Daugule I, Zavoronkova J, Santare D. Helicobacter pylori and allergy: Update of research. World J Methodol 2015; 5(4): 203-211 [PMID: 26713280 DOI: 10.5662/wjm.v5.i4.203]
Corresponding Author of This Article
Ilva Daugule, MD PhD, Faculty of Medicine, University of Latvia, Raina bulvaris 19, LV1586 Riga, Latvia. ilva_daugule@hotmail.com
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Methodology
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Minireviews
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Ilva Daugule, Jelizaveta Zavoronkova, Daiga Santare, Faculty of Medicine, University of Latvia, LV1586 Riga, Latvia
ORCID number: $[AuthorORCIDs]
Author contributions: Daugule I conceived and designed the review, made data analysis and interpretation and wrote the paper; Zavoronkova J made data acquisition and classification; Santare D drafted the article, and made critical revisions.
Conflict-of-interest statement: There is no conflict of interest.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Ilva Daugule, MD PhD, Faculty of Medicine, University of Latvia, Raina bulvaris 19, LV1586 Riga, Latvia. ilva_daugule@hotmail.com
Telephone: +371-26-320374 Fax: +371-67-034369
Received: May 11, 2015 Peer-review started: May 12, 2015 First decision: June 18, 2015 Revised: September 18, 2015 Accepted: October 16, 2015 Article in press: October 19, 2015 Published online: December 26, 2015 Processing time: 223 Days and 18.1 Hours
Abstract
Recently a lot of literature has been published about the possible preventive action of Helicobacter pylori (H. pylori) against allergy. The present review summarizes research data about the association between H. pylori and allergic diseases, as well as discusses possible hypotheses about the preventive action of H. pylori against atopy. There is evidence from observational studies to support a weak inverse association between prevalence of H. pylori infection and allergy. However, confounders like some unidentified socioeconomic factors, antibiotic use and others could bias the association. Although data from cohort studies point to a possible association of H. pylori with some of the allergic diseases, no definite proof for causal relationship has been clearly demonstrated yet. A biological mechanism proposed to explain the preventive action of H. pylori to allergy is reduced exposure to a major stimulus for the generation of Treg cells in individuals without H. pylori infection. In addition, H. pylori could be an indicator for changes in gut microbiome, reflecting the complex interaction between microbes and immune system.
Core tip: Review summarizes research data about the association between Helicobacter pylori (H. pylori) and allergic diseases. Results from observational studies support a weak inverse association between prevalence of H. pylori and allergy. However, different confounders like unidentified socioeconomic factors, antibiotic use and others could bias the observed association. Further, no definite proof for causal relationship has been clearly demonstrated yet, although data from cohort studies point to a possible association of H. pylori with some of the allergic diseases. Finally, microbiological studies show that H. pylori could be an indicator for changes in gut microbiome during recent decades, reflecting the complex interaction between microbes and immune system.
Citation: Daugule I, Zavoronkova J, Santare D. Helicobacter pylori and allergy: Update of research. World J Methodol 2015; 5(4): 203-211
Although Helicobacter pylori (H. pylori) infection is supposed to be associated with gastric and duodenal ulcer, gastric adenocarcinoma, MALT lymphoma and even recognized as grade-1 carcinogen[1-4], only minority of infected patients will develop a serious disease. Moreover, some researchers even suggest possible preventive effect of H. pylori against several diseases like gastro-esophageal reflux disease and Barret’s adenocarcinoma, obesity, autoimmune diseases, allergy and others[5,6].
The latest Maastricht consensus states that the evidence available shows no definite causative protective effect of H. pylori against asthma and atopy nor that its eradication causes or worsens them and further research is needed[7]. Thus, new data appear constantly about the possible role of bacterium in the development of allergic diseases. The present review summarizes research data about the association between H. pylori and allergic diseases.
EVIDENCE FOR OPPOSITE PREVALENCE TREND BETWEEN H. PYLORI AND ALLERGIC DISEASES
The idea about a possible protective role of H. pylori against allergy has arisen observing opposite prevalence trends between H. pylori and allergic diseases, showing that the prevalence of H. pylori in industrialized countries is decreasing while the prevalence of asthma and other allergic diseases is increasing[6].
Ironically, the first case-control studies showed a positive association between H. pylori infection and allergy. For example, in 1998 a study from Italy identified higher prevalence of H. pylori IgG antibodies among allergic patients compared to patients with inflammatory bowel disease[8]. Further, Figura et al[9] identified higher prevalence of anti-CagA antibodies in H. pylori infected persons with food allergy compared to controls (62.5% vs 28.0%, respectively; P = 0.03). In addition, the mean IgE level to the most common alimentary antigens was increased in CagA-positive individuals compared to CagA-negative patients. This made the authors suggest that mucosal and inflammatory lesions found in individuals infected with CagA-positive H. pylori strains could increase the epithelial permeability and promote the passage of allergens, which, in atopic persons, could directly stimulate an IgE response.
Higher prevalence of H. pylori among patients with allergic diseases observed in some studies raised question about the role of inflammation (observed in the presence of H. pylori infection) in the development of allergy. A positive association between H. pylori and allergic diseases is still being discussed in respect to urticaria. Moreover, International guidelines in Urticaria state that in some cases of chronic spontaneous urticaria eradication of infections, such as H. pylori, bowel parasites and bacterial infections of the nasopharynx, have shown to provide a benefit in the management of the disease[10].
One of the first well designed and controlled studies showing opposite prevalence trends between H. pylori and atopy comes from Finland, demonstrating 3.5-fold increase of total and allergen-specific IgE antibody level in random population from 1973 to 1994 (OR = 5.12, 95%CI: 2.32-11.3)[11]. However, increase of IgE was observed mainly in the subgroup with no H. pylori antibodies, thus raising the hypothesis that H. pylori could influence the development of atopic diseases[11].
A huge study from United States based on database containing information about asthma and H. pylori status in 7663 subjects showed an inverse association between cag-positive H. pylori strain and asthma (OR = 0.79, 95%CI: 0.63-0.99), with a stronger association in younger individuals[12]. An inverse association was found also with other allergic disorders (allergic rhinitis and sensitization to different allergens). Further, the authors tested the association in children up till 20 years of age (n = 7412) and again found inverse association with wheezing, allergic rhinitis and eczema[13].
Up to now many cross-sectional and case-control studies have been performed, thus, showing controversial results. Results are summarized in Tables 1 and 2.
Table 1 Association between Helicobacter pylori and allergy in cross-sectional studies.
Basing on the published studies, several meta-analyses have tested the association. Although in 2012 Wang et al[14] demonstrated no association between asthma and H. pylori infection, analyzing five studies with 770 cases and 785 controls (OR = 1.1, 95%CI: 0.82-1.24), another meta-analysis by the same authors showed pooled OR of all included studies (nine cross-sectional, seven case-control and three cohort studies) for asthma and H. pylori to be 0.81 (95%CI: 0.72-0.91); while pooled OR for asthma and H. pylori infection in cross-sectional studies was 0.84 (95%CI: 0.74-0.96), in case-control studies - 0.94 (95%CI:79-1.12)[15].
Similarly, Zhou et al[16] analyzing 14 studies with 28283 persons demonstrated a weak inverse association between H. pylori and asthma 0.84 (95%CI: 0.73-0.96). Taye et al[17] have performed meta-analysis of 16 studies (n = 21348) about the association of atopy with H. pylori. The authors found an inverse association with atopy (OR = 0.82, 95%CI: 0.73-0.91) as well as with increased level of specific IgE (OR = 0.75, 95%CI: 0.62-0.92).
Detailed overview about case-control and cross-sectional studies, as well as meta-analysis of studies, has been recently published by Lionetti et al[18]. The authors concluded that pooled results of case-control studies showed a significant inverse association of H. pylori infection with atopy/allergic disease (or with atopy, but not with allergic disease), while pooled results of cross-sectional studies showed only a significant association between allergic disease and H. pylori infection.
However, the analysis and comparison of studies is complicated and should be evaluated with caution due to differences among study designs. The authors of the meta-analysis argue that different diagnostic criteria for allergic disease and atopy are used - in some studies asthma was diagnosed by physician tests or by symptoms, while in others the authors evaluated self-reported disease or used only laboratory tests[18]. Further, difference between detection of active infection by urea breath test or stool antigen test and detection of H. pylori antibodies should be noted. In addition, the age of study population should also be taken into account since the time between H. pylori colonization and allergen sensitization is difficult to evaluate, therefore H. pylori negative adult patient could have been colonized since childhood and vice versa[18].
Therefore we could conclude, that, although evidence from observational studies show an inverse association between allergic disease and H. pylori, the association is weak and not consistent.
IS H. PYLORI TRULY INDEPENDENTLY INVERSELY ASSOCIATED WITH ALLERGIC DISEASE?
The idea about the inverse association of H. pylori with allergic diseases has been strongly criticized arguing, that H. pylori could be merely a marker of socio-economic status, known to be also associated with allergic disease[19].
Although Blaser et al[6] report, that the inverse association between H. pylori and asthma was observed independent of socioeconomic status, age, gender, ethnic background, smoking status, and hepatitis A infection, several studies indirectly suggest that other factors could influence the opposite prevalence trends and could play a role in the development of allergy.
For example, Jarvis et al[20] showed no association between presence of H. pylori antibodies and night cough, hay fever, wheezing within last 12 mo as well as sensitization to five allergens, after adjusting the patient sample for age, gender, area, number of siblings, social class. In addition, the authors observed a marked negative association of both hepatitis A and H. pylori with family size only in seropositive individuals (but not in those who were seronegative). This made authors suggest that those without either infection are likely to have grown up in hygienic environments, possibly less overcrowded and with a better diet.
Similarly, a well-designed cross sectional study from United Kingdom (also controlled for social class) could identify only lower lung function in individuals with H. pylori seropositivity. However, after adjustment for either height or social class the size of the association was reduced. No association was observed with wheezing, chronic bronchitis, self-reported asthma, atopy or bronchial hyper-reactivity[21].
No association with a group of infections was observed among Roma children living in poor hygienic conditions compared to non-Roma children in Greece[22]. Although Roma children were found significantly more often seropositive for Toxoplasma gondii, hepatitis A, H. pylori, herpes simplex virus-1 (HSV-1), cytomegalovirus and Hepatitis B, no statistically significant differences were found between Roma and non-Roma children in respect to atopy or specific IgE level. Despite the higher numbers of exposure to infectious agents among Roma children, no protective effect for allergic disease development was evident. Even more, a positive association of the cumulative index of exposure to infections with atopy was found in the non-Roma children (OR = 1.38, 95%CI: 1.08-1.75) and in the total population (OR = 1.42, 95%CI: 1.11-1.83).
An interesting study on schoolchildren with similar genetic background but different socioeconomic environment (Finland and Russian Karelia) showed higher prevalence of allergen-specific IgE in Finnish children, while in Russian children higher prevalence of antibodies to coxsackivirus B4, H. pylori, Toxoplasma gondi and hepatitis A was detected. However, an inverse association between infections and prevalence of atopy was observed only in Russian Karelian children and the biggest effect was observed for enterovirus. However, the authors also hypothised that some other factors could be associated with infections in Russian but not in Finnish populations are responsible for the effect[23].
Finally, in Malaysia low H. pylori prevalence goes together with low prevalence of wheezing among 6-7 and 13-14 years old children (5.4% and 5.7%, respectively)[24], therefore scientists have concluded that H. pylori is only a marker for poor hygiene[25]. Although no study has been performed yet comparing the prevalence of H. pylori among patients with and without asthma in Malaysia, Raj et al[26] consider that available data speak against the unique role for H. pylori infection as a protective factor against asthma.
To summarize, there is evidence that H. pylori could not be independently inversely associated with allergic disease, but just reflect changes in environment and/or diet. The inverse association between prevalence of H. pylori infection and allergic diseases observed in studies could also be biased by some other uncontrolled factors.
POSSIBLE CAUSAL RELATIONSHIP BETWEEN H. PYLORI AND ALLERGIC DISEASE
Although a weak inverse association between H. pylori and allergy can be recognized, scientists argue that opposite prevalence, possibly evident from observational studies, does not mean a causal relationship[19]. However, demonstration of a possible causal relationship between H. pylori and allergy is extremely complicated.
A biological mechanism proposed to explain the preventive association of H. pylori to allergy is reduced exposure to a major stimulus for the generation of Treg cells in individuals without H. pylori infection[27]. One of the latest ideas involves neutrophil-activating protein of H. pylori that could inhibit Th2-mediated bronchial inflammation in patients with allergic asthma[5]. Possible immunomodulatory properties of H. pylori are well described by Arnold et al[28].
Fulfilment of Bradford Hill criteria
Blaser et al[6] used Bradford Hill criteria to support the evidence about the inverse association between H. pylori and asthma. Hill’s criteria consist of several conditions fulfillment of which can provide evidence of a causal relationship between an incidence (H. pylori prevalence) and a possible consequence (asthma)[29].
To prove the causal link Blaser et al[6] mentioned the small but consistent trend demonstrated in several studies as well as the fact, that inverse causation is not likely and the decline is preceding the increase in asthma. However, although there is a weak trend showing inverse association between allergy and H. pylori, not all studies approve it. Further, Blaser et al[6] considered that the inverse association observed with early life asthma (not with long-standing asthma seen in adults) supported the role of H. pylori, since the effect of H. pylori might be less important in adult-onset asthma due to much more heterogeneous nature of adult asthma. However, confounding factors that could influence the association are not fully ruled out.
Further, one of the Bradford criteria states that there is no other likely explanation of disease - the more specific an association between a factor and an effect is, the bigger the probability of a causal relationship. However, at present allergologists consider asthma as a multifactorial disease associated with several other risk factors (like urban outdoor and indoor pollution, allergens, etc.) rather than H. pylori infection[30]. Therefore the fulfillment of Bradford Hill’s criteria, demonstrated by Blaser et al[6], should be interpreted with caution and should be considered only as one of the arguments for protection of H. pylori against asthma.
Data from cohort studies
Since it is impossible to perform interventional studies to test the link between H. pylori and allergy, some knowledge about a possible causal association could be driven from cohort studies. However, it should be noted that such studies are not conclusive and they give only a better insight about a possible causality.
Holster et al[31] detected the presence of H. pylori antibodies in 7-9 years old children who were followed from birth and assessed by yearly questionnaires about allergic symptoms and possible risk factors. The authors observed no association between H. pylori and atopic dermatitis, allergic rhinitis and asthma. A borderline association was found only between H. pylori and wheezing. However, the authors admit, that they were not able to detect if H. pylori infection preceded the diagnosis of allergic disease, since presence of H. pylori infection was diagnosed only at the age of 7-9 years.
Further, a cohort study in Ethiopia followed children since birth, detecting presence of allergic symptoms with questionnaires and performing allergic skin tests and H. pylori stool antigen tests at the age of one, there and five years. The sample was controlled for potential confounders. After three year follow-up the authors found only a borderline association with eczema[32]. Further, following the same cohort for five years an inverse association was observed only with eczema[33]. No association was observed with asthma or other allergic disease. Interestingly, that in the same cohort the association between paracetamolum therapy and allergic symptoms was analyzed separately and an inverse association was observed between use of paracetamolum and wheezing and eczema[34].
Development of allergy after H. pylori eradication
Several studies demonstrated development of an allergic disease or increase of IgE after H. pylori eradication. Korean study demonstrated increased levels of IgE related, non IgE related allergy as well as subclinical raise of IgE levels in patients after H. pylori eradication compared to H. pylori positive patients without eradication and H. pylori negative controls[35]. However, this could also be related to the change in gastric acidity due to treatment with proton pump inhibitors, used together with eradication therapy. In addition, some patients continue use of acid lowering drugs even after eradication therapy.
Data from animal studies
Finally, a possible causal relationship can be demonstrated in animal models. One of the first studies showing causal relationship was the study by Arnold et al[36], showing that animals infected with H. pylori infection had lower airway hyper-responsiveness, tissue inflammation, and goblet cell metaplasia. Further studies supported the finding that H. pylori infection could protect mice from development of allergic asthma[37]. However, effect observed in animal models quite often is not observed also in humans.
H. PYLORI AS A PART OF COMPLEX INTERACTION BETWEEN MICROBES AND HUMAN IMMUNE SYSTEM
H. pylori and other infectious agents
Blaser et al[6] speculate, that H. pylori could be merely a marker for other phenomena, for example, early life antibiotic use could eliminate H. pylori as well as other microbes that actually could be the protective agents. Therefore, the question arises if H. pylori per se plays the crucial role in the development of allergy or it is just a marker of frequent infections or other factors, since several other microbes have been shown to be inversely associated with allergic disease[38].
This could be indirectly supported by study, showing that seropositivity to H. pylori and Hepatitis A was unrelated to atopic status, while multivariate analysis showed that both the effect of having two or more younger siblings (OR = 0.1, 95%CI: 0.03-0.8) and of acquiring measles up to the age of three (OR = 0.2, CI: 0.03-0.8) were significantly related to a lower risk of asthma[39]. The finding indicates that frequent infections observed more often in families with siblings are more important than H. pylori infection per se. Further, Janson et al[40] demonstrated that combination of different infectious agents [hepatitis A, H. pylori, Toxoplasmosis gondii, HSV, Chlamydia pneumoniae, Ebstein Barr virus (EBV) and cytomegalovirus] was an independent risk factor for atopy (OR = 1.43, 95%CI: 1.06-1.93), allergic asthma (OR = 1.82, 95%CI: 1.12-2.98), and allergic rhinitis (OR = 1.69, 95%CI: 1.21-2.37).
Importance of several pathogens (Ascaris lumbricoides, T. gondii, HSV and EBV) for prevention of atopy has been shown in a study by Alcantara-Neves et al[41]: Children with three or fewer infection markers had a higher prevalence of specific IgE and skin prick test reactivity compared with those with four or more infection markers. On the contrary, isolated infections were not associated with the prevalence of atopic or non-atopic wheeze.
Therefore, evidence from studies suggests that H. pylori could be just a part of complex interaction between immune system and pathogens, as proposed by Janson et al[40].
H. pylori as a part of gut microbiome
This goes together with the idea that the increase in allergic diseases could be caused by changes in the composition of gut microflora due to global changes of environmental, socioeconomic and life style factors[27]. Data exist, showing lower diversity of microflora in allergic patients compared to healthy controls: A study in Sweden reports a lower diversity of the total microbiota at one month in infants with IgE-associated eczema[42].
Although previously H. pylori was considered as the major inhabitant of stomach, at present up-to-date sequence based molecular methods have allowed identifying gastric microbiota more precisely. von Rosenvinge et al[43] have shown that such phyla as Firmicutes, Bacteroidetes, Actinobacteria, Proteobacteria and Fusobacteria dominate in gastric fluid samples. In a review Engstrand et al[44] have also summarized that gastric micro-biota contains a large variety of genera including Staphylococcus, Streptococcus, Pervotella, Lactobacillus and some others, therefore H. pylori could be considered only a part of a complex microbial flora in the stomach.
Further, Rosenvinge has identified that treatment with proton pump inhibitors promotes bacterial overgrowth, while antibacterial treatment is associated with reduced bacterial diversity[43]. Decreased microbiota diversity in patients after H. pylori eradication therapy has been identified also by Jakobsson et al[45]. Therefore, one can conclude, that after H. pylori eradication the diversity of gastric microflora decreases that could possibly be associated with development of allergy.
Therefore we could hypothise that loss of H. pylori results in a small (possibly significant) reduction of stimulation of immune system, as proposed by other authors[44]. Importance of other microorganisms should also be considered in the complex interaction between the human immune system and microbes. However, how H. pylori specifically and the entire human microbial ecosystem affect human health is still questionable.
CONCLUSION
Evidence from observational studies supports a weak inverse association between prevalence of H. pylori infection and allergy. However, it could be biased by confounders like socioeconomic factors, antibiotic use and others. No definite proof for causal relationship has been clearly demonstrated yet, although data from cohort studies point to a possible association of H. pylori with some allergic diseases. In addition, H. pylori could be an indicator for changes in gut microbiome during recent decades, reflecting the complex interaction between microbes and immune system.
Summarizing the data, it seems that H. pylori infection alone cannot prevent development of allergy in all infected individuals, similarly like bacterium is not causing a serious gastrointestinal disease in all infected patients. In both conditions genetic and environmental factors (diet, other microbes, microflora, etc.) are of importance next to the recognized role of the bacterium.
Nevertheless, the intensive research in H. pylori field has brought a new insight into the interaction between microbes and immune system and the microbial - host relationship, supporting the idea that microbes could play a role in the development of allergy.
Footnotes
P- Reviewer: Allen M, Bernhardt GA, Lee YY S- Editor: Tian YL L- Editor: A E- Editor: Lu YJ
Schistosomes , liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994.IARC Monogr Eval Carcinog Risks Hum. 1994;61:1-241.
[PubMed] [DOI][Cited in This Article: ]
Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T. Management of Helicobacter pylori infection--the Maastricht IV/ Florence Consensus Report.Gut. 2012;61:646-664.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 1541][Cited by in F6Publishing: 1503][Article Influence: 125.3][Reference Citation Analysis (4)]
Corrado G, Luzzi I, Lucarelli S, Frediani T, Pacchiarotti C, Cavaliere M, Rea P, Cardi E. Positive association between Helicobacter pylori infection and food allergy in children.Scand J Gastroenterol. 1998;33:1135-1139.
[PubMed] [DOI][Cited in This Article: ]
Figura N, Perrone A, Gennari C, Orlandini G, Giannace R, Lenzi C, Vagliasindi M, Bianciardi L, Rottoli P. CagA-positive Helicobacter pylori infection may increase the risk of food allergy development.J Physiol Pharmacol. 1999;50:827-831.
[PubMed] [DOI][Cited in This Article: ]
Kosunen TU, Höök-Nikanne J, Salomaa A, Sarna S, Aromaa A, Haahtela T. Increase of allergen-specific immunoglobulin E antibodies from 1973 to 1994 in a Finnish population and a possible relationship to Helicobacter pylori infections.Clin Exp Allergy. 2002;32:373-378.
[PubMed] [DOI][Cited in This Article: ]
Raj SM, Choo KE, Noorizan AM, Lee YY, Graham DY. Evidence against Helicobacter pylori being related to childhood asthma.J Infect Dis. 2009;199:914-915; author reply 915-916.
[PubMed] [DOI][Cited in This Article: ]
Amberbir A, Medhin G, Erku W, Alem A, Simms R, Robinson K, Fogarty A, Britton J, Venn A, Davey G. Effects of Helicobacter pylori, geohelminth infection and selected commensal bacteria on the risk of allergic disease and sensitization in 3-year-old Ethiopian children.Clin Exp Allergy. 2011;41:1422-1430.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 73][Cited by in F6Publishing: 81][Article Influence: 6.2][Reference Citation Analysis (0)]
Amberbir A, Medhin G, Abegaz WE, Hanlon C, Robinson K, Fogarty A, Britton J, Venn A, Davey G. Exposure to Helicobacter pylori infection in early childhood and the risk of allergic disease and atopic sensitization: a longitudinal birth cohort study.Clin Exp Allergy. 2014;44:563-571.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 31][Cited by in F6Publishing: 39][Article Influence: 3.9][Reference Citation Analysis (0)]
Engler DB, Reuter S, van Wijck Y, Urban S, Kyburz A, Maxeiner J, Martin H, Yogev N, Waisman A, Gerhard M. Effective treatment of allergic airway inflammation with Helicobacter pylori immunomodulators requires BATF3-dependent dendritic cells and IL-10.Proc Natl Acad Sci USA. 2014;111:11810-11815.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 82][Cited by in F6Publishing: 93][Article Influence: 9.3][Reference Citation Analysis (0)]
Uter W, Stock C, Pfahlberg A, Guillén-Grima F, Aguinaga-Ontoso I, Brun-Sandiumenge C, Krämer A. Association between infections and signs and symptoms of ‘atopic’ hypersensitivity--results of a cross-sectional survey among first-year university students in Germany and Spain.Allergy. 2003;58:580-584.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 29][Cited by in F6Publishing: 32][Article Influence: 1.5][Reference Citation Analysis (0)]
Karimi A, Fakhimi-Derakhshan K, Imanzadeh F, Rezaei M, Cavoshzadeh Z, Maham S. Helicobacter pylori infection and pediatric asthma.Iran J Microbiol. 2013;5:132-135.
[PubMed] [DOI][Cited in This Article: ]
Konturek PC, Rienecker H, Hahn EG, Raithel M. Helicobacter pylori as a protective factor against food allergy.Med Sci Monit. 2008;14:CR452-CR458.
[PubMed] [DOI][Cited in This Article: ]
Jaber SM. Helicobacter pylori seropositivity in children with chronic disease in Jeddah, Saudi Arabia.Saudi J Gastroenterol. 2006;12:21-26.
[PubMed] [DOI][Cited in This Article: ]
Bartuzi Z, Korenkiewicz J, Romański B. Correlation between Helicobacter pylori infection and food allergy in chronic gastritis.Med Sci Monit. 2000;6:530-538.
[PubMed] [DOI][Cited in This Article: ]
Matricardi PM, Rosmini F, Riondino S, Fortini M, Ferrigno L, Rapicetta M, Bonini S. Exposure to foodborne and orofecal microbes versus airborne viruses in relation to atopy and allergic asthma: epidemiological study.BMJ. 2000;320:412-417.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 466][Cited by in F6Publishing: 501][Article Influence: 20.9][Reference Citation Analysis (0)]
