Skip to main content
  • Research article
  • Open access
  • Published:

Helicobacter pyloriinfection and its association with anemia among adult dyspeptic patients attending Butajira Hospital, Ethiopia

Abstract

Background

Helicobacter pylori infection is associated with anemia. Understanding the magnitude of H.pylori infection and its association with anemia is important in the management of anemic patients. The aim of this study was to assess the association between H.pylori infection and anemia among dyspeptic patients.

Methods

A cross-sectional study was conducted in Butajira Hospital, Southern Ethiopia among 401 systematically dyspeptic patients. A structured questionnaire was used to collected data about the patient characteristics. Blood samples were analyzed for red blood cell parameters. Stool samples were assessed for the presence of H.pylori antigens and the presence of intestinal helminthes. Data were summarized in frequencies (%) and mean (SD) as appropriate. Chi-square test, logistic regression and independent t-tests were used in the analysis as needed. In all cases P-value <0.05 was considered as statistically significant.

Results

The overall prevalence of H. pylori infection was 52.4% and it was significantly associated with age, presence of intestinal parasites, smoking habit, alcohol drinking habit and body mass index. The prevalence of anemia among H.pylori infected patients (30.9%) was significantly (P < 0.001) higher than uninfected patients (22.5%). The mean (SD) values of HGB, MCV, MCH, MCHC, HCT and RBC count was significantly different between H.pylori infected and uninfected patients.

Conclusion

This study showed high prevalence of H.pylori infection among dyspeptic patients and this was associated with age and some behavioral characteristics of the patients. H.pylori infected patients showed high rate of anemia prevalence as compared to their H.pylori unifected counter parts. From this study it can be recommended that intervention activities related to the behavioral characteristics and prevention of intestinal parasitic infections should be in place. The cross sectional nature of the study has a limitation to show cause and effect associations and hence association between H.pylori infections with anemia need to be investigated in cohort type studies.

Peer Review reports

Background

Helicobacter pylori infection has been recognized as one of the most common chronic bacterial infections in humans and infecting more than half of the population of the world. The overall prevalence is high in developing countries [1]. H. pylori infection is a worldwide problem but the prevalence varies from country to country [1],[2]. H. pylori infection is acquired in early childhood and becomes a chronic infection if left untreated [3]. The majority of infected people remain asymptomatic, and only small portions develop illness, usually in adulthood [4]. H. pylori cause upper gastrointestinal disease such as gastritis, peptic ulcer disease and also increase the risk of gastric cancer [5],[6]. Male gender, increasing age, shorter height, tobacco use, lower socioeconomic status, obesity, and lower educational status of the parents in studies conducted among children are proposed risk factors for infection [7].

Several studies suggested an association between H. pylori infection with iron deficiency and anemia [8],[9]. H. pylori infection and extra gastric manifestations, pernicious anemia (10) and idiopathic thrombocytopenic purpura have been reported [10],[11]. Active H. pylori infection was independently associated with iron deficiency and iron-deficiency anemia [12],[13] and presence of H. pylori infection is associated with a poorer response to oral iron therapy [14]. It has been suggested that eradication of H. pylori may result in improvement of anemia even without iron supplementation [14],[15].

It is hypothesized that H. pylori-associated with anemia is caused by both compromised absorption of bio-available iron in the context of hypochlorhydria [16], and the competing iron demands of H. pylori and the host [17],[18]. Most dietary iron is in the non-hemic ferric form, and an acidic intra-gastric pH is needed to reduce it to the ferrous form for absorption. This reaction is promoted by gastric acidity and ascorbic acid, which is thus considered the most potent regulator of iron absorption [19]. H. pylori a major cause of chronic superficial gastritis leading to atrophy of gastric glands and leading to decreased gastric acid secretion [20]. H. pylori need iron to thrive and it possesses a 19-kDa iron-binding protein resembling ferritin, that may play a role in storage of excessive iron by the bacteria [21]. Moreover, since these bacteria have a high turnover rate, a large amount of iron may be lost in stools in the form of dead bacteria [22]. H. pylori has been found more frequently in dyspeptic patients [23]. The aim of the current study was to investigate the relation between H. pylori infection and anemia among dyspeptic patients attending medical care at Butajira Hospital.

Methods

Study area

The study was conducted at Butajira hospital which is found in Butajira town, Gurage Zone, Southern Nations Nationalities, and People’s Region (SNNPR) located 135 km from the capital-city, Addis Ababa. The town lies on the average at 2,100 m above the sea level. Butajira hospital is a zonal hospital with 110 beds that gives health service for peoples living in Butajira and the surrounding rural kebeles. The hospital report shows that it gives health service for an average of about 250 patients per day at the outpatient department. The hospital catchment area population is estimated around 1.3 million.

Study design and period

A cross-sectional prospective study was conducted from April to Jun 2013.

Sample size and sampling technique

The sample size was determined by using single population proportion formula taking 53% prevalence of H. pylori infection among dyspeptic patients [24] and a marginal error of 5%. Accordingly the sample size was determined 382 but we also considered a 5% non-response rate so that the final sample size was 401.

Study subjects were included using systematic random sampling technique. In Butajira hospital an average of 18 dyspeptic patients attend the outpatient clinic each day. The total expected dyspeptic patients during the study period were estimated 792. When the total population was divided by the sample size, the sample interval was found 2 and every two dyspeptic patient were selected until a total of 401 samples obtained.

All adult (age ≥18 years) patients presented with dyspepsia complaint were included in the study. Among those patients who were voluntary to participate in the study, those who had any surgery and blood donation, previous stomach or small bowel surgery, those who took treatment for H. pylori within the last three month, and pregnant women excluded. The patients were excluded, due to any of the exclusion criteria, from the study following critical review of their medical charts.

Data collection and laboratory methods

General characteristics of the study participants

A structured questionnaire was used to collect data on demographic (sex, age, monthly income, marital status, educational status), behavioral (smoking, alcohol intake, dietary habit) and physical (body mass index) characteristics of the study participants. BMI ≤ 18.5 kg/m2 was classified as underweight; BMI = 18.6–24.9 kg/m2 as normal weight; BMI = 25-29.9 kg/m2 as overweight; and BMI ≥ 30 kg/m2 as obese [25].

Sample collection and analysis

About 3 ml of venous blood was collected and examined for hematological parameters using Sysmex K-21 hematology analyzer. Approximately three gram of stool sample was collected in a clean screw cupped plastic container and checked for the presence of H. pylori antigen using H. pylori Rapid Test Strip (Creative Diagnostics.). Portion of the stool sample was used to assess the presence of intestinal helminthes using formol ether concentration technique as per a standard procedure [26].

Data analysis and interpretation

Data were entered and analyzed using SPSS version 16.0. Continuous variables were summarized using means (±SD) and categorical variables were summarized in frequencies (percentages). Association between the prevalence of anemia and H.pylori infection was assessed by χ2 tests. Anemia was defined according to the WHO definition as a hemoglobin concentration of < 12 g/dL in women, < 13 g/dL in men [27]. The difference in the mean values of RBC parameters between H.pylori positive and negative individuals was explored using independent sample T-test. Logistic regression was used to determine the effect of independent variables on the prevalence of H.pylori infection. In all case a 95% confidence interval was used and P-values less than 0.05 were considered as statistically significant.

Ethical consideration

The study was commenced after ethically approved by the ethical review committee of the School of Biomedical and Laboratory Science, University of Gondar. Permission to conduct the study was also obtained from the hospital administration. Written informed consent was obtained from each study participant and the results were kept confidential. Any result that was necessary for the patient was communicated with the physician for appropriate management.

Results

Sociodemographic, behavioral and physical characteristics of the study participants

A total of 401 adult dyspeptic patients (148 males and 253 females) with a mean (±SD) age of 37.3 (±13.7) years participated in this study. Majority of them were rural residents (70%), married (72.8%), and illiterate (56.9%). The mean (±SD) body mass index of the study population was 20.4 (±2.3) kg/m2. During the time of data collection about 4.5% and 10.7% of the study participants had a habit of cigarette smoking and drinking alcohol respectively. An assessment on the food habits of the study participants revealed that 8.7%, 63.8% and 33.4% had a habit of eating meat, vegetables and eggs 1-3 days/week respectively. Intestinal parasites were identified in 30.7% of the study participants (Table 1).

Table 1 Sociodemographic, behavioral and physical characteristics of the study participants

Prevalence of H.pyloriinfection and associated risk factors

The overall prevalence of H. pylori infection was 52.4% (n = 210); 66.7% (n = 140) in females and 33.3% (n = 70) in males. The relative frequency of the infection was higher in the age group 39-48 (50.6%) and among urban dwellers (54.4%). Among the different characteristics of the study participants’; age, presence of intestinal parasites, smoking habit, alcohol drinking habit and BMI showed statistically significant association with H.pylori infection (Table 2).

Table 2 Bivariate and multivariate analysis of patient characteristics with H. pylori infection

Prevalence of anemia and its association with H.pyloriinfection

Prevalence of anemia among dyspeptic patient was 26.9% (n = 108); 64.8% in females and 35.2% in males. The mean (±SD) hemoglobin concentration was 13.2(±1.4) g/dl and 14.1(±1.5) g/dl in females and males respectively. The prevalence of anemia among H.pylori infected patients was 30.9% and 22.5% among uninfected patients. The difference in the prevalence of anemia between H.pylori infected and uninfected patients was statistically significant (χ2 = 26.8; P < 0.001) (Table 3). The mean (SD) of other parameters related to red blood cell were also compared between H.pylori infected and uninfected patients. Accordingly statistically significant differences were observed in HGB, MCV, MCH, MCHC, HCT and number of RBC (Table 4).

Table 3 Association between H.pylori sero-status and anemia prevalence among dyspeptic patients
Table 4 Association between RBC indices with H.pylori infection

Discussion

In this study, the prevalence of H. pylori infection among patients with dyspeptic symptoms was 52.37%. This prevalence is relatively lower than other reports conducted in different parts of African and Asia continent, which reported a prevalence ranging from 67% up to 86.8% [28]-[31]. The prevalence of H pylori varies greatly among countries and among population groups within the same country [2]. However, our finding is relatively similar with previous reports made in Ethiopia 53% [24] and Kuwait 49.7% [32]. Lack of clear cut definition of dyspepsia, H. pylori diagnostic method, sample size, social and economic factors could be some of the possible reasons for these variations.

The results of the current study also showed slight difference in prevalence of H. pylori infection between females and males (55.3% vs 47.3% respectively), but the difference was not statistically significant (P = 0.12). This finding goes in contrary to previous reports that indicated females were at significant risk to have for H. pylori infection (24, 32,33). However, our findings agree with other studies that showed the rate of H. pylori infection is independent of gender [31],[24],[30].

We found correlation between age and H. pylori infection being the prevalence was higher in older age groups (P < 0.001). This finding is in accordance with the results of former studies made in Kuwait [32] South Africa [33] and Ethiopia [30]. Moreover, study conducted in Addis Ababa, Ethiopia, showed a peak prevalence of H. pylori infection among older patients, within the age group between 54-61 years [24]. The most probable reason is that infection by H. pylori can be acquired in earlier age and persist throughout the life time of the patient and may cause disease at older age. However, there are also reports that showed higher prevalence of H. pylori infection during the younger age. For example, study conducted in Iran showed patient at younger age were more affected [31] and in Nigeria the peak prevalence of H. pylori infection was found among patients within the age group between 20-39 years old [29].

The current study result also showed a significant negative association betteween alcohol consumption and H. pylori infection (AOR 0.37; 95%; CI 0.17-0.82, P = 0.014). This result contradicts with previous report from Gondar, Ethiopia [30] and South Africa [33] that showed a positive association between H. pylori infection and alcohol consumption. In those studies it was reported that alcohol consumption could be a risk factor for H. pylori infection. Nevertheless, there are also reports that documented a non statistical risk reduction of H. pylori infection upon alcohol consumption [34]. Besides, the type and amount of alcohol had also an effect on the association. However, basic microbiology tells us that alcohol is known to have direct antimicrobial effects. Therefore, the lower prevalence of H. pylori infection among patients that consumed alcohol compared with the non-alcoholics attracted us to support the hypothesis that alcohol intake may have preventive effect for H. pylori infection.

In this study cigarette smoking was significantly associated with H. pylori infection (P = 0.01). Unlike other studies that reported no significant association with current smoking or any other measure of using tobacco [34]. Others proposed that smoking appears to affect treatment success [35]. These contradictory results may be due to uncontrolled confounding factors such as social class or differential antibiotic use.

Intestinal parasitic infection in this study was significantly associated with H. pylori infection (p = 0.009). This is different from a finding from Australia [36]. Intestinal parasitic infections and elevated IgE levels were associated with a reduced H. pylori prevalence in adults, living in Mexico, suggesting that intestinal parasites could affect persistence of H. pylori [37]. The presence of association in our study may be due to poor hygienic status that favors high rate of parasitic infection and similar route of transmission shared by H.pylori. But the real mechanism of interaction needs to be investigated with cohort studies.

There are quite a number of studies in the literature demonstrated the relationship between H. pylori infection and anemia. In the current study, the prevalence of anemia among H. pylori positive patients (n = 65, 30.95%) was significantly higher (P = 0.05) than H .pylori negative patients (n = 43; 22.5%). But other studies from Latin American countries showed no association [38] while a study from Haiti showed an inverse association [39]. The association observed in our study was also reflected on other RBC parameters as determined using t-test. We found that H. pylori stool antigen positive patients have significantly lower hemoglobin and hematocrit levels than H. pylori negative patients (13.3 g/dl versus 13.8 g/dl, P = 0.001) and (41.9% versus 43.3%, P = 0.009) respectively. Similar observation was reported from Turkish among teenager [40]. However, findings are not in agreement with the reports made by Fraser et al [41] and Kermati et al [42] where no association between H. pylori infection and Hgb/HCT levels was reported. Moreover, there was statistically significant difference in MCHC (P = 0.002) and MCH (P = 0.003) values between H. pylori stool antigen positive and negative dyspeptic patients, indicating the impact of H. pylori infection on hematological parameters.

Limitations of the study

This study was conducted on dyspeptic patients who have had many underline disease conditions as a confounding factors that could not fully controlled so that it might have impact on the outcome of the statistical correlations between H. pylori infection, anemia and other variables of interest. The cross sectional nature of the study was also another limitation to show cause and effect relationship between the variables.

Conclusion

This study indicated that the prevalence of H. pylori infection was high among dyspeptic patients in the study area. The rate of H. pylori infection was also increasing in advancing age showing that age is one of the risk factors in acquiring the infection. Moreover, cigarette smoking, and intestinal helmintic infection were identified as risk factors for H. pylori infection too. Alcohol consumption habit in our study was negatively associated with H. pylori infection. Mean hematological parameters and RBC were significantly reduced among H. pylori positive patients compared. This study indicated the need for further large scale study to determine the possible risk factors for such high rate of infection. Moreover cohort type studies are recommended to formulate a cause and effect relationship between the risk factors and H.pylori sero-positivity.

References

  1. Hunt RH, Xiao SD, Megraud F, Leon-Barua R, Bazzoli F, van der Merwe S, Vaz Coelho LG, Fock M, Fedail S, Cohen H, Malfertheiner P, Vakil N, Hamid S, Gohl KL, Wong BC, Krabshuis J, Le Mair A: World Gasteroenterology Organization Global Guide line: Helicobacter pylori in Developing Countries. World Gasteroenerology Organization, 2010. , [http://www.worldgastroenterology.org/assets/downloads/en/pdf/guidelines/11_helicobacter_pylori_developing_countries_en.pdf]

  2. Suerbaum S, Michetti P: Helicobacter pylori infection. N Engl J Med. 2002, 347: 1175-1186. 10.1056/NEJMra020542.

    Article  CAS  PubMed  Google Scholar 

  3. Torres J, Perez-Perez G, Goodman KJ, Atherton JC, Gold BD, Harris PR, La Garza AM, Guarner J, Muñoz O: A comprehensive review of the natural history of Helicobacter pylori infection in children. Arch Med Res. 2000, 31: 431-469. 10.1016/S0188-4409(00)00099-0.

    Article  CAS  PubMed  Google Scholar 

  4. Cover TL, Blaser MJ: Helicobacter pylori in health and disease. Gastroenterology. 2009, 136: 1863-1873. 10.1053/j.gastro.2009.01.073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Egan BJ, O’Connor HJ, Morain CAO: What is new in the management of Helicobacter pylori?. Ir J Med Sci. 2008, 177: 185-188. 10.1007/s11845-008-0173-8.

    Article  CAS  PubMed  Google Scholar 

  6. Malfertheiner P, Megraud F, O’Morain C, Bazzoli F, El-Omar E, Graham D, Hunt R, Rokkas T, Vakil N, Kuipers EJ: Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut. 2007, 56: 772-781. 10.1136/gut.2006.101634.

    Article  CAS  PubMed  Google Scholar 

  7. Ford AC, Axon ATR: Epidemiology of Helicobacter pylori infection and Public Health Implications. Helicobacter. 2010, 15: 1-6. 10.1111/j.1523-5378.2010.00779.x.

    Article  PubMed  Google Scholar 

  8. Qu XH, Huang XL, Xiong P, Zhu CY, Huang YL, Lu LG, Sun X, Rong L, Zhong L, Sun DY, Lin H, Cai MC, Chen ZW, Hu B, Wu LM, Jiang YB, Yan WL: Does Helicobacter pylori infection play a role in iron deficiency anemia? A metaanalysis. World J Gastroenterol. 2010, 16: 886-896.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Muhsen K, Cohen D: Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter. 2008, 13: 323-340. 10.1111/j.1523-5378.2008.00617.x.

    Article  CAS  PubMed  Google Scholar 

  10. Sarari AS, Farraj MA, Hamoudi W, Essawi TA: Helicobacter pylori, a causative agent of vitamin B12 deficiency. J Infect Dev Countries. 2008, 2: 346-349.

    Google Scholar 

  11. Stasi R, Sarpatwari A, Segal JB, Osborn J, Evangelista ML, Cooper N, Provan D, Newland A, Amadori S, Bussel JB: Effects of eradication of Helicobacter pylori infection in patients with immune thrombocytopenic purpura: a systematic review. Blood. 2009, 113: 1231-1240. 10.1182/blood-2008-07-167155.

    Article  CAS  PubMed  Google Scholar 

  12. Baggett HC, Parkinson AJ, Muth PT, Gold BD, Gessner BD: Endemic iron deficiency associated with helicobacter pylori infection among school-aged children in Alaska. Pediatrics. 2006, 117: 396-404. 10.1542/peds.2005-1129.

    Article  Google Scholar 

  13. Ashorn M, Ruuska T, Makipenaa A: Helicobacter pylori infection and iron deficiency anemia in children. Scand J Gastroenterol. 2001, 36: 701-705. 10.1080/003655201300191950.

    Article  CAS  PubMed  Google Scholar 

  14. Valiyaveettil AN, Hamide A, Bobby Z, Krishnan R: Effect of anti-Helicobacter pylori therapy on outcome of iron-deficiency anemia: a randomized, controlled study. Indian J Gastroenterol. 2005, 24: 155-157.

    PubMed  Google Scholar 

  15. Malik R, Guleria K, Kaur I, Sikka M, Radhakrishnan G: Effect of Helicobacter pylori eradication therapy in iron deficiency anaemia of pregnancy – A pilot study. Indian J Med Res. 2011, 134: 224-231.

    PubMed  PubMed Central  Google Scholar 

  16. Harris PR, Serrano CA, Villagrán A, Walker MM, Thomson M, Duarte I, Windle HJ, Crabtree JE: Helicobacter pylori-associated hypochlorhydria in children, and development of iron deficiency. J Clin Pathol. 2013, 66: 343-347. 10.1136/jclinpath-2012-201243.

    Article  CAS  PubMed  Google Scholar 

  17. Shaw JG, Friedman JF: Iron deficiency anemia: focus on infectious diseases in lesser developed countries. Anemia 2011:1–10. , [http://www.hindawi.com/journals/anemia/2011/260380/]

  18. Annibale B, Capurso G, Lahner E, Passi S, Ricci R, Maggio F, Delle FG: Concomitant alterations in intragastric pH and ascorbic acid concentration in patients with Helicobacter pylori gastritis and associated iron deficiency anaemia. Gut. 2003, 52: 496-501. 10.1136/gut.52.4.496.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Conrad ME, Umbreit JN: Iron absorption and transport-an update. Am J Hematol. 2000, 64: 287-298. 10.1002/1096-8652(200008)64:4<287::AID-AJH9>3.0.CO;2-L.

    Article  CAS  PubMed  Google Scholar 

  20. Lacy BE, Rosemore J: Helicobacter pylori: ulcers and more: the beginning of an Era;symposium. J Nutr. 2001, 131: 2789-2793.

    Google Scholar 

  21. Doig P, Austin JW, Trust TJ: The Helicobacter pylori 19.6-kilodalton protein is an iron-containing protein resembling ferritin. J Bacteriol. 1993, 61: 2694-2697.

    Google Scholar 

  22. Seo JK, Ko JS, Choi KD: Serum ferritin and Helicobacter pylori infection in children: a sero-epidemiologic study in Korea. J Gastroenterol Hepatol. 2002, 17: 754-757. 10.1046/j.1440-1746.2002.02797.x.

    Article  PubMed  Google Scholar 

  23. Kandulski A, Venerito M, Malfertheiner S: Therapeutic strategies for the treatment of dyspepsia. Expert Opin Pharmaco Ther. 2010, 11: 2517-2525. 10.1517/14656566.2010.501794.

    Article  CAS  Google Scholar 

  24. Taddesse G, Habteselassie A, Desta K, Esayas S, Bane A: Association of dyspepsia symptoms and Helicobacter pylori infections in private higher clinic, Addis Ababa, Ethiopia. Ethiop Med J. 2011, 49: 109-116.

    PubMed  Google Scholar 

  25. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, Curtin LR, Roche AF, Johnson CL: CDC growth charts for the United States: methods and development. Vital Health Stat. 2002, 11: 1-190.

    Google Scholar 

  26. Cheesbrough M: District Laboratory Practice in Tropical Countries Part I. 2006, Cambrige University Press, New York, 2

    Book  Google Scholar 

  27. Iron Deficiency Anaemia: As -sessment, Prevention and Control. A Guide for Programme Managers. 2001, WHO, Geneva, Switzerland

  28. Hashemi MR, Rahnavardi M, Bikdeli B, Zahedani MD: H. pylori infection among 1000 southern Iranian dyspeptic Patients. World J Gastroenterol. 2006, 12: 5479-5482.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Mustapha S, Pindiga U, Yusuph H, Goni B, Jibrin Y: Helicobacter pylori infection among dyspeptic patients at a tertiary hospital in Northern Nigeria. Int J Infect Dis. 2011, 9: 42-48.

    Google Scholar 

  30. Moges F, Kassu A, Mengistu G, Adugna S, Andualem B, Nishikawa T, Ota F: Seroprevalence of Helicobacter pylori in dyspeptic patients and its relationship with HIV infection, ABO blood groups and life style in a university hospital, Northwest Ethiopia. World J Gastroenterol. 2006, 12: 1957-1961.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Shokrzadeh L, Baghaei K, Yamaoka Y, Shiota S, Mirsattari D, Porhoseingholi A, Zali MR: Prevalence of Helicobacter pylori infection in dyspeptic patients in Iran. Gastroenterol Insights. 2012, 4: 24-27. 10.4081/gi.2012.e8.

    Article  Google Scholar 

  32. Alazmi WM, Siddique I, Alateeqi N, Al-Nakib B: Prevalence of Helicobacter pylori infection among new outpatients with dyspepsia in Kuwait. BMC Gastroenterol. 2010, 10: 1-4. 10.1186/1471-230X-10-14.

    Article  Google Scholar 

  33. Tanih NF, Okeleye BI, Ndip LM, Clarke AM, Naidoo N, Mkwetshana N, Green E, Ndip RN: Helicobacter pylori prevalence in dyspeptic patients in the Eastern Cape province – race and disease status. S Afr Med J. 2010, 100: 734-737.

    Article  CAS  PubMed  Google Scholar 

  34. Hishida A, Matsuo K, Goto Y, Naito M, Wakai K, Tajima K, Hamajima N: Smoking behavior and risk of helicobacter pylori infection, gastric atrophy and gastric cancer in Japanese. Asian Pac J Cancer Prev. 2010, 11: 313-317.

    PubMed  Google Scholar 

  35. Suzuki T, Matsuo K, Ito H, Sawaki A, Hirose K, Wakai K, Sato S, Nakamura T, Yamao K, Ueda R, Tajima K: Smoking increases the treatment failure for helicobacter pylori eradication. Am J Med. 2006, 119: 217-224. 10.1016/j.amjmed.2005.10.003.

    Article  PubMed  Google Scholar 

  36. Cherian S, Forbes D, Sanfilippo F, Cook A, Burgner D: Helicobacter pylori, helminth infections and growth: a cross-sectional study in a high prevalence population. Acta Paediatr. 2009, 95: 860-864. 10.1111/j.1651-2227.2009.01221.x.

    Article  Google Scholar 

  37. Torres J, Perez GP, Ximenez C, Muñoz L, Camorlinga-Ponce M, Ramos F, Gomez A, Muñoz O: The association of intestinal parasitosis and H. Pylori infection in children and adults from a Mexican community with high prevalence of parasitosis. Helicobacter. 2003, 8: 179-185. 10.1046/j.1523-5378.2003.00142.x.

    Article  PubMed  Google Scholar 

  38. Santos IS, Boccio J, Davidsson L, Hernandez-Triana M, Huanca-Sardinas E, Janjetic M, Moya-Camarena SY, Paez-Valery MC, Ruiz-Alvarez V, Valencia ME, Valle NCJ, Vargas-Pinto G, Solano L, Thomas J: Helicobacter pylori is not associated with anaemia in Latin America: results from Argentina, Brazil, Bolivia, Cuba, Mexico and Venezuela. Public Health Nutr. 2009, 12: 1862-1870. 10.1017/S1368980009004789.

    Article  PubMed  Google Scholar 

  39. Shak JR, Sodikoff JB, Speckman RA, Rollin FG, Chery MP, Cole CR, Suchdev PS: Anemia and Helicobacter pylori seroreactivity in a rural Haitian population. Am J Trop Med Hyg. 2011, 85: 913-918. 10.4269/ajtmh.2011.11-0101.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Süoglu OD, Gökçe S, Saglam AT, Sökücü S, Saner G: Association of Helicobacter pylori infection with gastroduodenal disease, epidemiologic factors and iron-deficiency anemia in Turkish children undergoing endoscopy, and impact on growth. Pediatr Int. 2007, 49: 858-863. 10.1111/j.1442-200X.2007.02444.x.

    Article  PubMed  Google Scholar 

  41. Fraser AG, Scragg R, Schaaf D, Metcalf P, Grant CC: Helicobacter pylori infection and iron deficiency in teenage females in New Zealand. N Z Med J. 2010, 123: 38-45.

    PubMed  Google Scholar 

  42. Kermati MR, Siadat Z, Mahmoudi M: The correlation between H pylori infection with serum ferritin concentration and iron deficiency anemia. Int J Hematol Oncol. 2007, 17: 16-20.

    Google Scholar 

Download references

Acknowledgment

We would like to acknowledge all study participants who were volunteers to give samples and respond to questionnaires. Our special thanks go to Butajira hospital administration for their unreserved support during the data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zelalem Addis.

Additional information

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

This work was carried out in collaboration between all authors. Author DK designed the study, wrote the protocol, and wrote the first draft of the manuscript. Author BG commented the protocol and analyze the data. Author AA managed the literature search and involved in data analysis. Author ZA participated in data analysis and prepare the final manuscript for publication. All authors read and approved the final manuscript.

Rights and permissions

Open Access  This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.

The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/.

The Creative Commons Public Domain Dedication waiver (https://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kibru, D., Gelaw, B., Alemu, A. et al. Helicobacter pyloriinfection and its association with anemia among adult dyspeptic patients attending Butajira Hospital, Ethiopia. BMC Infect Dis 14, 656 (2014). https://0-doi-org.brum.beds.ac.uk/10.1186/s12879-014-0656-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://0-doi-org.brum.beds.ac.uk/10.1186/s12879-014-0656-3

Keywords