained or even increased due to population expansion, reinfection, and recrudescence due to unsuccessful eradication [8].

It was estimated that 4.4 billion people worldwide tested positive for H.pylori in 2015, with Asia (54.7%), the Caribbean and Latin America (63.4%), and Africa (79.1%) having the greatest prevalence rates [9]. In Ethiopia, the overall polled prevalence of H.pylori infection was 52.2% [10].

H.pylori has been associated with numerous diseases both inside and outside of the stomach area because of the very virulent substances it produces [11]. Around 80% of duodenal ulcers and 50% of gastric ulcers are connected with this infection [12]. H.pylori is one of the infections designated by the World Health Organization (WHO) as a carcinogen and the main risk factor for non-cardia gastric adenocarcinoma [13, 14].

The settlement of the stomach by H.pylori initiates the surrounding area’s inflammation by attracting lymphocytes and neutrophils [15, 16]. Infection and inflammation induces the activation of different cytokine like IL-1, IL-6, and TNF, which trigger the alteration of lipid metabolism [17]. The activation of cytokines can change lipid metabolism through the initiation of hepatic fatty acid synthesis, stimulation of adipose tissue lipoprotein lipase, and increased lipolysis [18]. People with H.pylori infection have atherogenic lipid profiles, which could induce atherosclerosis and related cardiovascular diseases like peripheral vascular diseases, stroke, and myocardial infarction [19, 20]. Cardiovascular diseases are the leading cause of disability and are accountable for around thirty-five million deaths per year, of which 85% are in low socioeconomic countries [21].

Furthermore, H.pylori has been linked to hematological symptoms like anemia [22]. Approximately 1.62 billion individuals are affected by anemia worldwide, and from those, almost half of all the incidence of anemia is caused by iron deficiency [23]. The incidence of iron deficiency anemia increased by 2.6-fold in H.pylori infection patients [24]. The association between H.pylori and iron deficiency may be due to bleeding and occult bleeding loss secondary to PUD, gastric malignancy, and chronic erosive gastritis that occur due to surface virulent factors of H.pylori like Cag A or due to iron uptake and utilization by H.pylori and may be due to decreased absorption of iron and intrinsic factor deficiency secondary to chronic gastritis and hypochlorhydria [25]. A lack of intrinsic factors results in less vitamin B12 being absorbed, which could change hematologic parameters [26].

H.pylori is also accountable for a decrease in platelet count because of the molecular mimicry with H.pylori CagA, which causes the generation of autoantibodies against H.pylori CagA and the cross-reactivity of these antibodies with platelet surface antigens [27]. H.pylori attachment to gastric epithelial cells enhanced Na-K-ATPase ubiquitylation and decreased its surface and total levels [28]. Alteration of Na + K + ATPase might affect the level of serum sodium levels by inhabiting the efflux of sodium out of the cell. H.pylori infection has also had a significant association with chronic kidney disease, which may have been related to electrolyte derangement [29, 30]. Any changes in serum electrolyte levels increase the risk of cardiovascular morbidity and its associated death [31].

Regarding the association between the presence of H.pylori infection and hematologic parameters, electrolyte imbalance, and lipid profiles, the findings of several researchers have been inconsistent and occasionally contradictory [23, 32–34]. Although H.pylori infection is very common in Ethiopia [10], there is little data available on the association between H.pylori infection and hematological parameters and lipid profiles. As far as our knowledge, there is no study on the assessment of electrolyte imbalance among H.pylori dyspeptic patients in Ethiopia. Therefore, this study was conducted to fill the gap in earlier findings and to look into the relationships existing in our nation that could aid in the inpatient care and complication prevention of dyspeptic patients who are H.pylori positive.

Materials and methods

Study design, period and area

An institutional-based comparative cross-sectional study was conducted from February 5 to April 20, 2023, at Jimma Medical Center (JMC), Ethiopia. Geographically, it is situated in Jimma town, which is 352 kilometers southwest of Addis Ababa, the capital city of Ethiopia. JMC is one of the oldest hospitals in Ethiopia, with over 800 beds and a capacity for 16,000 inpatients, 220,000 outpatient attendants, and 12,000 emergency cases. It serves a catchment population of about 15 million people and is the only teaching and referral facility in southwest Ethiopia.

Study participants

The study populations for this study were all dyspeptic patients attending JMC during the study period. The study was conducted on two groups of the study population: one group of dyspeptic patients with H.pylori positive and the other group of dyspeptic patients without H.pylori infection. Subjects with an age <18 years, a history of H.pylori eradication therapy within the past four weeks, on lipid-lowering medications, with known hematological disorders, pregnant women, renal disease, liver disease, and diabetes were excluded from the study.

Sample size determination and sampling technique

The sample size was determined by using the formula for the comparison of two means with equal sample sizes in each group by considering the following assumptions: a confidence interval of 95%, a power of 80%, the mean and standard deviation of Hgb from the previous study [35], 13.32 and 1.56 for the H.pylori-infected group, and 14.25 and 1.89 for the H.pylori negative group. This gives a total of 108 study participants, with 54 in each group. A consecutive sampling technique was employed to recruit the required sample size.

Data and sample collection and laboratory methods

After the study participants were asked for their consent, approximately 3 grams of stool were collected in a sterile, single-use bottle and analyzed by stool antigen test kits from Wondfo (Guangzhou Wondfo Biotech Co., China.) to detect H.pylori antigen. Data on sociodemographic characteristics were collected using a structured questionnaire by trained nurses. In addition, 5 ml of venous blood was withdrawn from the study participants. Two-point-five (2.5) ml of blood sample was used to measure serum electrolytes (Na+, K+, and Cl-) and lipid profiles (TC, HDL-cholesterol, LDL-cholesterol, and triglycerides) using the COBAS 6000 core (Hitachi High-Technologies Corporation, Japan), while 2.5 ml of blood sample was used to measure hematological parameters (Hgb, HCT, RBC, MCV, MCH, MCHC, WBC, and PLT) using SYSMEX XN 550 per the standard operating procedure (SOP).

Data processing and analysis

The data were coded, entered into EpiData version 4.6, and exported to the SPSS version 25 package, where the different variables were tested and analyzed. The Kolmogorov-Shapiro test was used to determine whether the distribution of the data was normal. Simple descriptive statistics and the Chi-square test were used to present the socio-demographic characteristics of the study subjects, and outcomes variables were presented as mean ± standard deviation and compared using two independent t-tests for normally distributed data and media ± interquartile range and compared using the Mann-Whitney U-test for not normally distributed data to test for significant differences between groups, and a P value < 0.05 was considered significant.

Ethics approval and consent to participation

After ethical approval, ethical clearance was obtained from the institutional review board of Jimma University Institute of Health with a reference number (JUIH/IRB2/2/22). Written informed consent was obtained from all the study participants. All patients with abnormal findings were linked to the physician, and the information was maintained confidentially.

Results

Sociodemographic characteristics of the patients

This study included a total of 108 dyspeptic patients, with 54 H.pylori-positive patients and 54 H.pylori-negative patients. The mean age of H.pylori-negative patients was 31.57 with a standard deviation of ±11.46 and 33.15 with a standard deviation of ±10.55 years for H.pylori-infected patients. Among the study subjects, 57 (52.78%) were women, and 56 (51.9%) of the study participants were rural residents. All sociodemographic characteristics were not significantly associated with H.pylori infection (Table 1).

thumbnail
Download:
Table 1. Sociodemographic characteristics of study participants (N = 108, JMC, Jimma, 2023) (Pearson’s Chi-square test).

https://doi.org/10.1371/journal.pone.0310047.t001

Comparisons of hematologic parameters in study participants

The mean (SD) of hematological parameters of patients diagnosed with H.pylori and those without H.pylori infection were compared. Accordingly, red blood cell mean level (RBC = 4.66 ± 0.52 × 106/μL vs. 4.99 ± 0.6 × 106/μL), hemoglobin (Hgb = 13.62 ± 1.69 g/dL vs. 14.48 ± 1.81 g/dL), mean corpuscular hemoglobin concentration (MCHC = 31.79 ± 2.03 g/dl vs. 33.46 ± 1.7 g/dl), and platelet count (PLT = 260.02 ± 70.14 x103/μL vs. 288.85 ± 49.86 x103/μL) were all significantly lower in the H.pylori-infected than the H.pylori-negative group, with p-values of 0.002, 0.012, <0.001, and 0.001, respectively. The mean level of white blood cell counts (WBCs) was slightly higher among participants who had positive H.pylori compared to the mean participants with negative results. However, there is no statistically significant difference (P > 0.05) (Table 2).

thumbnail
Download:
Table 2. Comparisons of mean values of hematologic parameters of H. pylori-infected patients and non-infected study participants at JMC, 2023.

https://doi.org/10.1371/journal.pone.0310047.t002

Comparisons of serum electrolyte level in study participants

The serum median level of sodium (Na+) was significantly lower in the H.pylori-infected group when compared to the H.pylori-negative group (p = 0.006). However, the median serum levels of potassium (K+) and chlorine (Cl-) were not statistically significant between the two groups (p > 0.05) (Table 3).

thumbnail
Download:
Table 3. Comparisons of electrolyte level of H. pylori-infected and non-infected study participants at JMC, 2023 (Mann–Whitney U-Test).

https://doi.org/10.1371/journal.pone.0310047.t003

Comparison of lipid profiles among study participants

The mean serum levels of low-density lipoprotein and total cholesterol were significantly higher among H.pylori-positive patients when compared to H.pylori-negative patients, with p-values of 0.012 and 0.02, respectively. Even though there was a higher level of triglyceride and lower levels of high-density lipoprotein among the H.pylori-infected group, there was no significant difference between the two groups (P > 0.05) (Table 4).

thumbnail
Download:
Table 4. Comparisons of mean values of lipid profiles of H. pylori-infected and non-infected study participants at Jimma Medical Hospital, 2023.

https://doi.org/10.1371/journal.pone.0310047.t004

Discussion

H.pylori has been known for about 40 years as a serious human pathogen that affects half of the world`s population and continues to be a leading cause of mortality and morbidity globally [6]. It has been associated with numerous diseases both inside and outside of the stomach area because of the very virulent substances it produces [11]. Studies revealed that H.pylori infection was connected with derangement of some hematologic parameters, electrolyte levels, and lipid profiles, which may be related to different diseases [36–38].

According to the current study, H.pylori-positive patients had significantly lower mean RBC concentrations than H.pylori-negative patients (p 0.002). This result was consistent with findings from research carried out in Palestine and Sudan [39, 40]. RBC counts may have decreased in H.pylori-positive patients as a result of occult blood loss secondary to peptic ulcers or erosion of chronic gastritis [25]. However, the results of this study were in contrast with previous studies [39] that described no significant difference in RBC count between the two groups. This difference may be due to methodology and socio-demographic characteristics.

In addition, our study revealed that the mean level of Hgb was significantly lower among H.pylori-positive patients when compared to H.pylori-negative participants. This result was in line with other studies conducted in Egypt and Ethiopia [41, 42]. H.pylori’s contribution to the decrement of Hgb count might be due to a change in the pH of the gastric mucosa that causes a decreased level of ascorbic acid, which leads to a decrease in iron absorption from the diet; long-term blood loss secondary to PUD, gastric malignancy, and chronic erosive gastritis that occur due to surface virulent factors of H.pylori like Cag A or due to iron uptake and utilization by H.pylori; and an increase in the liver’s production of hepcidin, which leads to a decrease in iron absorption by enterocytes and release from macrophages [43, 44]. However, the result was not in line with the studies conducted in Saudi Arabia [32].

Furthermore, in this study, there was a statistically significant median difference in MCHC (P < 0.001) levels between the two groups, indicating the effect of H.pylori infection on hematological parameters.

In this study, there was a statistically significant median difference in platelet counts (P = 0.001) between the two groups, as there was higher in H.pylori negative groups (median (IQR)): 288.85 (49.86×103/μl) versus H.pylori positive groups 260.02 (70.14×103/μl). Our result is in line with a study conducted in Egypt [41]. H.pylori might contribute to the decrement in platelet count due to the molecular similarity with H.pylori CagA and the production of autoantibody against H.pylori CagA and the cross-reactivity of these antibodies with platelet surface antigens (GP Ia/IIa and GP Ib/IX) and platelet clump due to the presence of von Willebrand factor and anti-H-pylori IgG [45]. However, our findings contradict those of studies from Saudi Arabia [32] and Palestine [40], which reported there was no significant mean difference in platelet count between the two groups.

In the current study, median values of sodium (Na+) concentration were lower in H.pylori-infected patients compared to the H.pylori negative group, which was statistically significant (P = 0.006). This finding is supported by studies conducted in Saudi Arabia [38]. H.pylori may have contributed to the drop in sodium concentration due to H.pylori’s attachment to gastric mucosal cells, which decreases Na-K-ATPase through enhanced ubiquitylation of Na-K-ATPase [28]. Alteration of Na + K + ATPase might affect the level of serum sodium levels by inhabiting the efflux of sodium out of the cell. In addition, H.pylori produces ammonia, leading to the accumulation of excessively hazardous levels of ammonia, which decreases the absorption of sodium due to damage to the digestive tract by ammonia [46].

Persisted H.pylori infection may affect the lipid profile, which leads to increased levels of total cholesterol, LDL-c, lipoprotein Lp(a), apolipoprotein apo-B, triglyceride concentrations, and decreased levels of HDL-C and apolipoprotein apoA-1 concentrations [18, 47]. The current study also found that patients with H.pylori infections had significantly higher levels of total cholesterol and LDL-c than did healthy people (p-values of 0.02 and 0.012, respectively). This result is consistent with earlier researches [48–50].

This could be due to the involvement of cytokines in H.pylori infection, especially IL-6, IL-1, INF-α, and TNF-α, which affect lipid metabolism through stimulation of hepatic fatty acid synthesis, activation of adipose tissue lipoprotein lipase, and influencing lipolysis [18, 47]. Since H.pylori increases small intestine mucosal permeability, which allows bacterial toxins to reach the liver through the portal vein and cause hepatic tissue damage, lipid levels can also be altered by direct liver dysfunction [51].

A change in lipid profile may also be caused by H.pylori-related ghrelin and leptin release or by an imbalance in nutritional absorption as a result of digestive system inflammation, which might lead to atherosclerotic lipid profiles and elevated cardiovascular risk [52]. After H.pylori was effectively eradicated, LDL returned to levels that were nearly H.pylori-negative, confirming their close relationship [51]. Contrary to the aforementioned discoveries, some studies did not show the association of H.pylori infection with altered LDL-c and total cholesterol [37, 53, 54]. These controversial study findings may be explained by the varying study methodologies employed, such as different study populations or sample sizes.

Limitations of the study

This study used a non-probability sampling technique to recruit the study participants, which may affect the external validity of the findings. In our study, stool bacterial load and the strain of H.pylori were not evaluated; therefore, the effect of H.pylori virulence factors could not be identified.

Conclusions

This study revealed that the mean values of platelet, RBC, Hgb, and MCHC count were significantly decreased in H.pylori-positive participants when compared to H.pylori-negative patients. In addition, H.pylori infection alters the serum electrolytes, which were significant in Na+. There were also significant increments in LDL-c and total cholesterol in the H.pylori-infected group, which created an atherogenic lipid. Hence, dyspeptic patients infected by H.pylori will be at high risk for anemia, atherosclerosis, and associated cardiovascular disease. Therefore, timely diagnosis and eradication of H.pylori in the infected patients and evaluation of serum electrolytes, hematologic parameters, and lipid profiles for those infected by H.pylori were recommended.

Acknowledgments

The authors would like to express their appreciation to the study participants for their cooperation in this study. In addition, we would like to thank data collectors and laboratory personnel at Jimma Medical Center for their support.

References

  1. 1. Boakye-Yiadom M, Obiri DD, Martey ONK, Yeboah R, Offei-Abrokwa D, Ocloo A, et al. Management of Dyspepsia with Enterica, Mist Dyspepsia and Natural Pain Killer herbal-combination at the Centre for Plant Medicine Research Clinic, Ghana. J Herb Med. 2022;32:100553.
  2. 2. Tonde T V, Patil SS, Vaishnav BT, Reddy S, Barla DR. Study of High sensitivity C Reactive Protein Levels in Patients with Chronic Dyspepsia and Its Correlation with Helicobacter Pylori Infection. Indian J Basic Appl Med Res. 2019;9(1):423–8.
  3. 3. William OR, Martín GZ, Lina OP. Update on approaches to patients with dyspepsia and functional dyspepsia. Rev Colomb Gastroenterol. 2014;29(2):132–8.
  4. 4. Koduru P, Irani M, Quigley EMM. Definition, Pathogenesis, and Management of That Cursed Dyspepsia. Clin Gastroenterol Hepatol. 2018;16(4):467–79.
  5. 5. Abass A, Mohamed KO, Yosif AA, Mohamed FA, Mohamed Z, Elfadil M. Evaluation of Serum Vitamin B12 and Ferritin Levels in H. Pylori- Associated Gastritis. IOSR J Pharm Biol Sci. 2016;11(1):1–5.
  6. 6. Katelaris P, Hunt R, Bazzoli F, Cohen H, Fock KM, Gemilyan M, et al. Helicobacter pylori. World Gastroenterol Organ Glob Guidel. 2021;(May):1–31.
  7. 7. Natuzzi E. is it time to add helicobacter pylorito the list? Glob Heal Promot. 2013;20(3):47–8.
  8. 8. Hu Y, Wan JH, Li XY, Zhu Y, Graham DY, Lu NH. Systematic review with meta-analysis: the global recurrence rate of Helicobacter pylori. Aliment Pharmacol Ther. 2017;46(9):773–9. pmid:28892184
  9. 9. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, et al. Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology. 2017;153(2):420–9. pmid:28456631
  10. 10. 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(8).
  11. 11. Kishk RM, Soliman NM, Anani MM, Nemr N, Salem A, Attia F, et al. Genotyping of Helicobacter pylori Virulence Genes cagA and vacA: Regional and National Study. Int J Microbiol. 2021;5540560. pmid:34306090
  12. 12. Diaconu S, Predescu A, Moldoveanu A, Pop CS, Fierbințeanu-Braticevici C. Helicobacter pylori infection: old and new. J Med Life. 2017;10(2):112–7. pmid:28616085
  13. 13. Plummer M, Franceschi S, Vignat J, Forman D, De Martel C. Global burden of gastric cancer attributable to pylori. Int J Cancer. 2015;136(2):487–90.
  14. 14. Shah SC, Iyer PG, Moss SF. Clinical Practice Update on the Management of Refractory Helicobacter pylori Infection: Expert Review. Gastroenterology. 2021;160(5):1831–41.
  15. 15. Dincă AL, Melit LE, Mărginean CO. Old and New Aspects of H. pylori-Associated Inflammation and Gastric Cancer. Children. 2022;9(7):1083. pmid:35884067
  16. 16. Ndebi ME, Guimtsop YAT, Tamokou J-D. The assessment of risk factors, lipid profile, uric acid and alanine aminotransferase in Helicobacter pylori-positive subjects. Int J Res Med Sci. 2018;6(9):2889.
  17. 17. Khovidhunkit W, Kim MS, Memon RA, Shigenaga JK, Moser AH, Feingold KR, et al. Effects of infection and inflammation on lipid and lipoprotein metabolism: Mechanisms and consequences to the host. J Lipid Res. 2004;45(7):1169–96. pmid:15102878
  18. 18. Furuto Y, Kawamura M, Yamashita J, Yoshikawa T, Namikawa A, Isshiki R, et al. Relationship between Helicobacter pylori infection and arteriosclerosis. Int J Gen Med. 2021;14:1533–40. pmid:33935515
  19. 19. Jacek B, Kozin M, Kłopocka M, Kubica JM, Kubica J. Clinical significance of Helicobacter pylori infection in patients with acute coronary syndromes: an overview of current evidence. Clin Res Cardiol. 2014;103(11):855–86. pmid:24817551
  20. 20. Watanabe J, Hamasaki M, Kotani K. The Effect of Helicobacter pylori Eradication on Lipid Levels: J Clin Med. 2021;10(5):904.
  21. 21. Angaw DA, Ali R, Tadele A, Shumet S. The prevalence of cardiovascular disease in Ethiopia: a systematic review and meta ‑ analysis of institutional and community ‑ based studies. BMC Cardiovasc Disord [Internet]. 2021;21(37):1–9. Available from: pmid:33461482
  22. 22. Campuzano-Maya G. Hematologic manifestations of Helicobacter pylori infection. World J Gastroenterol. 2014;20(36):12818–38. pmid:25278680
  23. 23. Elamin EAI, Suliman MA, Azoz ME, Ali EW, Olerile LD, Jiao Y, et al. Effect of Helicobacter pylori infection on haematological parameters in Kosti teaching hospital, Sudan. Iran Red Crescent Med J. 2018;20(2):e58276.
  24. 24. Hudak L, Jaraisy A, Haj S, Muhsen K. An updated systematic review and meta-analysis on the association between Helicobacter pylori infection and iron deficiency anemia. Helicobacter. 2017;22(1):1–16. pmid:27411077
  25. 25. Rahman A, Raihan A, Ahmed DS, Karim ME, Saeed A, Siddique AR, et al. Association between Helicobacter Pylori Infection and Iron Deficiency Anemia: A Cross Sectional Study. J Bangladesh Coll Physicians Surg. 2020;38(2):68–78.
  26. 26. Tsay F, Hsu P.H. pylori infection and extra-gastroduodenal diseases. J Biomed Sci. 2018;25(65):1–8.
  27. 27. Jang JH, Kim JY, Mun YC, Bang SM, Lim YJ, Shin DY, et al. Management of immune thrombocytopenia: Korean experts recommendation in 2017. Blood Res. 2017;52(4):254–63. pmid:29333401
  28. 28. Marcus EA, Tokhtaeva E, Jimenez JL, Wen Y, Naini B V., Heard AN, et al. Helicobacter pylori infection impairs chaperone-assisted maturation of Na-K-ATPase in gastric epithelium. Am J Physiol—Gastrointest Liver Physiol. 2020;318(5):G931–45. pmid:32174134
  29. 29. Molla MD, Degef M, Bekele A, Geto Z, Challa F, Lejisa T, et al. Assessment of serum electrolytes and kidney function test for screening of chronic kidney disease among Ethiopian Public Health Institute staff members, Addis Ababa, Ethiopia. BMC Nephrol. 2020;21(1):494–504. pmid:33208123
  30. 30. Hata K, Koyama T, Ozaki E, Kuriyama N, Mizuno S, Matsui D, et al. Assessing the relationship between helicobacter pylori and chronic kidney disease. Healthc. 2021;9(2):162–9. pmid:33546229
  31. 31. Kughapriya P, Ponnudhali D, Jones E. Evaluation of serum electrolytes in Ischemic Heart Disease patients. Natl J Basic Med Sci. 2016;6(4):163–7.
  32. 32. Ibrahim NK, Al-sayes FM, Alidrous FA, Alahmadi MM. Helicobacter Pylori: Prevalence and Relationship to Hematological Parameters of Symptomatic Patients who Conducted Gastroscopy at King Abdulaziz University Hospital, Jeddah. J Adv Med Med Res. 2019;28(9):1–9.
  33. 33. AlFawaeir S, Zaid M, Awad A, Alabedallat B. Serum lipid profile in Helicobacter pylori infected patients. J Investig Biochem. 2013;2(2):132.
  34. 34. Darabi H, Hadavand F, Ostovar A, Manesh ZM, Vahdat K, Nabipour I. Association of Helicobacter pylori infection with lipid profiles: Healthy heart, population based study, Bushehr. Iran South Med J. 2014;17(4).
  35. 35. Haile K, Timerga A. Evaluation of hematological parameters of Helicobacter pylori-infected adult patients at Southern Ethiopia: A comparative cross-sectional study. J Blood Med. 2021;12:77–84. pmid:33654446
  36. 36. Haile K, Timerga A. Evaluation of Hematological Parameters of Helicobacter pylori -Infected Adult Patients at Southern Ethiopia: A Comparative Cross-Sectional Study. J Blood Med. 2021;12:77–84. pmid:33654446
  37. 37. Sun Y, Fu D, Yk W, Liu M, Xd L. Prevalence of Helicobacter pylori infection and its association with lipid pro fi les. Bratislava Med J. 2016;117(9):521–4.
  38. 38. Bhal G, Fa A, Alhayyani S, Naqvi S, Kumar V, Anwar F. The Association Between ABO Blood Group Distribution and Helicobacter Pylori Infec- tion: A Cross-Sectional Study. Japanese J Gastroenterol Hepatol Clin. 2022;8(6):1–8.
  39. 39. Azoz ME, Almugadam BS, Ibrahim OM, Ahmed YM, Tayeb AA, Eshagg NH, et al. Detection, clinical features, and laboratory markers of H.pylori infection in individuals attended kosti teaching hospital, Sudan. Biomed Biotechnol Res J. 2022;6(2):278–83.
  40. 40. Mwafy SN, Afana WM. Hematological parameters, serum iron and vitamin B12 levels in hospitalized Palestinian adult patients infected with Helicobacter pylori: a case–control study. Hematol Transfus Cell Ther. 2018;40(2):160–5. pmid:30057990
  41. 41. Rahman YA, Ahmed LA wahid, Hafez RMM, Ahmed RMM. Helicobacter pylori and its hematological effect. Egypt J Intern Med. 2019;31(3):332–42.
  42. 42. 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. 2014;14:656. pmid:25487159
  43. 43. Mendoza E, Duque X, I J, Franco H, Maldonado ER, Morán S, et al. Association between Active H. pylori Infection and Iron Deficiency Assessed by Serum Hepcidin Levels in School-Age Children. Nutrients. 2019;11:2141. pmid:31500264
  44. 44. Stein J, Connor S, Virgin G, Eng D, Ong H, Pereyra L. Anemia and iron deficiency in gastrointestinal and liver conditions. World Joural Gastroenterol. 2016;22(35):7908–25. pmid:27672287
  45. 45. Ihtesham A, Maqbool S, Nadeem M, Abbas MB. Helicobacter pylori induced Immune Thrombocytopenic Purpura and perspective role of Helicobacter pylori eradication therapy for treating Immune Thrombocytopenic Purpura. AIMS Microbiol. 2021;7(3):284–303. pmid:34708173
  46. 46. Nasrat SAM, Nasrat AM. An Alternative Approach for the Rising Challenge of Hypertensive Illness via Helicobacter pylori Eradication. CardiolResparatory. 2015;6(1):221–5. pmid:28197229
  47. 47. Albaker WI. Helicobacter pylori infection and its relationship to metabolic syndrome: is it a myth or fact? Saudi J Gastroenterol. 2011;17(3):165–9. pmid:21546717
  48. 48. Nigatie M, Asmelash D. Dyslipidemia and Its Associated Factors Among Helicobacter pylori -Infected Patients Attending at University of Gondar Comprehensive Specialized Hospital, Gondar, North-West Ethiopia: A Comparative Cross-Sectional Study. J Multidiscip Healthc. 2022;15:1481–91. pmid:35873092
  49. 49. Hashim M, Mohammed O, Egzeabeher TG, Wolde M. Heliyon The association of Helicobacter Pylori infection with dyslipidaemia and other atherogenic factors in dyspeptic patients at St. Paul ‘ s Hospital Millennium Medical College. Heliyon. 2022;8:e09430.
  50. 50. Ibrahim HA, Mohammed MO, Dhahir HAR, Mahmood KA, Nuradeen BE. Impact of Helicobacter pylori Infection on Serum Lipid Profile and Atherosclerosis of Carotid Artery. Int J Clin Med. 2014;05(15):933–9.
  51. 51. Wang Z, Wang W, Gong R, Yao H, Fan M, Zeng J, et al. Eradication of Helicobacter pylori alleviates lipid metabolism deterioration: a large-cohort propensity score-matched analysis. Lipids Health Dis. 2022;21(7):857–66. pmid:35369887
  52. 52. Shimamoto T, Id NY, Gondo K, Takahashi Y. The association of Helicobacter pylori infection with serum lipid profiles: An evaluation based on a combination of meta-analysis and a propensity score-based observational approach. PLoS One. 2020;15(6):e0234433. pmid:32511269
  53. 53. Aarabi MH, Shokofeh Alvani HE. Lipid Profile in Subjects with Helicobacter pylori Infection. Iran J Pathol. 2010;5(4):199–203.
  54. 54. Upala S, Sanguankeo A, Saleem SA, Jaruvongvanich V. Effects of Helicobacter pylori eradication on insulin resistance and metabolic parameters: A systematic review and meta-analysis. Eur J Gastroenterol Hepatol. 2017;29(2):153–9. pmid:27832037