Helicobacter pylori infects more than 50% of the world population and is acquired in infancy. Higher prevalence is found in developing countries, and within geographic areas the predominance correlates inversely with socioeconomic status, especially with living conditions during childhood. Initially, in adults, H. pylori was only associated with gastric diseases, such as peptic ulcer, gastritis, gastric adenocarcinoma, and gastric mucosa-associated lymphoid tissue (MALT) lymphoma, and in childhood, with chronic gastritis and duodenal ulcers in children. Recently, H. pylori has been related to non-gastric diseases, including hematological disorders such as iron deficiency anemia (IDA), chronic idiopathic thrombocytopenia (cITP), and vitamin B12 deficiency. H. pylori can trigger autoimmune atrophic gastritis and be responsible initially for an oral iron refractory anemia. Other hematological associations have been made, such as an increased risk of childhood leukemia in children of H. pylori-infected mothers and gastric bleeding in children with coagulation pathologies. H. pylori infection is important in the immune pathogenesis of chronic gastric inflammation and hematological diseases. The diagnostic methodology is based on non-invasive (serology, C-urea breath test, stool HP antigen) and invasive tests. The scientific community discussed and incorporated in international consensus for the investigation and management of these hematological extragastric pathologies (IDA, cITP, vitamin B12 deficiency, and MALT lymphoma). In children, a similar attitude was obtained in all of these pathologies except for cITP, in which the investigation for H. pylori is not indicated.
- Helicobacter pylori
- iron deficiency anemia
- immune thrombocytopenia
- MALT lymphoma
- vitamin B12 deficiency
After the discovery made by Marshall and Warren, histological features of chronic gastritis in upper gastrointestinal endoscopy were revealed. Moreover, a Canadian group also found
Although over 80% of infected subjects remain asymptomatic,
2. The interaction between
H. pylori and the immune system
Epithelial and myeloid cells form the initial line of the innate immune system response against
MyD88 (myeloid differentiation primary response protein 88) is an intracellular adaptor protein used by all TLRs except TLR3, and the signaling is done in two forms: MyD88 dependent, responsible for pro-inflammatory cytokine production as well as MyD88 independent, responsible for interferon type 1 production (ITF1). TLR4 inducts both dependent and independent MyD88, so it inducts both cytokines and ITF1. The expression of MyD88 in macrophage cells is essential for the induction of anti-inflammatory cytokines (IL-6, IL-1B, IL-10, and IL-12) . Recently, a new group of innate immune molecules, including activating receptors involved in modulating the intensity of innate immune response in myeloid cells (TREM), has been described [24, 25]. TREM family receptors (TREM-1 to TREM 4), are cell surface activating receptors with a transmembrane region containing charged lysine residues and a short cytoplasmatic tail lacking signaling motifs. TREM-1, a 30-Kda glycoprotein of the Ig family is the most well-known member of the TREM family and is responsible for inflammation amplification and activation of antigen-presenting cells (APC). TREM-1 is exhibited in neutrophils and monocytes and linked to innate immunity by phagocyte secretion of pro-inflammatory chemokines and cytokines such as IL-8 and TNF-α. TREM-1 is involved in the amplification of TLR-dependent signals and in the improvement of NOD-like receptors (NLRs)–mediated responses, including NOD-1, involved in the protection against
3. Epidemiology and risk factors
More than 50% of the world’s population is infected with
3.1. Routes of transmission
A number of studies propose environmental sources, such as animal and water exposure, as potential forms of
3.1.1. Animals as potential source of H. pylori
Two epidemiological studies reported that the exposure to sheep was implicated in
3.1.2. Water transmission
3.1.3. Fecal-oral transmission
Some studies support the evidence of the transmission of
3.1.4. Oral-oral transmission
It is accepted that
4. Pathogenesis of
H. pylori infection in extradigestive pathologies
It is known that the immunological response triggered by the bacteria is responsible for gastric mucosa damage. Large amounts of pro-inflammatory substances, such as cytokines, eicosanoids, and acute phase proteins, are released after
4.1. Pathogenesis of
H. pylori in extradigestive disorders
The role of
Gastric MALT lymphoma, also known as mucosa-associated lymphoid tissue (lymphoma), is a low grade B-cell lymphoma described by Isaac and Wright in 1993 as an adult disease and extremely rare in children.
The Scientific community has discussed and incorporated international consensus guidelines for investigation and management of these hematological extragastric pathologies (IDA, cITP, vitamin B12 deficiency, and MALT lymphoma) [5, 49-51]. No international consensus was obtained for other hematological changes. However, autoimmune neutropenia was documented in 2002 by Gupta et al.  with the report of a patient with a neutropenia (400/μl), which normalized after
According to literature, other hematologic problems may be associated to
5. Iron deficiency anemia
The World Health Organization (WHO) estimates that approximately 50% of all anemic patients have a diagnosis of IDA [1, 30, 31, 50, 51, 54]. In infancy, IDA is associated to abnormal mental and motor development. In developed countries, low intake, increased host requirements to supply the physiological needs for normal development, dietary errors, and blood loss are the most frequent causes of IDA in children [15, 45]. The evidence to support a causal association between
5.1. Pathophysiology of iron deficiency by
The intrinsic biological mechanisms by which
5.1.1. Occult blood loss
Chronic gastrointestinal blood loss is one of the supposed intrinsic mechanisms. However, most case series of
5.1.2. Changes in gastric physiology: gastric inflammation and chronic disease anemia
Gastric mucosal inflammation is an invariable finding in
188.8.131.52. Directed mucosal injury
Two instances should be considered in the invasion of
184.108.40.206. Adherence of bacteria to the gastric mucosal
After the initial colonization,
220.127.116.11. Toxic effect
Several enzymes produced by
5.1.3. Recruitment of inflammatory chemokines and inflammatory cells
Iron absorption takes place in the small intestine in accordance with the metabolic demands that reflect the amount of iron stored for erythropoiesis. Haem iron refers to the pool of iron incorporated in the protoporfirin ring. Its absorption is more effective than non-haem iron and the mechanisms for absorption are different. HCP 1 (haem carrier protein) is a protein capable of the transmembrane transport of haem into the lumen of enterocytes to be catabolized by the microsomal enzyme haem oxygenase. The non-haem iron (Fe3+) is not soluble and is the most prevalent alimentary iron. Its absorption is dependent on endogenous factors related to its reduction to a soluble iron form (Fe2+), such as duodenal cytochrome
5.1.5. Low ascorbic acid level
Vitamin C is an acidic molecule with strong reducing activity. Ascorbic acid (AA) is the reduced form of vitamin C. It is a potent antioxidant, a protector against gastric carcinogenesis, neutralizing nitrite-derived mutagens. Vitamin C is essentially absorbed and secreted in the antral mucosa. It has two major redox forms: AA and dehydroascorbic acid (DHA), the reduced and oxidized forms, respectively, and interconvertible. Within the cell, DHA is rapidly converted to AA by the specific enzyme systems, such as DHA reductase, glutaredoxins, and protein disulfide isomerase, in the presence of glutathione or other thiols as electron donors [76, 77]. Unlike AA, DHA is relatively unstable and undergoes rapid, spontaneous, and irreversible hydrolysis particularly at pH>4. Annibale et al.  demonstrated that gastric juice and ascorbate content are negatively affected by
5.1.6. Utilization/sequestering iron by
6. Idiopathic thrombocytopenia purpura (ITP)
Immune thrombocytopenic purpura (ITP) is an autoimmune hemorrhagic disease, characterized by isolated thrombocytopenia, which affects nearly 1:25000 children per year [85-87]. ITP can present itself as an acute, self-limiting condition or a chronic process. Persistent thrombocytopenia, for longer than 6 months, may be present in about 20% of children [88-91]. A controversial issue in children is the designation “Chronic immune thrombocytopenia (cITP),” because about a third of children with ITP spontaneously cure from 6 months to 1 year later [87-89]. The International Childhood ITP Study Group recommends that 12 months must be the cutoff point for defining cITP [88, 90]. ITP is characterized by a premature destruction of platelets. Autoantibodies interact with the glycoprotein membrane on surface platelets (GIIb/IIIa or GIb), resulting in accelerated platelet destruction and clearance by mononuclear phagocytes [86, 91-93]. Increased megakaryocyte number in bone marrow is the marker of ITP in childhood . However, studies performed in 1980 revealed that in two thirds of adults the expected increase of megakaryocyte production was not observed. Most of ITP had normal or depressed platelets turnover . Chang et al. evaluated the effect of plasma, from childhood patients with ITP (44 with an acute form and 9 with chronic ITP), on induced thromboietin production of megakaryocytes in liquid culture. They reported that plasma from pediatric patients with ITP suppressed in vitro megakaryocyte production. They cultured cord blood cells as a source of CD34+ cells, which is a thrombopoietic growth factor, and plasma from control subjects or, children with ITP. After 8 days of culture, nearly 16% of cells were megakaryocytes. The effect of plasma in three groups was compared: control plasma, antibody ITP plasma (anti-GPIb, anti-GPIIIa, or both). They observed that in cultures with anti-GPIb antibodies the number of megakaryocytes were strongly reduced but this did not occur in ITP plasma negative antibody or in ITP plasma with only anti-GPIIb-IIIa antibody [93, 94]. Recently, thrombocyte kinetic studies have been carried out and autoantibodies affecting the megakaryocytes production in the bone marrow were observed [87, 91, 93, 95]. Also, studies using electronic microscopy showed 50–75% of ITP megakaryocytes damaged and in some cases attached by monocytes . In most cases, ITP in childhood is triggered by a previous viral disease or a vaccination [87, 90]. HIV, hepatitis C, measles, cytomegalovirus, varicella, pertussis, and parvovirus can all be found in this context [95, 97]. After a benign viral infection, a predominant proinflammatory state may trigger ITP. Both proinflammatory cytokines and T-cells persist, creating a permissive environment for the emergence of autoantibodies that bind to platelet membrane antigens [91, 93]. Zehnder et al. highlighted an increased expression of gamma interferon-dependent genes in early states of ITP, supporting a proinflammatory or TH1 profile [91, 95]. ITP affects both adults and children. However, the natural course of ITP in children is different from adults. Spontaneous recovery occurs in one third of the pediatric patients, months or years after the diagnosis. Several studies in adults reported improvement in platelet counts after
Several mechanisms by which
6.1. Possible mechanisms by which
H. pylori may be related to ITP
6.1.1. Molecular mimicry
One theory is that cross-reactive antibodies produce reactions with
6.1.2. Binding between
H. pylori to von Willebrand factor/induction of platelet aggregation and apoptosis
Many diseases associated to platelet aggregation have been described as related to
6.1.3. Modulation in the monocyte/macrophage function
Change in the balance of the Fcγ receptor, related to the activation of monocytes, leads to increased monocyte function with phagocytosis and autoreactivity of B and T lymphocytes .
6.1.4. Non-specific activation of immune system
The major antigenic component for antibody production against
6.2. Genetic characteristics of the patients
Recently, the role of genetic factors has emerged, indicating that
Based on the previously mentioned studies and mechanisms described, which lead to ITP in
7. MALT lymphoma
For the first time, in 1983, Isaacson and Wright introduced the concept of mucosa-associated lymphoid tissue (MALT), a marginal, extranodal, indolent B-cell non-Hodgkin lymphoma [105, 106]. Predominantly found in females over the age of 50, it is quite rare in childhood. In prospective, multicenter NHL-BFM treatment studies performed since 1986, composed of 2703 children, only in 4 (0.1%) MALT lymphoma was found.
7.1. Pathogenesis and
Gastric MALT lymphoma results from a multistage process that begins with the
8. Diagnostic tests for
Published consensus developed guidelines for the management of
Who should be tested? What tests should be used? Testing for
8.1. Invasive tests
Invasive tests require a gastric endoscopy and a biopsy with culture for detecting
8.1.1. Rapid urease test (RUT)
Histology is considered a standard method for detecting
Cultures method has high specificity for the diagnosis of
8.1.4. Polymerase chain reaction
PCR is a DNA amplification that uses the rapid production of a target DNA sequence to identify
8.2. Non-invasive tests
Although the gold standard method for diagnosis is gastric histology and rapid urea test, an important disadvantage is their invasiveness. Non-invasive tests, such as urea breath test (UBT), serology, and more recently, fecal
8.2.1. Urea breath test (UBT)
UBT is one of the preferred tests to diagnose active
8.2.2. Antibody test
8.2.3. Fecal antigen test
The fecal antigen test (FAT) identifies
Note: PPI must be withheld two weeks before performing RUT, UBT, and FAT [49, 51]
The goal of treatment is to obtain 90% eradication. The therapeutic regimens are variable and dependent on local resistance data. Several studies have documented high resistance to clarithromycin and metronidazole . The first treatment commonly administered in children and adults is a triple therapy, for 14 days, that includes a PPI and two antibiotics, amoxicillin and metronidazole or clarithromycin [49-51, 127]. The first line of recommended eradication therapies are as follows: amoxicillin, 50 mg/kg twice a day for 14 days; clarithromycin, 15 mg/kg/twice daily for 14 days; and PPI, 1 mg/kg twice daily for 1 month. Alternatively, amoxicillin, 50 mg/kg twice a day for 14 days; metronidazole, 20 mg/kg twice daily for 14 days; and PPI, 1 mg/kg twice daily for 1 month or clarithromycin, 15 mg/kg/twice daily for 14 days; metronidazole, 20 mg/kg twice daily for 14 days; and PPI, 1 mg/kg twice daily for 1 month . Several studies revealed that the use of probiotics improves the treatment tolerance, but there is no evidence of higher eradication . Koletzko et al.  revealed a rate of resistance to clarithromycin of 20%, and a rate of resistance to metronidazole of 23% after a first treatment [82, 127]. In Portugal, a higher clarithromycin resistance rate was reported in children (44.8%) compared with adults (14.8%) . The main factors for triple therapy failure are the low compliance and the bacteria’s resistance to antibiotics. The risk for clarithromycin resistance is related with the previous consumption of macrolides, which is substantially prescribed in children for respiratory tract diseases. Double resistance strains were found in up to 50% of strains after failure of therapy using both clarithromycin and metronidazole . The failure after the first therapeutic approach is predictive of resistance to other therapeutic approaches [50, 51, 128]. NASPHGAN recommend, in case of failure in the first line of treatment in children, and if possible, to perform culture with testing for antibiotic sensitivity to guide a second-line therapy. Other options may be taken if a
10. Conclusion and possibilities of new studies
Approximately 50% of the world’s population is
11. New studies
Several new antibiotics are under investigation for the treatment of H. pylori in adults. (1) Rifabutin. Triple therapy for 10 days with rifabutin + pantoprazole + amoxicillin is showing good results in resistant H. pylori areas. Resulting in eradication rates of 50% [82, 132]; (2) Nitazoxanide that includes levofloxacin, nitazoxanide, doxycycline, and omeprazole is showing better efficacy than standard triple therapy .
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