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American Journal of Bioscience and
Bioinformatics (AJBB)
Insights into the Pathogenesis, Virulence Factors, and Diagnosis of
Helicobacter pylori
: A
Comprehensive Review
Ali Saad Kadhim
1
, Abdullah Salim Al-Karawi
2*
Volume 2 Issue 1, Year 2023
https://journals.e-palli.com/home/index.php/ajbb
Article Information
ABSTRACT
Received:
Jun 20, 2023
Accepted:
August 11, 2023
Published:
September 06, 2023
The
H. pylori
bacterium, which resides in the human stomach and is linked to a number of
gastrointestinal illnesses, is introduced in-depth in this article. We examine how
H. pylori
establishes infection, thwarts the hosting immune response, and causes inflammation as
we explore the pathophysiology of this bacterium. We also talked about how
H. pylori
influences host cells and develops a favorable environment for survival. We also go over the
many methods for identifying H. pylori, such as endoscopy, biopsy, blood, breath, feces, and
others. We stress the importance of an accurate and speedy diagnosis while outlining the
advantages and disadvantages of each diagnostic strategy to manage disorders caused by
H.
pylori
effectively. Throughout this review, we aim to unravel the mysteries surrounding H.
pylori, providing valuable insights into its pathogenesis, the intricate interplay of virulence
factors, and the diverse diagnostic strategies employed in clinical practice. Enhancing our
understanding of
H. pylori
can pave the way for improved therapies and patient outcomes.
Keywords
Helicobacter pylori, Endoscopy,
PCR, Urea Breath Test,
Serology Test
1
Department of science, Basic Education collage, Wasit University, Wasit, Iraq
2
Department of Biology, College of Science, Mustansiriyah University, Baghdad, Iraq
*
Corresponding author’s e-mail:
Abdullah.S.Shaker@uomustansiriyah.edu.iq
INTRODUCTION
Firstly,
Helicobacter pylori
infection has become more
frequent in recent years, affecting around population
(Keller
et al
., 2021; Tonkic
et al
., 2012). Accurate
H.
pylori
detection is essential for treating symptomatic
people who are infected. Since Marshall and others’
1983 discovery of this spiral-shaped, gram-negative
bacteria, many diagnostic methods have been created
(Kim & Wang, 2021). Some tests base their results on
a variety of bacterial traits, such as their appearance
(histology, culture), immunology (serology, stool test,
immunohistochemistry), genetics (PCR), or enzymatic
activity (13C-urea breath test, quick urease test) (Mišak &
Hojsak, 2021). Generally, these techniques may be divided
between invasive testing (histology, urease test, culture),
which demands endoscopy of the upper gastrointestinal
tract and stomach biopsies, and non-invasive tests
(serology, 13C-urea breath test, stool antigen test). Each
test has advantages, weaknesses, and restrictions that vary
depending on the clinical circumstances and the inquest
(Mišak & Hojsak, 2021).
Description of
H. pylori
Genomic characteristics, plasmid presence, and
strain diversity are all pertinent factors that warrant
consideration. The two sequenced genomes of
Helicobacter
pylori
exhibit a size of more or less 1.9 Mbp and possess a
G+C composition ranging from 31% to 45% (4). Notably,
this bacteria strain 27595 encompasses 1,587 genes, while
strain J99 contains a slightly lower count of 1,491 genes
(Zamani
et al
., 2018). It is deserve noting with various
strains of this bacteria may harbor cryptic plasmids
that lack discernible antibiotic resistance or virulence
genes. Interestingly, certain plasmids are utilized in the
development of
H. pylori
- Escherichia coli shuttlecock
vectors for cloning investigations (Pohl
et al
., 2019). While
the presence of
H. pylori
-infected bacterial virus has been
recognized, there remains a need for comprehensive
characterization in this regard. In contrast to highly clonal
bacterial diseases such as Mycobacterium tuberculosis,
H. pylori
exhibits genetic diversity, indicating a lack of
clonality (Leszczyńska
et al
., 2010). Consequently, each
patient harboring
H. pylori
carries a distinct strain, although
minor variations may exist among relatives. The genetic
variability observed in
H. pylori
may represent an adaptive
response to the gastrointestinal environment of its host
and the unique patterns exhibited (Leszczyńska
et al
.,
2010). Various mechanisms such as DNA rearrangement,
as well as the insertion and deletion of foreign sequences,
are considered to contribute to the genetic heterogeneity
observed in
H. pylori
(Ferwana
et al
., 2015).
Virulence factors of
H. pylori
PAI cag
Although
H. pylori
infection always leads in recurrent
gastritis, the majority of infected patients have absence
further issues and show no evident clinical indicators of
infection (Mezmale
et al
., 2020). This raised the possibility
that certain strains are more virulent than others. Early
studies of
H. pylori
strains’ varied pathogenic qualities
revealed that increasing pathogenicity was associated into
capacity of their in addition aggressive strains to generate
phenotypic alterations, hyalinization, and progressive
degeneration of in vitro-cultured cells. This gene is
present in around 60 to 80% it (Malfertheiner
et al
.,
2017). and is a signal for a genomic PAI of about 40 kb
that estimate between 37 and 51 proteins (Bessède
et al
.,
2017), depending on the strain examined. CagA+ strains
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about
H. pylori
in vitro extension, it has been shown
to contribute to
H. pylori
stomach colonization in mice
significantly (Zamani
et al
., 2018). VacA’s activities include
membrane channel formation, disruption of endosomal
and lysosomal activity, influence on integrin receptor-
induced cell signaling, interference with cytoskeleton-
dependent cell functions, induction of apoptosis, and
immunological control (Fig.2) (Bessède
et al
., 2017;
Nakashima
et al
., 2018).
Acid Resistance
Although
Helicobacter pylori
is not classified as an acidophile,
it possesses a noteworthy capacity to thrive in the stomach’s
acidic environment (Ferwana
et al
., 2015). The pH levels
within the gastrointestinal mucosa are typically believed
to range from 4 to 6.5; however, instances of acid shocks
can occur. Consequently,
H. pylori
necessitate protective
mechanisms against critical acid shocks and the ability to
adapt to pH levels of approximately 5.5. Upon entry,
H.
pylori
is presumed to swiftly migrate towards employing
chemotactic motility to exploit the urea and bicarbonate
gradients in the stomach situation (Nakashima
et al
.,
2018). This quick migration is imperative for
H. pylori
as
its motility is compromised within the acidic milieu of the
stomach lumen (Malfertheiner
et al
., 2017).
Adhesins and Outer Membrane Proteins
Numerous bacterial element influence
H. pylori
’s adhesion
to the gastric epithelium. considering the bacterium’s
restricted horde assortment, the prevalence of adhesins
likely signifies their relevance to the bacteria. However,
evaluating the individual contribution of each adhesin
presents significant challenges (Nakashima
et al
., 2018).
Consequently, our primary focus will be directed toward
investigating the potential significance of the three Hop
proteins, which possess sufficient evidence to elucidate
their role in the pathophysiology of
H. pylori
infection
(Tonkic
et al
., 2018).
Methods of Diagnosis
Invasive Tests
Rapid Urease Test
An affordable, fast, and accurate test for finding
Helicobacter
pylori
is the rapid urease test (RUT). In terms of sensitivity,
it is nonetheless constrained. If the bacterial load in the
biopsy is less than 10
4
, many commercial tests might
produce false-negative findings (Zamani
et al
., 2018).
Additionally, urease-positive bacteria like Staphylococcus
capitis uratolytic have the potential to provide false-
positive findings (Pohl
et al
., 2019). Different commercial
RUTs were evaluated in a German investigation, and it
was discovered that they were all
H. pylori
detection is
both sensitive and specific.
(5)
Amazingly, they were even
more accurate than histology, particularly in individuals
who had recently taken antibiotics or proton pump
inhibitors (PPIs) (Leszczyńska
et al
., 2010). The stomach
biopsy used for the rapid urease test (RUT) also has the
added advantage that it may be used for other assays,
have the cag PAI and are usually recognized in sufferer
by their capability to produce important antidiv titers
toward the CagA marker protein (Leszczyńska
et al
., 2010;
Pohl
et al
., 2019).
VacA Vacuolating Cytotoxin
Ninety-five kDa protein that promotes extensive
hyalinization in epithelial cells is secreted by approximately
fifty percent of all pylori strains (Pohl
et al
., 2019). VacA
protein involved in the etiology of peptic ulcers and
gastric cancer. Notwithstanding, VacA hasn’t required
Figure 1:
Roles of the Cag type IV in immunological
regulation, cell multiplication, and morphologic alterations
are depicted schematically.
Figure 2:
The VacA protein regulates cellular processes
in several ways, helping in
H. pylori
chronic colonization
of the stomach mucosa (6).
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such the
Helicobacter pylori
PCR (Ferwana
et al
., 2015). In
Japanese inquiries, the same RUT material was utilized
for a quantitative PCR (qPCR) highlighting the EBV oriP
gene because the Epstein-Barr virus (EBV) causes only
a small fraction of gastric hostilities (GCs) (Mezmale
et
al
., 2020). In the 10 patients that were examined, EBV was
present in 4 cases whereas
H. pylori
was present in 9 cases.
This method emphasizes the possibility of examining
numerous infections with the same biopsy sample in order
to gain useful diagnostic data (Malfertheiner
et al
., 2017).
Histology
Helicobacter pylori
may still be seen using immunostaining
or standard staining procedures in histology, which
is still a common diagnostic approach (Bessède
et al
.,
2017). However, an innovation uses a fresh strategy with
a fluorescent probe that can be activated by glutamyl
transpeptidase (GGT) (Nakashima
et al
., 2018). In
this approach, a probe called-glutamyl hydroxymethyl
rhodamine green combines with GGT to produce
an instantaneous fluorescence (Bang
et al
., 2020).The
probe was used ex-vivo on stomach biopsies to assess
H. pylori
’s GGT activity. Its sensitivity, which ranges
from 75% to 82%, is still rather low. Another research,
which concentrated on the pathogenic features, showed
how
H. pylori
affected diseases including Brunner’s gland
hyperplasia and duodenal hamartomas (Tonkic
et al
., 2018).
Menetic Methods
Poly Chain Reaction (PCR)
Compared to other approaches, PCR, particularly the test
that targets the 16S rRNA gene, has been shown to be a
much sensible way to detect H pylori in stomach biopsies
(Benoit
et al
., 2018). The rising problem of antibiotic
resistance complicates the management of
H. pylori
infection (Makristathis
et al
., 2019). Before cultivating
H.
pylori
, real-time polymerase chain reaction (RT-PCR) is
being used increasingly frequently to solve this problem
(Godbole
et al
., 2020). High sensitivity and specificity, Fast
response for a few hours, and comfortable transportation
circumstances are only a few of the noteworthy benefits
of RT-PCR. There are many commercial RT-PCR tests
that have the added benefit of identifying resistance
to macrolide antibiotics linked to 3 distinct genetic
variation-A2142C on the 23S rRNA gene (Dalla Nora
et al
., 2016). However, alone mercantile assay—the
Genotype HelicoDR method made by German company
can identify frequent SNPs in the gyrA and 23S rRNA
genes (N87K, D91G, D91N, and D91Y) (Dalla Nora
et
al
., 2016; Stefano, Rosalia,
et al
., 2018)
Advancing Genetics Method
The molecular biology discipline uses next-generation
sequencing (NGS), a potent and sophisticated technique,
to analyze the genetic makeup of many species, including
H pylori (Pich, 2019). NGS technology enables rapid
and high-throughput DNA or RNA sample sequencing,
providing precise information on the genetic makeup of
the organism under study (Szymczak
et al
., 2020). NGS has
demonstrated to be an effective technology in the context
of
H. pylori
for a diversity of applications. It enables the
detection of genetic adjusting in the
H. pylori
genome,
such as integration, abolition, and structural variants
(Szymczak
et al
., 2020). Using this data, researchers may
trace the spread of
H. pylori
throughout communities,
study the genetic variety of various strains, and look into
the development of antibiotic resistance (Nezami
et al
.,
2019). Researchers may explore the intricate connections
between
H. pylori
and other microbes in the human gut
thanks to NGS, which makes it easier to comprehensively
analyze the whole microbial community contained in a
sample. This method sheds light on the
H. pylori
infection
and related disorders’ effects on the microbiome’s makeup
and functional capabilities (Nyssen
et al
., 2022).
NGS may also be used for proteome research, which
enables the profiling of gene expression patterns in
H. pylori
. This helps in understanding the molecular
processes underlying
H. pylori
pathogenesis and host-
pathogen interactions (Sonnenberg
et al
., 2020).
According to a Swiss research, there is a high degree
of concordance more than 99% between the findings
of tests for phenotypic antibiotic sensitivity and the
discovery of genetic diversity in certain genes linked to
antibiotic opposition (Bair
et al
., 2020). The 23S rRNA,
gyrA, and rpoB genes, which are linked to levofloxacin,
and rifampicin resistance, respectively, were examined
using whole genome sequencing (WGS) (Ding, 2020).
This association suggests that for these specific drugs,
WGS can accurately predict antibiotic resisting in
H. pylori
strains. However, the study discovered that the presence
of different SNPs in the frxA and rdxA genes could
not predict metronidazole resistance, indicating that
alternative processes may be involved in metronidazole
resistance. The results of a study carried out in Cambodia,
which showed a substantial association between genotypic
antibiotic susceptibility and WGS analysis of
H. pylori
strains, were reported with similar findings (Dore & Pes,
2021; Zhao
et al
., 2021)
Non-Invasive Tests
Urea Breath Test
Studies on urea breath tests (UBT) have been published
in the previous year. One noteworthy investigation
examined the accuracy of Bags for collecting breath
in identifying
H. pylori
. Over 250 patients participated
in the trial, which used the Breath-ID HP Lab System
(Keller
et al
., 2021). The Breath-ID HP Lab System is
very accurate and has a number of improvements over
the prior Breath-ID HP equipment, according to the
study’s authors (Makristathis
et al
., 2019). These benefits
include the capacity to examine numerous samples at
once and the bags’ outstanding stability, which makes
transportation easier. The novel approach performed
better than histology and the rapid urease test (RUT)
when compared (Ford
et al
., 2020). It is important to note
that further study is needed to examine and evaluate the
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results and possible advantages of the Breath-ID Hp
Lab System in
H. pylori
identification and management
because there haven’t been many studies published on
UBT in the last year (Q. Chen
et al
., 2019). A recent meta-
analysis conducted by (Chiang
et al
., 2021) focused on
the accuracy of 13C-urea breath tests (13C-UBT) in Asia
(Lee
et al
., 2021).
The results of the meta-analysis revealed that the
sensitivity and specificity of the 13C-UBT exploring
magnificent (Graham, 2020). However, some degree of
multiformity was esteemed across the various assessments.
Nonetheless, reconsideration indicated that it is feasible
to reduce this multiformity by adjusting certain factors,
such as the dose of urea administered and the timing
of breath sample collection. The findings of this meta-
analysis highlight the overall reliability of 13C-UBT as
a diagnostic tool for detecting
H. pylori
infection in the
Asian population (Graham, 2020). The authors suggest
that standardizing the dose and collection time of breath
samples could further enhance the consistency and
accuracy of 13C-UBT results across different studies (Al
Nabhani
et al
., 2019).
Serology
Research was done in Japan to evaluate the diagnostic
precision of two ELISA kits and two latex immunoassay
kits, which make up the four commercially available
assays for identifying
H. pylori
infection (D. Chen
et al
.,
2019). In Tokyo, the study’s main goal was to assess how
well these kits can identify
H. pylori
infection. In order to
compare the diagnostic accuracy of the kits to recognized
reference techniques, they were put through extensive
testing and analysis (Baruch
et al
., 2021). Seropositivity to
H pylori proteins was used in research conducted mostly
in the United States to identify individuals with current
infection. They used multiplex serology to evaluate
antidiv triggering to 13 H pylori proteins in blood
specimens from patients undergoing UBT (Davar
et al
.,
2021). A cutoff was used to assess sensitivity in order
to obtain 90% specificity. They eventually came to the
conclusion that seropositivity to at least two of the
H.
pylori
proteins, including VacA, and HP1564, indicated
vibrant
H. pylori
infection with high specificity and
sensitivity and may enable an estimation of the incidence
of active
H. pylori
disorder essentially accomplice (Begka
et al
., 2020).
In an analysis that combined anti-H pylori antibodies
with the Kyoto endoscopic score, the role of these
antibodies in the development of GC was finally clarified.
Scalability, emaciation and ageing among 41 and 59 years
were linked to improved serum antidiv titer infected
individuals, according to a multivariate analysis of 874
cases (D’Amato
et al
., 2020).
Stool Antigen Tests
The medical efficacy of the Meridian pylori faeces antigen
testing evaluated in a study involving 277 individuals
who underwent endoscopies. Compared to an integrated
mention test comprising other tests, the Meridian H
pylori SAT demonstrated an accuracy of 97.5% and a
precision of 98.6%, indicating as a whole effectiveness
with identifying pylori. A comparison was made between
a CLIA assay and an ELISA, the R-BioPharma, and an
immunochromatography test (ICT) using stool samples
from 266 patients. The results obtained from both kits
used for H pylori detection agreed. To assess the reliability
about a novel ICT called the Vstrip® pylori faeces antigen
fast test (Fumet
et al
., 2018)And monitor the frequency
about
H. pylori
in kora, researchers conducted a study
involving 367 participants, such as 152 asymptomatic
voluntary work and 195 instructive patients (Uribe-
Herranz
et al
., 2018; van Wijck
et al
., 2018)
Genetics Test
A comparative scrutiny was done to evaluate the efficiency
of an enhanced high-throughput, semi-automated
technique in detecting and assessing clarithromycin
susceptibility of
H. pylori
in unpreserved fecal and stomach
specimens, as compared to a previously described manual
procedure (Wilson
et al
., 2020). DNA extraction was
performed on samples obtained from 96 symptomatic
patients using both the Magna Pure 96 and QIAamp
Fast Stool kits in parallel (57). The results obtained from
stomach biopsies and fecal samples demonstrated the
feasibility of using the semi-automated method for the
detection and genotyping of pylori (Zamani
et al
., 2018).
A prospective multicenter trial involving 1200 people was
done to evaluate the Amplidiag® H pylori + ClariR test’s
capacity to detect
H. pylori
and measure clarithromycin
resistance (Aguilera Matos
et al
., 2020). To identify the
H.
pylori
glmM gene and mutations in the 23S rRNA genes
associated with clarithromycin resistance, DNA extracted
from stools using an automatic extraction method
(EasyMAG® bioMérieux) was compared to culture/E-
test and quadruplex real-time PCR performed on two
gastric biopsies (Htun
et al
., 2018). However, only 160
patients (Jaka
et al
., 2018). from the group produced valid
data. After testing several published nested PCR assays
that exhibited limited specificity, the authors designed
a novel nested PCR assay targeting the variable regions
of the 16S rRNA gene (de Martel
et al
., 2020; Stefano,
Marco,
et al
., 2018).
Novel Endoscopic Imaging Techniques
Several attempts have been made in the past to forecast
the possibility of an
H. pylori
infection during endoscopy
(Poddar, 2019). Nonetheless, there hasn’t been much of
a relationship between reported gastritis and histology
using typical white-light endoscopy. magnification
with high-resolution Endoscopes with 115 times
magnification and a resolution of 7.9 ml (Hooi
et al
.,
2017). The microvasculature of the div is seen below,
which is made up of a honeycomb-like subepithelial
capillary network produced by polygonal capillary loops
that circle the stomach pits before combining into
collecting venules (Park
et al
., 2021). Chronic
H. pylori
-
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associated gastritis disrupts this normal microvascular
arrangement. The narrowing of the pits and the
disappearance of collecting venules signify Magnification
endoscopy and narrow-band imaging appear to provide
accurate
H. pylori
infection prediction with an excellent
degree of collaboration among observers (Hathroubi
et
al
., 2020). New endoscopic methods, including confocal
endomicroscopy, focus on seeing microorganisms up
close (Ierardi
et al
., 2020).
CONCLUSION
In conclusion, a variety of considerations, including as
the unique clinical environment, efficiency, the liability of
getting positive test results, and the accessibility of the
tests, must be taken into consideration when selecting
the most suitable diagnostic test for
H. pylori
infection.
These factors are essential in choosing the best strategy
for correctly identifying
H. pylori
infection in a particular
situation. For to choose the best diagnostic test for their
patients, healthcare professionals and physicians should
carefully consider these variables.
Conflict of Interest
Non
Funding Statement
Non
Acknowledgment
We do appreciate the kind cooperation of the management
of Wasit University and Also, we thank Mustansiriyah
University in Baghdad/Iraq (http://uomustansiriyah.edu.
iq) for its support to achievement this work
REFERENCES
Aguilera Matos, I., Diaz Oliva, S. E., Escobedo, A. A.,
Villa Jiménez, O. M., & Velazco Villaurrutia, Y. D. C.
(2020). Helicobacter pylori infection in children.
BMJ
Paediatr Open, 4
(1), e000679. https://doi.org/10.1136/
bmjpo-2020-000679
Al Nabhani, Z., Dulauroy, S., Marques, R., Cousu, C., Al
Bounny, S., Déjardin, F., Sparwasser, T., Bérard, M.,
Cerf-Bensussan, N., & Eberl, G. (2019). A weaning
reaction to microbiota is required for resistance to
immunopathologies in the adult.
Immunity, 50
(5),
1276-1288. e1275.
Bair, M. J., Chuang, S. L., Lei, W. Y., Chen, C. L., Tian, H.
W., Chiang, T. H., Su, W. W. Y., Lin, C. C., Chung Lo,
Y. T., & Jou, Y. Y. (2020). Planning mass eradication
of Helicobacter pylori infection for indigenous
Taiwanese peoples to reduce gastric cancer.
Journal of
Gastroenterology and Hepatology, 35
(4), 609-616.
Bang, C. S., Lee, J. J., & Baik, G. H. (2020). Artificial
intelligence for the prediction of Helicobacter pylori
infection in endoscopic images: systematic review and
meta-analysis of diagnostic test accuracy.
Journal of
medical Internet research, 22
(9), e21983.
Baruch, E. N., Youngster, I., Ben-Betzalel, G., Ortenberg, R.,
Lahat, A., Katz, L., Adler, K., Dick-Necula, D., Raskin,
S., & Bloch, N. (2021). Fecal microbiota transplant
promotes response in immunotherapy-refractory
melanoma patients.
Science, 371
(6529), 602-609.
Begka, C., Pattaroni, C., Mooser, C., Nancey, S., McCoy,
K. D., Velin, D., & Maillard, M. H. (2020). Toll-
Interacting protein regulates immune cell infiltration
and promotes colitis-associated cancer.
Iscience, 23
(3).
Benoit, A., Hoyeau, N., & Flejou, J.-F. (2018). Diagnosis
of Helicobacter pylori infection on gastric biopsies:
Standard stain, special stain or immunohistochemistry?
Annales de Pathologie,
Bessède, E., Arantes, V., Mégraud, F., & Coelho, L. G.
(2017). Diagnosis of Helicobacter pylori infection.
Helicobacter, 22
, e12404.
Chen, D., Wu, J., Jin, D., Wang, B., & Cao, H. (2019). Fecal
microbiota transplantation in cancer management:
Current status and perspectives.
International journal of
cancer, 145
(8), 2021-2031.
Chen, Q., Liang, X., Long, X., Yu, L., Liu, W., & Lu, H.
(2019). Cost
‐e
ffectiveness analysis of screen
‐
and
‐
treat strategy in asymptomatic Chinese for preventing
Helicobacter pylori
‐
associated diseases.
Helicobacter,
24
(2), e12563.
Chiang, T.-H., Chang, W.-J., Chen, S. L.-S., Yen, A. M.-F.,
Fann, J. C.-Y., Chiu, S. Y.-H., Chen, Y.-R., Chuang, S.-
L., Shieh, C.-F., & Liu, C.-Y. (2021). Mass eradication
of Helicobacter pylori to reduce gastric cancer
incidence and mortality: a long-term cohort study on
Matsu Islands.
Gut, 70
(2), 243-250.
D’Amato, A., Di Cesare Mannelli, L., Lucarini, E., Man,
A. L., Le Gall, G., Branca, J. J., Ghelardini, C., Amedei,
A., Bertelli, E., & Regoli, M. (2020). Faecal microbiota
transplant from aged donor mice affects spatial
learning and memory via modulating hippocampal
synaptic plasticity-and neurotransmission-related
proteins in young recipients.
Microbiome, 8
(1), 1-19.
Dalla Nora, M., Hörner, R., De Carli, D. M., ROCHA,
M. P. d., ARAUJO, A. F. d., & Fagundes, R. B.
(2016). Is the immunocromatographic fecal antigen
test effective for primary diagnosis of Helicobacter
pylori infection in dyspeptic patients?
Arquivos de
Gastroenterologia, 53
, 224-227.
Davar, D., Dzutsev, A. K., McCulloch, J. A., Rodrigues,
R. R., Chauvin, J.-M., Morrison, R. M., Deblasio,
R. N., Menna, C., Ding, Q., & Pagliano, O. (2021).
Fecal microbiota transplant overcomes resistance
to anti–PD-1 therapy in melanoma patients.
Science,
371
(6529), 595-602.
de Martel, C., Georges, D., Bray, F., Ferlay, J., & Clifford,
G. M. (2020). Global burden of cancer attributable to
infections in 2018: a worldwide incidence analysis.
The
Lancet Global Health, 8
(2), e180-e190.
Ding, S.-Z. (2020). Global whole family based-
Helicobacter pylori eradication strategy to prevent
its related diseases and gastric cancer.
World journal of
gastroenterology, 26
(10), 995.
Dore, M. P., & Pes, G. M. (2021). What is new in
Pag
e
36
https://journals.e-palli.com/home/index.php/ajbb
Am. J. Biosci. Bioinforma. 2(1) 31-37, 2023
Helicobacter pylori diagnosis. An overview.
Journal of
Clinical Medicine, 10
(10), 2091.
Ferwana, M., Abdulmajeed, I., Alhajiahmed, A., Madani,
W., Firwana, B., Hasan, R., Altayar, O., Limburg, P. J.,
Murad, M. H., & Knawy, B. (2015). Accuracy of urea
breath test in Helicobacter pylori infection: meta-
analysis.
World journal of gastroenterology: WJG, 21
(4),
1305.
Ford, A. C., Yuan, Y., & Moayyedi, P. (2020). Helicobacter
pylori eradication therapy to prevent gastric cancer:
systematic review and meta-analysis.
Gut, 69
(12),
2113-2121.
Fumet, J.-D., Richard, C., Ledys, F., Klopfenstein, Q.,
Joubert, P., Routy, B., Truntzer, C., Gagné, A., Hamel,
M.-A., & Guimaraes, C. F. (2018). Prognostic and
predictive role of CD8 and PD-L1 determination
in lung tumor tissue of patients under anti-PD-1
therapy.
British journal of cancer, 119
(8), 950-960.
Godbole, G., Mégraud, F., & Bessède, E. (2020). Diagnosis
of Helicobacter pylori infection.
Helicobacter, 25
,
e12735.
Graham, D. Y. (2020). Transitioning of Helicobacter
pylori therapy from trial and error to antimicrobial
stewardship.
Antibiotics, 9
(10), 671.
Hathroubi, S., Hu, S., & Ottemann, K. M. (2020). Genetic
requirements and transcriptomics of Helicobacter
pylori biofilm formation on abiotic and biotic
surfaces.
npj Biofilms and Microbiomes, 6
(1), 56.
Hooi, J. K., Lai, W. Y., Ng, W. K., Suen, M. M., Underwood,
F. E., Tanyingoh, D., Malfertheiner, P., Graham, D. Y.,
Wong, V. W., & Wu, J. C. (2017). Global prevalence of
Helicobacter pylori infection: systematic review and
meta-analysis.
Gastroenterology, 153
(2), 420-429.
Htun, N. S. N., Odermatt, P., Müller, I., Yap, P.,
Steinmann, P., Schindler, C., Gerber, M., Du Randt,
R., Walter, C., & Pühse, U. (2018). Association
between gastrointestinal tract infections and glycated
hemoglobin in school children of poor neighborhoods
in Port Elizabeth, South Africa.
PLoS neglected tropical
diseases, 12
(3), e0006332.
Ierardi, E., Losurdo, G., Mileti, A., Paolillo, R., Giorgio,
F., Principi, M., & Di Leo, A. (2020). The puzzle of
coccoid forms of Helicobacter pylori: beyond basic
science.
Antibiotics, 9
(6), 293.
Jaka, H., Rhee, J. A., Östlundh, L., Smart, L., Peck, R.,
Mueller, A., Kasang, C., & Mshana, S. E. (2018). The
magnitude of antibiotic resistance to Helicobacter
pylori in Africa and identified mutations which confer
resistance to antibiotics: systematic review and meta-
analysis.
BMC Infectious Diseases, 18
(1), 1-10.
Keller, J., Hammer, H. F., Afolabi, P. R., Benninga, M.,
Borrelli, O., Dominguez
‐
Munoz, E., Dumitrascu, D.,
Goetze, O., Haas, S. L., & Hauser, B. (2021). European
guideline on indications, performance and clinical
impact of 13C
‐
breath tests in adult and pediatric
patients: an EAGEN, ESNM, and ESPGHAN
consensus, supported by EPC.
UEG Journal, 9
(5),
598-625.
Kim, J., & Wang, T. C. (2021). Helicobacter pylori and
gastric cancer.
Gastrointestinal Endoscopy Clinics, 31
(3),
451-465.
Lee, Y.-C., Chiang, T.-H., Chiu, H.-M., Wu, M.-S., Yeh, Y.-
P., Chen, T. H.-H., Chen, S. L.-S., Yen, A. M.-F., Fann,
J. C.-Y., & Chiu, S. Y.-H. (2021). Community-based
gastric cancer screening coupled with a National
Colorectal Cancer Screening Program: baseline
results.
Gastroenterology, 160
(6), 2159-2161. e2154.
Leszczyńska, K., Namiot, A., Namiot, Z., Leszczyńska,
J., Jakoniuk, P., Chilewicz, M., Namiot, D., Kemona,
A., Milewski, R., & Bucki, R. (2010). Patient factors
affecting culture of Helicobacter pylori isolated from
gastric mucosal specimens.
Advances in medical sciences,
55
(2), 161-166.
Makristathis, A., Hirschl, A. M., Mégraud, F., & Bessède,
E. (2019). Diagnosis of Helicobacter pylori infection.
Helicobacter, 24
, e12641.
Malfertheiner, P., Megraud, F., O’morain, C., Gisbert,
J., Kuipers, E., Axon, A., Bazzoli, F., Gasbarrini, A.,
Atherton, J., & Graham, D. Y. (2017). Management
of Helicobacter pylori infection—the Maastricht V/
Florence consensus report.
Gut, 66
(1), 6-30.
Mezmale, L., Coelho, L. G., Bordin, D., & Leja, M. (2020).
Epidemiology of Helicobacter pylori.
Helicobacter, 25
,
e12734.
Mišak, Z., & Hojsak, I. (2021). Helicobacter Pylori
Gastritis and Peptic Ulcer Disease. In Textbook
of Pediatric Gastroenterology, Hepatology and
Nutrition: A Comprehensive Guide to Practice (pp.
169-184). Springer.
Nakashima, H., Kawahira, H., Kawachi, H., & Sakaki, N.
(2018). Artificial intelligence diagnosis of Helicobacter
pylori infection using blue laser imaging-bright and
linked color imaging: a single-center prospective
study.
Annals of gastroenterology, 31
(4), 462.
Nezami, B. G., Jani, M., Alouani, D., Rhoads, D. D.,
& Sadri, N. (2019). Helicobacter pylori mutations
detected by next-generation sequencing in formalin-
fixed, paraffin-embedded gastric biopsy specimens
are associated with treatment failure.
Journal of clinical
microbiology, 57
(7), 10.1128/jcm. 01834-01818.
Nyssen, O. P., Vaira, D., Tepes, B., Kupcinskas, L., Bordin,
D., Pérez-Aisa, Á., Gasbarrini, A., Castro-Fernández,
M., Bujanda, L., & Garre, A. (2022). Room for
improvement in the treatment of Helicobacter pylori
infection: lessons from the European Registry on
H. pylori
management (Hp-EuReg).
Journal of clinical
gastroenterology, 56
(2), e98-e108.
Park, J. S., Jun, J. S., Seo, J. H., Youn, H. S., & Rhee, K.
H. (2021). Changing prevalence of Helicobacter
pylori infection in children and adolescents.
Clin
Exp Pediatr, 64
(1), 21-25. https://doi.org/10.3345/
cep.2019.01543
Pich, J. (2019). Noninvasive diagnostic tests for
helicobacter pylori infection.
Gastroenterology Nursing,
42
(1), 101-102.
Poddar, U. (2019). Helicobacter pylori: a perspective in
Pag
e
37
https://journals.e-palli.com/home/index.php/ajbb
Am. J. Biosci. Bioinforma. 2(1) 31-37, 2023
low-and middle-income countries.
Paediatrics and
International Child Health, 39
(1), 13-17.
Pohl, D., Keller, P. M., Bordier, V., & Wagner, K. (2019).
Review of current diagnostic methods and advances
in Helicobacter pylori diagnostics in the era of next
generation sequencing.
World journal of gastroenterology,
25
(32), 4629.
Sonnenberg, A., Turner, K. O., & Genta, R. M. (2020).
Low prevalence of Helicobacter pylori-positive peptic
ulcers in private outpatient endoscopy centers in the
United States.
Official journal of the American College of
Gastroenterology| ACG, 115
(2), 244-250.
Stefano, K., Marco, M., Federica, G., Laura, B., Barbara, B.,
Gioacchino, L., & Gian, L. d. A. (2018). Helicobacter
pylori, transmission routes and recurrence of
infection: state of the art.
Acta Bio Medica: Atenei
Parmensis, 89
(Suppl 8), 72.
Stefano, K., Rosalia, A., Chiara, B., Federica, G., Marco,
M., Gioacchino, L., Fabiola, F., & Gian, L. d. A.
(2018). Non-invasive tests for the diagnosis of
helicobacter pylori: state of the art. Acta Bio Medica:
Atenei Parmensis, 89
(Suppl 8), 58.
Szymczak, A., Ferenc, S., Majewska, J., Miernikiewicz, P.,
Gnus, J., Witkiewicz, W., & Dąbrowska, K. (2020).
Application of 16S rRNA gene sequencing in
Helicobacter pylori detection. PeerJ, 8, e9099.
Tonkic, A., Tonkic, M., Lehours, P., & Mégraud, F. (2012).
Epidemiology and Diagnosis of H elicobacter pylori
Infection.
Helicobacter, 17
, 1-8.
Tonkic, A., Vukovic, J., Vrebalov Cindro, P., Pesutic Pisac,
V., & Tonkic, M. (2018). Diagnosis of Helicobacter
pylori infection: A short review.
Wiener klinische
Wochenschrift, 130
, 530-534.
Uribe-Herranz, M., Bittinger, K., Rafail, S., Guedan,
S., Pierini, S., Tanes, C., Ganetsky, A., Morgan, M.
A., Gill, S., & Tanyi, J. L. (2018). Gut microbiota
modulates adoptive cell therapy via CD8α dendritic
cells and IL-12.
JCI insight, 3
(4).
van Wijck, Y., de Kleijn, S., John-Schuster, G., Mertens, T.
C., Hiemstra, P. S., Müller, A., Smits, H. H., & Taube,
C. (2018). Therapeutic application of an extract of
Helicobacter pylori ameliorates the development
of allergic airway disease.
The Journal of Immunology,
200
(5), 1570-1579.
Wilson, B. E., Routy, B., Nagrial, A., & Chin, V. T. (2020).
The effect of antibiotics on clinical outcomes in
immune-checkpoint blockade: a systematic review
and meta-analysis of observational studies.
Cancer
Immunology, Immunotherapy, 69
, 343-354.
Zamani, M., Ebrahimtabar, F., Zamani, V., Miller,
W., Alizadeh
‐
Navaei, R., Shokri
‐
Shirvani, J., &
Derakhshan, M. (2018). Systematic review with meta
‐
analysis: the worldwide prevalence of Helicobacter
pylori infection.
Alimentary pharmacology & therapeutics,
47
(7), 868-876.
Zhao, J. B., Yuan, L., Yu, X. C., Shao, Q. Q., Ma, J., Yu, M.,
Wu, Y., Qi, Y. B., Hu, R. B., & Wei, P. R. (2021). Whole
family—based Helicobacter pylori eradication is a
superior strategy to single
‐
infected patient treatment
approach: A systematic review and meta
‐
analysis.
Helicobacter, 26
(3), e12793.