Insights into the Pathogenesis, Virulence Factors, and Diagnosis of Helicobacter pylori: A Comprehensive Review

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Кадхим, А. С., & Ал-Карави, А. С. (2024). Insights into the Pathogenesis, Virulence Factors, and Diagnosis of Helicobacter pylori: A Comprehensive Review. in Library, 1(2), 31–37. извлечено от https://inlibrary.uz/index.php/archive/article/view/30690
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Аннотация

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.

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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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Am. J. Biosci. Bioinforma. 2(1) 31-37, 2023

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

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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


background image

Pag

e

36

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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


background image

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.

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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 inHelicobacter 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 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 Helicobacterpylori 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.

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