Overview of <i>Helicobacter pylori</i> Infection, Prevalence, Risk Factors, and Its Prevention

Bashir, Samina Khan; Khan, Muhammad Bashir

doi:https://doi.org/10.1155/2023/9747027

Advanced Gut & Microbiome Research

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Review Article | Open Access

Volume 2023 | Article ID 9747027 | https://doi.org/10.1155/2023/9747027

Overview of Helicobacter pylori Infection, Prevalence, Risk Factors, and Its Prevention

Samina Khan Bashir¹and Muhammad Bashir Khan²

Academic Editor: Jian Wu

Received30 Dec 2022

Revised13 Apr 2023

Accepted26 Apr 2023

Published10 May 2023

Abstract

Helicobacter pylori (H. pylori) (formerly known as Campylobacter pyloridis) has been studied for over a century due to its association with peptic ulcer disease and gastric cancer. Its prevalence has been declining due to improvements in hygienic conditions and effective curative and preventive approaches. However, it is still present in different communities and continues to spread, increasing its global presence in both developing as well as developed countries. Extensive research has been ongoing to eradicate this pathogen, and at present, scientists have discovered different management options. This article highlights the global prevalence of H. pylori infection and the factors responsible for its transmission, treatment regimens, and prevention.

1. Introduction

Helicobacter pylori belongs to the family Helicobacteraceae. It is a transmissible and pathogenic gram-negative spiral-shaped bacterium thought to be a contaminant of digested food as opposed to being a true colonizer of the gastric mucosa [1]. It was first successfully isolated and discovered by Barry Marshall and Robin Warren in 1980, for which they were awarded the Nobel Prize in 2005 [2]. They intentionally ingested the bacterium and subsequently developed persistent gastritis. Later, it was found that the bacteria are strongly associated with multiple upper gastrointestinal disorders, such as chronic gastritis, peptic ulcer disease, gastric mucosa-associated lymphoid tissue (MALT) lymphoma, and gastric cancer [3–5].

H. pylori is the most common human bacterial infection occurring in ~4.4 billion people, representing over 50% of the world population. The World Health Organization (WHO) now considers it a class 1 carcinogen leading to peptic ulcer disease and gastric cancer [6–8]. The H. pylori infection rate is 30–50% in developed and 85–95% in developing countries [9–12]. More specifically, the infection rate is 30% in Western countries and 20–30% in North America, in which it is 23% in the province of Ontario and 13% in Quebec. Infection rates are higher in Africans (25%), Asians (30%), and South Americans (34%) and significantly lower in Caucasians (8%) who reside in Canada [13–15]. The pathogen is more prevalent in North Americans, Aboriginals, and recent immigrants [16].

In 2006, the Canadian North Helicobacter pylori Working Group (CANHelp) was established to identify specifically the impact of H. pylori infection in the Canadian Arctic communities [15–17]. The rate of documented infection in these communities was 55% in the 2008 survey. In one study, 95% seropositivity was revealed in the native community in northwestern Manitoba and a 67% infection rate in children two years of age. The pathogen is also prevalent in Aboriginals of Russia, Alaska, and Greenland, and the infection ratio ranged from 47% to 88% [18–20]. Furthermore, the infection rate is relatively higher in immigrants from countries such as India or China than in those born in Canada from the same ethnic groups [14].

H. pylori infection prevalence increases with age within the first ten years of life [21–23]. The incidence of H. pylori infection in childhood varies greatly [24]. The childhood infection rate in some underdeveloped countries is reported to be 90% [25, 26], while in developed countries, it ranges from as low as 1.8% to as high as 65% [27, 28]. Details about the global prevalence are elaborated in Table 1.

1.1. Factors Contributing to H. pylori Infection

The exact mechanism of H. pylori infection is currently unknown; however, socioeconomic and environmental factors are known to play an important role [1, 31]. H. pylori infection occurs in early childhood and remains silent for years; only 30% of individuals develop observable signs and symptoms of gastritis. Transmission occurs through oral-oral, fecal-oral, and gastro-oral routes [32, 33]. As an example, mother-to-child transmission occurs if the mother’s saliva is contaminated or due to poor hand hygiene. The pathogen is transmitted by direct means, e.g., kissing or sharing utensils [34], or by indirect means, such as drinking water, air, animals, flies, and food [33]. The occurrence of H. pylori infection supports the transmission of fecal contaminants in the institutionalized young population during the epidemic of gastroenteritis [35]. Similarly, in refrigerated food, the pathogen may survive for a short period and is the source of infection [36]. Additionally, it is associated with dietary habits, particularly milk, meat, and vegetables [1, 37–39]. One Indian study revealed that the prevalence is more common in the lower socioeconomic group [40]. Drinking unfiltered water, tobacco, and meat consumption are risk factors for developing H. pylori infection. Moreover, drinking unboiled water in restaurants in urban areas increases the spread of the pathogen [41, 42]. The acquisition and transmission of the pathogen increase in dense living conditions, when using nonsteroidal anti-inflammatory drugs, in the blood group O, with obesity, and with a family history of gastric disease [43–46]. Eating fried food has a positive correlation with infection [47].

Antibiotic resistance is another contributing factor for H. pylori infection as antibiotic resistance is primarily responsible for failing to completely eradicate H. pylori. In certain cases, a patient will undergo 14 days of quadruple therapy and, subsequently, either develop the infection again or develop complications of H. pylori infection. The main cause of antibiotic resistance is the overuse of antibiotics; metronidazole shows the highest resistance rate and is widely used in most countries for various gastrointestinal illnesses [48–53].

A major contributor to the increased prevalence of bacterial infections, including H. pylori infection, is the global emergence of antibiotic-resistant bacteria, threatening the efficacy of antibiotics which have transformed medicine and saved countless lives [54–56]. The leading cause of antibiotic resistance is the overuse or misuse of antibiotics due to a misguided perception in many people that antibiotics can cure any kind of illness. This has caused people to view antibiotics as a cure-all and routinely request them from their physicians, even for viral illnesses. This, compounded with the improper use of antibiotics, leads to resistance. Additionally, incorrectly prescribed antibiotics also promote antibiotic resistance. Research reveals that in 30–50% of cases, the indication for treatment, antibiotic choice, and duration of antibiotic therapy is incorrect [57, 58]. In many countries, antibiotics are available over the counter without prescription; this ease of obtaining antibiotics also contributes to the problem [59, 60]. Lack of regulation and easy availability of a variety of cheap antibiotics in the market as well as online lead to the misuse and overuse of antibiotics [59].

Finally, the lack of new drug development by the pharmaceutical industry due to the decreased financial incentives and challenging regulatory requirements is contributing to the antibiotic resistance crisis [59, 61, 62]. New research policies and coordinated efforts to control antibiotic resistance are greatly needed [63]. This will help in the eradication of bacterial pathogens.

1.2. The Clinical Course of H. pylori Infection

H. pylori infection is not a disease in itself, but it presents with a spectrum of clinical disorders of the upper gastrointestinal tract and hepatobiliary tract [1]. Dyspepsia is the predominant symptom, and a patient may present with epigastric pain, early satiety, nausea, vomiting, and heartburn [64] (Figure 1). H. pylori infection positivity is two times more common in dyspeptic patients than in asymptomatic individuals [65], and the first warning sign for peptic ulcer disease and gastric cancer is dyspepsia [66]. The association between gastroesophageal reflux disease (GERD) and H. pylori infection is still in debate. However, esophageal inflammation is increased by H. pylori, and it increases the incidence of Barrett’s esophagitis (BE) and GERD [67, 68]. A casual causative factor for chronic gastritis is H. pylori infection, which leads to the persistent inflammation of the gastric mucosa that may progress to gastric atrophy and intestinal metaplasia [69].

The lifetime risk of developing ulcer disease is 10–20%, distal gastric cancer risk is 1–2% [70–72], and mucosa-associated lymphoid tissue (MALT) lymphoma risk is <0.1% [73] in H. pylori-positive patients (Figure 1). Both gastric and duodenal ulcers are strongly associated with this pathogen. In the initial decade after the H. pylori discovery, it was found that 95% of duodenal ulcers and 85% of gastric cancer occurred with H. pylori [72]. The development of peptic ulcer disease (PUD) is commonly caused by H. pylori and nonsteroidal anti-inflammatory (NSAID) use; nevertheless, every individual using NSAID and infected with H. pylori does not develop PUD [74, 75]. Patients with duodenal ulcers usually complain of abdominal pain two to three hours after taking meals on an empty stomach or abdominal pain at night, whereas patients with gastric ulcers complain of nausea, vomiting, weight loss, and postprandial abdominal pain. The complication of PUD is bleeding, perforation, penetration, gastric outlet obstruction, and gastric malignancy (adenocarcinoma and MALT) [76]. Bleeding is the most common complication of PUD, and almost 40–60% of upper gastrointestinal bleeding is caused by PUD [77]. With regard to gastric cancer, which is the fifth most common cancer and the third leading cause of death globally, H. pylori is the major risk factor for its development. The precancerous lesion is usually started by the H. pylori infection with the transformation of the normal mucosa to nonatrophic gastritis that may lead to atrophic gastritis and intestinal metaplasia [78].

All these complications of H. pylori are attributed to the severity of gastric inflammation, which is determined by multiple hosts and bacterial factors. The cytotoxin-associated gene-A pathogenic island (cag PAI) is a well-characterized H. pylori virulence determinant. It is a 42 kb insertion element that consists of 32 genes that encode the bacterial type 4 secretion system. The cag A pathogenic island is 60–70% present in the western strain of H. pylori and almost 100% of the East Asian H. pylori strain. The cag PAI presence is associated with more severe gastritis, peptic ulceration, atrophic gastritis, and gastric cancer [79, 80]. Among host factors, the evidence emphasizes H. pylori-induced acid production. Increased production of acid limits H. pylori gastritis to the antrum, which increases the risk of duodenal ulceration, while reducing acid secretion promotes more proximal inflammation that favors the risk of atrophic gastritis, gastric ulcer disease, and gastric cancer [81].

1.3. Diagnosis and Management

Accurate diagnosis of H. pylori infection is essential for the effective treatment of various gastroduodenal diseases. Multiple tests have been developed over time for the detection of H. pylori infection. Each test has its benefits and limitations. In a clinical setting, the use of a single test is generally adequate for the diagnosis. Generally, the tests are divided into two categories, i.e., invasive and noninvasive tests (Table 2) [1, 82].

Invasive tests are based on the endoscopic biopsy taken from the gastroduodenal part for histology, culture, rapid urease test, and molecular methods. Noninvasive tests are based on peripheral samples, such as the blood, breath samples, and stool specimens, for the detection of antibodies, bacterial antigen, and urease activity. Fecal antigen tests and urea breath tests are the most widely used noninvasive tests in clinical settings for the detection of H. pylori infection and during follow-up after eradication antibiotic treatment, while blood samples are used for screening and epidemiological studies [83]. However, the complications of H. pylori infection are not diagnosed by noninvasive tests. H. pylori-infected individuals usually develop certain antibodies in their circulation, such as IgA, IgG, and IgM. These antibodies are determined by specific serological tests which are noninvasive, rapid, cheap, and helpful in diagnosing the H. pylori infection or when there are equivocal test results by other methods due to complications, e.g., bleeding ulcers, or when the patient is on antibiotics or antisecretory treatment [84]. The detection of serological responses to cytotoxin-associated gene A (cag A) gives useful information about serious gastroduodenal infections, such as gastric malignancy and MALT.

cag A is common in Western and East Asian strains of H. pylori. However, this is not useful in other countries as the bacterial virulence strains are different in other countries [86]. Serum antibodies were detected via the enzyme-linked immunosorbent assay (ELISA), latex agglutination, or immunochromatography [84, 87].

Different antibiotic regimens have been used for the eradication of H. pylori infection. Generally, a single drug does not cure the infection. Usual treatment regimens consist of multiple antibiotics that are taken for two weeks (14 days). The standard triple therapy (STT) was established in the past for the eradication of this pathogen. STT consists of amoxicillin, clarithromycin, and proton pump inhibitor; however, the efficacy of the STT regimens has changed over time in many countries mainly because of antibiotic resistance, and other factors contributing to reduced eradication are patient compliance, genetic polymorphism, obesity, smoking, and reinfection. Most of the treatment regimens involve taking proton pump inhibitors, which reduce gastric acid production and allow the bacterial-damaged tissues to heal [88, 89].

Initial regimens to eradicate H. pylori in patients suffering from peptic ulcer disease relied on proton pump inhibitors (PPIs) to inhibit the final step in the acid secretion pathway (gastric H⁺ and K⁺-ATPase) [90] (Figure 2). However, PPIs and antibiotics were subsequently found to work synergistically with each other to eradicate H. pylori. Since then, antibiotics have been included in eradication regimens. Current treatments rely on acid suppression combined with at least two antibiotics. The role of acid suppression has been attributed to the antibacterial activity of PPIs, either directly through the inhibition of urease activity or through increased stability and activity of antibiotics [91–93].

One of the widely used first-line antibiotic regimens is the quadruple therapy for 14 days, which involves taking bismuth, tetracycline, PPI, and metronidazole [88, 89, 94]. The quadruple therapy is superior to the triple therapy (STT) [95]. Concomitant therapy consists of three antibiotics, i.e., metronidazole or nitroimidazole, amoxicillin, tetracycline, and PPI, for 14 days [88, 89, 94]. Concomitant therapy is better than STT [96]. Sequential therapy, which involves taking a PPI and amoxicillin for five days followed by clarithromycin, tinidazole, and PPI for another five days is less effective than the concomitant therapy; however, there is still debate about which one is superior [97, 98]. Some studies recommend a treatment of levofloxacin once daily along with PPI, cefuroxime, and bismuth for 7 to 14 days [99], while some suggest rifabutin-based therapy for rescue [100]. As PPI has a shorter duration of action, now, the longer-acting potassium competitive acid blocker (P-CAB), which has a rapid onset of action and is effective for a longer duration, is also used in some countries, such as Japan, and is considered a more potent first-line treatment in reducing gastric secretion [101]. In case primary therapy fails, the second line should be selected based on the previous therapy used and local antibiotic resistance data [88]. Different antibiotic regimens are shown in Figure 3 [88, 102].

1.4. Modern Approach

A novel approach utilizes the susceptibility-guided strategy that is published in the 2017 Maastricht VI guidelines to create a tailored therapy against H. pylori infection. The new approach depends on choosing the antibiotics according to local antibiotic resistance data. Maastricht guidelines propose different regimens of quadruple therapy, primarily concomitant therapy, and bismuth-based therapy [94]. Modifications in usual antibiotic regimens (metronidazole, amoxicillin, and clarithromycin) used in the treatment of H. pylori infection have also been proposed, such as sequential, hybrid, and reverse hybrid therapies [103, 104]. However, eradication efficacy is rarely above 90%, which has been the main goal of modified antimicrobial therapy, and this is due to complex multiple antibiotic use at one time and possible side effects of antibiotics limiting the compliance and effectiveness of therapy [105].

New proposals support the use of 14 days of triple therapy, usage of four drug regimens, higher doses of PPI, or the use of a novel PPI, i.e., vonoprazan (P-CAB) and probiotic supplementation with antibiotics [106]. Probiotics, such as Lactobacillus spp, Bifidobacterium spp, and Saccharomyces boulardii, are not directly involved in the eradication of H. pylori infection; rather, they reduce the side effects of antibiotics [103, 107, 108].

The 2022 Maastricht VI guidelines support susceptibility testing before prescribing antibiotics for H. pylori infection [104] by obtaining a culture from gastric mucosa following endoscopic biopsy and using agar dilution, disc diffusion, or an E test for the detection of antibiotic sensitivity [109]. The gold standard is the agar dilution method, but it is expensive, time-consuming, and labor-intensive [110]. The other method to test antibiotic sensitivity is by genotype molecular testing from the stool and stomach biopsy specimens using real-time polymerase chain reaction (PCR) and fluorescence in situ hybridization (FISH), while commercially available kits are used to detect point mutations related to specific antibiotic resistance [111]. Moreover, whole-genome sequencing techniques have been used to identify drug-resistant mutations [112]. These practices will need to be established in clinical settings as it is debatable whether each dyspeptic patient should be subjected to endoscopy. However, noninvasive techniques, i.e., PCR testing on stool samples or DNA extraction from stool samples, make it possible to avoid invasive testing, such as endoscopy, for the detection of antibiotic sensitivity [113, 114]. The prospects in H. pylori management [103, 115] are shown in Table 3.

2. Conclusion

H. pylori infection prevalence has been reduced overall, but the pathogen is still present in different communities globally. Poor socioeconomic factors, hygiene, eating processed food, restaurant meals, meat, and unfiltered water have been the major contributing factors to H. pylori infection and its complications. Antibiotic resistance creates major problems in curing the infection and controlling the prevalence of H. pylori. However, antibiotic susceptibility testing is a novel way to provide a tailored therapy to achieve a complete cure.

Lifestyle modifications are necessary to minimize the risk of H. pylori infection. These include proper hand washing, reducing the consumption of frozen/processed food, washing packed salads/vegetables properly before eating, and drinking boiled water. Overuse and misuse of antibiotics need to be discouraged, and completion of the antibiotic course along with probiotics should be promoted.

Hence, providing awareness through various ethnic media channels to various communities and demographic groups is the most important tool available to achieve these measures. Furthermore, routine screening for H. pylori infection in both immigrant and nonimmigrant populations will help in curing the infection. Ongoing research into new drugs and vaccines is greatly needed with a global collaborative effort to eradicate this pathogen, as H. pylori is a serious global health issue and a major cause of gastric cancer.

Data Availability

Previously reported (statistics) data were used to support this study. These prior studies (and datasets) are cited at relevant places within the text as references [1–98].

Conflicts of Interest

The authors declare that they have no conflicts of interest.

References

J. G. Kusters, A. H. van Vliet, and E. J. Kuipers, “Pathogenesis of Helicobacter pylori infection,” Clinical Microbiology Reviews, vol. 19, no. 3, pp. 449–490, 2006.
View at: Publisher Site | Google Scholar
A. Morris and G. Nicholson, “Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH,” The American Journal of Gastroenterology, vol. 82, no. 3, pp. 192–199, 1987.
View at: Google Scholar
K. M. Fock, D. Y. Graham, and P. Malfertheiner, “Helicobacter pylori research: historical insights and future directions,” Nature Reviews Gastroenterology & Hepatology, vol. 10, no. 8, pp. 495–500, 2013.
View at: Publisher Site | Google Scholar
M. D. Burkitt, C. A. Duckworth, J. M. Williams, and D. M. Pritchard, “Helicobacter pylori-induced gastric pathology: insights from in vivo and ex vivo models,” Disease Models & Mechanisms, vol. 10, no. 2, pp. 89–104, 2017.
View at: Publisher Site | Google Scholar
B. Bauer and T. F. Meyer, “The Human Gastric Pathogen Helicobacter pylori and Its Association with Gastric Cancer and Ulcer Disease,” Ulcers, vol. 2011, Article ID 340157, 23 pages, 2011.
View at: Publisher Site | Google Scholar
L. E. Wroblewski, R. M. Peek, and K. T. Wilson, “Helicobacter pylori and gastric cancer: factors that modulate disease risk,” Clinical Microbiology Reviews, vol. 23, no. 4, pp. 713–739, 2010.
View at: Publisher Site | Google Scholar
D. Bravo, A. Hoare, C. Soto, M. A. Valenzuela, and A. F. Quest, “Helicobacter pylori in human health and disease: mechanisms for local gastric and systemic effects,” World Journal of Gastroenterology, vol. 24, no. 28, pp. 3071–3089, 2018.
View at: Publisher Site | Google Scholar
S. M. Alexander, R. J. Retnakumar, D. Chouhan et al., “Helicobacter pylori in human stomach: the inconsistencies in clinical outcomes and the probable causes,” Frontiers in Microbiology, vol. 12, article 713955, 2021.
View at: Publisher Site | Google Scholar
C. Burucoa and A. Axon, “Epidemiology ofHelicobacter pyloriinfection,” Helicobacter, vol. 22, Supplement 1, 2017.
View at: Publisher Site | Google Scholar
World Gastroenterology Organisation, “World Gastroenterology Organisation global guideline: Helicobacter pylori in developing countries,” Journal of Clinical Gastroenterology, vol. 45, no. 5, pp. 383–388, 2011.
View at: Publisher Site | Google Scholar
G. Khoder, J. S. Muhammad, I. Mahmoud, S. S. M. Soliman, and C. Burucoa, “Prevalence of Helicobacter pylori and its associated factors among healthy asymptomatic residents in the United Arab Emirates,” Pathogens, vol. 8, no. 2, 2019.
View at: Publisher Site | Google Scholar
R. H. Hunt, S. D. Xiao, F. Megraud et al., “Helicobacter pylori in developing countries. World Gastroenterology Organisation global guideline,” Journal of Gastrointestinal and Liver Diseases, vol. 20, no. 3, pp. 299–304, 2011.
View at: Google Scholar
P. Willems, J. de Repentigny, G. M. Hassan, S. Sidani, G. Soucy, and M. Bouin, “The prevalence of Helicobacter pylori infection in a quaternary hospital in Canada,” Journal of Clinical Medical Research, vol. 12, no. 11, pp. 687–692, 2020.
View at: Publisher Site | Google Scholar
F. Naja, N. Kreiger, and T. Sullivan, “Helicobacter pylori infection in Ontario: prevalence and risk factors,” Canadian Journal of Gastroenterology, vol. 21, no. 8, pp. 501–506, 2007.
View at: Publisher Site | Google Scholar
K. J. Goodman, K. Jacobson, and S. Veldhuyzen van Zanten, “Helicobacter pylori infection in Canadian and related Arctic Aboriginal populations,” Canadian Journal of Gastroenterology, vol. 22, no. 3, pp. 289–295, 2008.
View at: Publisher Site | Google Scholar
N. Jones, N. Chiba, C. Fallone et al., “Helicobacter pylori in First Nations and recent immigrant populations in Canada,” Canadian Journal of Gastroenterology, vol. 26, no. 2, pp. 97–103, 2012.
View at: Publisher Site | Google Scholar
J. Cheung, K. Goodman, R. Munday et al., “Helicobacter Pylori infection in Canada’s Arctic: searching for the solutions,” Canadian Journal of Gastroenterology, vol. 22, no. 11, pp. 912–916, 2008.
View at: Publisher Site | Google Scholar
J. K. Johansen, A. Sehested, T. Myrhøj, K. Ladefoged, and K. A. Krogfelt, “Helicobacter pylori infection in Greenlandic patients with dyspepsia,” International Journal of Circumpolar Health, vol. 63, no. sup2, pp. 219-220, 2004.
View at: Publisher Site | Google Scholar
O. V. Reshetnikov, Y. P. Nikitin, M. V. Kholmogortsev, S. A. Kurilovich, and O. A. Pycllik, “Helicobacter pylori in a Chukotka Native male population,” International Journal of Circumpolar Health, vol. 57, Supplement 1, pp. 293–295, 1998.
View at: Google Scholar
J. Zhu, M. Davidson, M. Leinonen et al., “Prevalence and persistence of antibodies to herpes viruses, Chlamydia pneumoniae and Helicobacter pylori in Alaskan Eskimos: the GOCADAN study,” Clinical Microbiology and Infection, vol. 12, no. 2, pp. 118–122, 2006.
View at: Publisher Site | Google Scholar
J. Younger and A. Duggan, “Helicobacter pylori infection in elderly patients,” The Lancet, vol. 360, no. 9337, p. 947, 2002.
View at: Publisher Site | Google Scholar
M. C. Bateson, “Helicobacter pylori infection with age,” The Lancet, vol. 339, no. 8801, p. 1121, 1992.
View at: Publisher Site | Google Scholar
S. K. Tiwari, G. Manoj, G. V. Kumar et al., “Prognostic significance of genotyping Helicobacter pylori infection in patients in younger age groups with gastric cancer,” Postgraduate Medical Journal, vol. 84, no. 990, pp. 193–197, 2008.
View at: Publisher Site | Google Scholar
D. Mahalanabis, M. M. Rahman, S. A. Sarker et al., “Helicobacter pylori infection in the young in Bangladesh: prevalence, socioeconomic and nutritional aspects,” International Journal of Epidemiology, vol. 25, no. 4, pp. 894–898, 1996.
View at: Publisher Site | Google Scholar
B. A. Salih, “Helicobacter pylori infection in developing countries: the burden for how long?” Saudi Journal of Gastroenterology, vol. 15, no. 3, pp. 201–207, 2009.
View at: Publisher Site | Google Scholar
E. Hestvik, T. Tylleskar, D. H. Kaddu-Mulindwa et al., “Helicobacter pylori in apparently healthy children aged 0-12 years in urban Kampala, Uganda: a community-based cross sectional survey,” BMC Gastroenterology, vol. 10, p. 62, 2010.
View at: Publisher Site | Google Scholar
E. Roma and E. Miele, “Helicobacter pylori infection in pediatrics,” Helicobacter, vol. 20, Supplement 1, pp. 47–53, 2015.
View at: Publisher Site | Google Scholar
H. M. Malaty, V. Paykov, O. Bykova et al., “Helicobacter pylori and socioeconomic factors in Russia,” Helicobacter, vol. 1, no. 2, pp. 82–87, 1996.
View at: Publisher Site | Google Scholar
J. K. Y. Hooi, W. Y. Lai, W. K. Ng et al., “Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis,” Gastroenterology, vol. 153, no. 2, pp. 420–429, 2017.
View at: Publisher Site | Google Scholar
M. Zamani, F. Ebrahimtabar, V. Zamani et al., “Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection,” Alimentary Pharmacology & Therapeutics, vol. 47, no. 7, pp. 868–876, 2018.
View at: Publisher Site | Google Scholar
S. Kayali, M. Manfredi, F. Gaiani et al., “Helicobacter pylori, transmission routes and recurrence of infection: state of the art,” Acta Bio Medica: Atenei Parmensis, vol. 89, no. 8-S, pp. 72–76, 2018.
View at: Publisher Site | Google Scholar
T. Yılmaz, M. D. Bajin, R. Günaydın, S. Ozer, and T. Sözen, “Laryngopharyngeal reflux and Helicobacter pylori,” World Journal of Gastroenterology, vol. 20, no. 27, pp. 8964–8970, 2014.
View at: Publisher Site | Google Scholar
R. P. Allaker, K. A. Young, J. M. Hardie, P. Domizio, and N. J. Meadows, “Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission,” Journal of Medical Microbiology, vol. 51, no. 4, pp. 312–317, 2002.
View at: Publisher Site | Google Scholar
H. Brenner, D. Rothenbacher, G. Bode, P. Dieudonné, and G. Adler, “Active infection with Helicobacter pylori in healthy couples,” Epidemiology and Infection, vol. 122, no. 1, pp. 91–95, 1999.
View at: Publisher Site | Google Scholar
R. Laporte, P. Pernes, P. Pronnier, F. Gottrand, and P. Vincent, “Acquisition of Helicobacter pylori infection after outbreaks of gastroenteritis: prospective cohort survey in institutionalised young people,” BMJ, vol. 329, no. 7459, pp. 204-205, 2004.
View at: Publisher Site | Google Scholar
R. E. Poms and S. R. Tatini, “Survival of Helicobacter pylori in ready-to-eat foods at 4°C,” International Journal of Food Microbiology, vol. 63, no. 3, pp. 281–286, 2001.
View at: Publisher Site | Google Scholar
S. Kabir, “Detection of Helicobacter pylori DNA in feces and saliva by polymerase chain reaction: a review,” Helicobacter, vol. 9, no. 2, pp. 115–123, 2004.
View at: Publisher Site | Google Scholar
D. A. Ferguson, C. Jiang, D. S. Chi, J. J. Laffan, C. Li, and E. Thomas, “Evaluation of two string tests for obtaining gastric juice for culture, nested-PCR detection, and combined single- and double-stranded conformational polymorphism discrimination of Helicobacter pylori,” Digestive Diseases and Sciences, vol. 44, no. 10, pp. 2056–2062, 1999.
View at: Publisher Site | Google Scholar
D. A. Ferguson, C. Li, N. R. Patel, W. R. Mayberry, D. S. Chi, and E. Thomas, “Isolation of Helicobacter pylori from saliva,” Journal of Clinical Microbiology, vol. 31, no. 10, pp. 2802–2804, 1993.
View at: Publisher Site | Google Scholar
R. S. Mhaskar, I. Ricardo, A. Azliyati et al., “Assessment of risk factors of Helicobacter pylori infection and peptic ulcer disease,” Journal of Global Infectious Diseases, vol. 5, no. 2, pp. 60–67, 2013.
View at: Publisher Site | Google Scholar
D. Palli, N. E. Caporaso, Y. H. Shiao et al., “Helicobacter pylori, and p53 mutations in gastric cancer: a molecular epidemiology study in Italy,” Cancer Epidemiology, Biomarkers & Prevention, vol. 6, no. 12, pp. 1065–1069, 1997.
View at: Google Scholar
R. K. Phukan, K. Narain, E. Zomawia, N. C. Hazarika, and J. Mahanta, “Dietary habits and stomach cancer in Mizoram, India,” Journal of Gastroenterology, vol. 41, no. 5, pp. 418–424, 2006.
View at: Publisher Site | Google Scholar
I. Segal, R. Ally, and H. Mitchell, “Helicobacter pylori--an African perspective,” QJM, vol. 94, no. 10, pp. 561–565, 2001.
View at: Publisher Site | Google Scholar
V. H. Chong, K. C. Lim, and N. Rajendran, “Prevalence of active Helicobacter pylori infection among patients referred for endoscopy in Brunei Darussalam,” Singapore Medical Journal, vol. 49, no. 1, pp. 42–46, 2008.
View at: Google Scholar
C. Dube, T. C. Nkosi, A. M. Clarke, N. Mkwetshana, E. Green, and R. N. Ndip, “Helicobacter pylori antigenemia in an asymptomatic population of Eastern Cape Province, South Africa: public health implications,” Reviews on Environmental Health, vol. 24, no. 3, pp. 249–255, 2009.
View at: Publisher Site | Google Scholar
A. Ogihara, S. Kikuchi, A. Hasegawa et al., “Relationship between Helicobacter pylori infection and smoking and drinking habits,” Journal of Gastroenterology and Hepatology, vol. 15, no. 3, pp. 271–276, 2000.
View at: Publisher Site | Google Scholar
Y. Zhu, X. Zhou, J. Wu, J. Su, and G. Zhang, “Risk factors and prevalence of Helicobacter pylori infection in persistent high incidence area of gastric carcinoma in Yangzhong city,” Gastroenterology Research and Practice, vol. 2014, Article ID 481365, 10 pages, 2014.
View at: Publisher Site | Google Scholar
F. Mégraud, “H pylori antibiotic resistance: prevalence, importance, and advances in testing,” Gut, vol. 53, no. 9, pp. 1374–1384, 2004.
View at: Publisher Site | Google Scholar
F. Mégraud, “The challenge of Helicobacter pylori resistance to antibiotics: the comeback of bismuth-based quadruple therapy,” Therapeutic Advances in Gastroenterology, vol. 5, no. 2, pp. 103–109, 2012.
View at: Publisher Site | Google Scholar
J. Chen, P. Li, Y. Huang, Y. Guo, Z. Ding, and H. Lu, “Primary antibiotic resistance of Helicobacter pylori in different regions of China: a systematic review and meta-analysis,” Pathogens, vol. 11, no. 7, 2022.
View at: Publisher Site | Google Scholar
A. Shiotani, H. Lu, M. P. Dore, and D. Y. Graham, “Treating Helicobacter pylori effectively while minimizing misuse of antibiotics,” Cleveland Clinic Journal of Medicine, vol. 84, no. 4, pp. 310–318, 2017.
View at: Publisher Site | Google Scholar
J. Yaxley and B. Chakravarty, “Helicobacter pylori eradication - an update on the latest therapies,” Australian Family Physician, vol. 43, no. 5, pp. 301–305, 2014.
View at: Google Scholar
W. Wu, Y. Yang, and G. Sun, “Recent insights into antibiotic resistance in Helicobacter pylori eradication,” Gastroenterology Research and Practice, vol. 2012, Article ID 723183, 8 pages, 2012.
View at: Publisher Site | Google Scholar
Z. Golkar, O. Bagasra, and D. G. Pace, “Bacteriophage therapy: a potential solution for the antibiotic resistance crisis,” The Journal of Infection in Developing Countries, vol. 8, no. 2, pp. 129–136, 2014.
View at: Publisher Site | Google Scholar
C. L. Ventola, “The antibiotic resistance crisis: part 1: causes and threats,” Pharmacy and Therapeutics, vol. 40, no. 4, pp. 277–283, 2015.
View at: Google Scholar
S. Sengupta, M. K. Chattopadhyay, and H. P. Grossart, “The multifaceted roles of antibiotics and antibiotic resistance in nature,” Frontiers in Microbiology, vol. 4, p. 47, 2013.
View at: Publisher Site | Google Scholar
C. E. Luyt, N. Bréchot, J. L. Trouillet, and J. Chastre, “Antibiotic stewardship in the intensive care unit,” Critical Care, vol. 18, no. 5, p. 480, 2014.
View at: Publisher Site | Google Scholar
“Antibiotic resistance threats in the United States, 2013,” 2013, https://stacks.cdc.gov/view/cdc/20705.
View at: Google Scholar
C. A. Michael, D. Dominey-Howes, and M. Labbate, “The antimicrobial resistance crisis: causes, consequences, and management,” Frontiers in Public Health, vol. 2, p. 145, 2014.
View at: Publisher Site | Google Scholar
E. Nature, “The antibiotic alarm,” Nature, vol. 495, no. 7440, p. 141, 2013.
View at: Publisher Site | Google Scholar
J. G. Bartlett, D. N. Gilbert, and B. Spellberg, “Seven ways to preserve the miracle of antibiotics,” Clinical Infectious Diseases, vol. 56, no. 10, pp. 1445–1450, 2013.
View at: Publisher Site | Google Scholar
I. M. Gould and A. M. Bal, “New antibiotic agents in the pipeline and how they can help overcome microbial resistance,” Virulence, vol. 4, no. 2, pp. 185–191, 2013.
View at: Publisher Site | Google Scholar
B. Spellberg and D. N. Gilbert, “The future of antibiotics and resistance: a tribute to a career of leadership by John Bartlett,” Clinical Infectious Diseases, vol. 59, Supplement 2, pp. S71–S75, 2014.
View at: Publisher Site | Google Scholar
P. Moayyedi, B. E. Lacy, C. N. Andrews, R. A. Enns, C. W. Howden, and N. Vakil, “ACG and CAG clinical guideline: management of dyspepsia,” The American Journal of Gastroenterology, vol. 112, no. 7, pp. 988–1013, 2017.
View at: Publisher Site | Google Scholar
B. Suvak, A. C. Dulger, O. Suvak, E. Aytemiz, and O. Kemik, “The prevalence of Helicobacter pylori among dyspeptic patients in an earthquake-stricken area,” Clinics, vol. 70, no. 1, pp. 69–72, 2015.
View at: Publisher Site | Google Scholar
A. B. Olokoba, O. A. Obateru, M. O. Bojuwoye, O. K. Ibrahim, and L. B. Olokoba, “That dyspepsia in the young could be cancer,” Nigerian Medical Journal, vol. 54, no. 2, pp. 143–145, 2013.
View at: Publisher Site | Google Scholar
F. X. Liu, W. H. Wang, J. Wang, J. Li, and P. P. Gao, “Effect of Helicobacter pylori infection on Barrett’s esophagus and esophageal adenocarcinoma formation in a rat model of chronic gastroesophageal reflux,” Helicobacter, vol. 16, no. 1, pp. 66–77, 2011.
View at: Publisher Site | Google Scholar
F. R. Polat and S. Polat, “The effect of Helicobacter pylori on gastroesophageal reflux disease,” Journal of the Society of Laparoendoscopic Surgeons, vol. 16, no. 2, pp. 260–263, 2012.
View at: Publisher Site | Google Scholar
P. Sipponen and H. Hyvärinen, “Role of Helicobacter pylori in the pathogenesis of gastritis, peptic ulcer and gastric cancer,” Scandinavian Journal of Gastroenterology. Supplement, vol. 28, no. sup196, pp. 3–6, 1993.
View at: Publisher Site | Google Scholar
P. B. Ernst and B. D. Gold, “The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer,” Annual Review of Microbiology, vol. 54, no. 1, pp. 615–640, 2000.
View at: Publisher Site | Google Scholar
E. J. Kuipers, “Review article: exploring the link between Helicobacter pylori and gastric cancer,” Alimentary Pharmacology & Therapeutics, vol. 13, Supplement 1, pp. 3–11, 1999.
View at: Publisher Site | Google Scholar
E. J. Kuipers, J. C. Thijs, and H. P. Festen, “The prevalence of Helicobacter pylori in peptic ulcer disease,” Alimentary Pharmacology & Therapeutics, vol. 9, Supplement 2, pp. 59–69, 1995.
View at: Google Scholar
R. M. Peek and J. E. Crabtree, “Helicobacter infection and gastric neoplasia,” The Journal of Pathology, vol. 208, no. 2, pp. 233–248, 2006.
View at: Publisher Site | Google Scholar
B. B. Zhang, Y. Li, X. Q. Liu, P. J. Wang, B. Yang, and D. L. Bian, “Association between vacA genotypes and the risk of duodenal ulcer: a meta-analysis,” Molecular Biology Reports, vol. 41, no. 11, pp. 7241–7254, 2014.
View at: Publisher Site | Google Scholar
M. Feldman, L. S. Friedman, and L. J. Brandt, Sleisenger and Fordtran's Gastrointestinal and Liver Disease E-book: Pathophysiology, Diagnosis, Management, Elsevier Health Sciences, 2020.
M. Narayanan, K. M. Reddy, and E. Marsicano, “Peptic ulcer disease and Helicobacter pylori infection,” Missouri Medicine, vol. 115, no. 3, pp. 219–224, 2018.
View at: Google Scholar
A. Lanas, L. A. García-Rodríguez, M. Polo-Tomás et al., “The changing face of hospitalisation due to gastrointestinal bleeding and perforation,” Alimentary Pharmacology & Therapeutics, vol. 33, no. 5, pp. 585–591, 2011.
View at: Publisher Site | Google Scholar
P. Díaz, M. Valenzuela Valderrama, J. Bravo, and A. F. G. Quest, “Helicobacter pylori and gastric cancer: adaptive cellular mechanisms involved in disease progression,” Frontiers in Microbiology, vol. 9, p. 5, 2018.
View at: Publisher Site | Google Scholar
J. F. Tomb, O. White, A. R. Kerlavage et al., “The complete genome sequence of the gastric pathogen Helicobacter pylori,” Nature, vol. 388, no. 6642, pp. 539–547, 1997.
View at: Publisher Site | Google Scholar
N. S. Akopyants, S. W. Clifton, D. Kersulyte et al., “Analyses of the cag pathogenicity island of Helicobacter pylori,” Molecular Microbiology, vol. 28, no. 1, pp. 37–53, 1998.
View at: Publisher Site | Google Scholar
E. J. Kuipers, “Helicobacter pylori and the risk and management of associated diseases: gastritis, ulcer disease, atrophic gastritis and gastric cancer,” Alimentary Pharmacology & Therapeutics, vol. 11, Supplement 1, pp. 71–88, 1997.
View at: Publisher Site | Google Scholar
Y. K. Wang, F. C. Kuo, C. J. Liu et al., “Diagnosis of Helicobacter pylori infection: current options and developments,” World Journal of Gastroenterology, vol. 21, no. 40, pp. 11221–11235, 2015.
View at: Publisher Site | Google Scholar
S. Kayali, R. Aloe, C. Bonaguri et al., “Non-invasive tests for the diagnosis of Helicobacter pylori: state of the art,” Acta Bio Medica: Atenei Parmensis, vol. 89, no. 8-S, pp. 58–64, 2018.
View at: Publisher Site | Google Scholar
H. Suzuki, T. Masaoka, S. Nomura et al., “Current consensus on the diagnosis and treatment of H. pylori-associated gastroduodenal disease,” The Keio Journal of Medicine, vol. 52, no. 3, pp. 163–173, 2003.
View at: Publisher Site | Google Scholar
P. Sabbagh, M. Mohammadnia-Afrouzi, M. Javanian et al., “Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations,” European Journal of Clinical Microbiology & Infectious Diseases, vol. 38, no. 1, pp. 55–66, 2019.
View at: Publisher Site | Google Scholar
D. Vaira, J. Holton, M. Menegatti et al., “New immunological assays for the diagnosis of Helicobacter pylori infection,” Gut, vol. 45, Supplement 1, pp. I23–I27, 1999.
View at: Publisher Site | Google Scholar
W. D. Chey, B. C. Wong, and Practice Parameters Committee of the American College of Gastroenterology, “American College of Gastroenterology guideline on the management of Helicobacter pylori infection,” The American Journal of Gastroenterology, vol. 102, no. 8, pp. 1808–1825, 2007.
View at: Publisher Site | Google Scholar
W. D. Chey, G. I. Leontiadis, C. W. Howden, and S. F. Moss, “ACG clinical guideline: treatment of Helicobacter pylori infection,” The American Journal of Gastroenterology, vol. 112, no. 2, pp. 212–239, 2017.
View at: Publisher Site | Google Scholar
C. A. Fallone, N. Chiba, S. V. van Zanten et al., “The Toronto consensus for the treatment of Helicobacter pylori infection in adults,” Gastroenterology, vol. 151, no. 1, pp. 51–69.e14, 2016.
View at: Publisher Site | Google Scholar
K. Abe, K. Irie, H. Nakanishi, H. Suzuki, and Y. Fujiyoshi, “Crystal structures of the gastric proton pump,” Nature, vol. 556, no. 7700, pp. 214–218, 2018.
View at: Publisher Site | Google Scholar
J. P. Gisbert, “Potent gastric acid inhibition in Helicobacter pylori eradication,” Drugs, vol. 65, no. 1, pp. 83–96, 2005.
View at: Publisher Site | Google Scholar
D. R. Scott, G. Sachs, and E. A. Marcus, “The role of acid inhibition in Helicobacter pylori eradication,” F1000Research, vol. 5, 2016.
View at: Publisher Site | Google Scholar
P. Malfertheiner, S. F. Moss, P. Daniele et al., “Potassium-competitive acid blocker and proton pump inhibitor-based regimens for first-line Helicobacter pylori eradication: a network meta-analysis,” Gastro Hep Advances, vol. 1, no. 5, pp. 824–834, 2022.
View at: Publisher Site | Google Scholar
P. Malfertheiner, F. Megraud, C. A. O'Morain et al., “Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report,” Gut, vol. 66, no. 1, pp. 6–30, 2017.
View at: Publisher Site | Google Scholar
B. Z. Li, D. E. Threapleton, J. Y. Wang et al., “Comparative effectiveness and tolerance of treatments for Helicobacter pylori: systematic review and network meta-analysis,” BMJ, vol. 351, article h4052, 2015.
View at: Publisher Site | Google Scholar
J. P. Gisbert and X. Calvet, “Review article: non-bismuth quadruple (concomitant) therapy for eradication of Helicobacter pylori,” Alimentary Pharmacology & Therapeutics, vol. 34, no. 6, pp. 604–617, 2011.
View at: Publisher Site | Google Scholar
J. W. Chung, J. P. Han, K. O. Kim et al., “Ten-day empirical sequential or concomitant therapy is more effective than triple therapy for Helicobacter pylori eradication: a multicenter, prospective study,” Digestive and Liver Disease, vol. 48, no. 8, pp. 888–892, 2016.
View at: Publisher Site | Google Scholar
A. G. McNicholl, A. C. Marin, J. Molina-Infante et al., “Randomised clinical trial comparing sequential and concomitant therapies for Helicobacter pylori eradication in routine clinical practice,” Gut, vol. 63, no. 2, pp. 244–249, 2014.
View at: Publisher Site | Google Scholar
Z. Song, W. Fu, and L. Zhou, “Cefuroxime, levofloxacin, esomeprazole, and bismuth as first-line therapy for eradicating Helicobacter pylori in patients allergic to penicillin,” BMC Gastroenterology, vol. 19, no. 1, p. 132, 2019.
View at: Publisher Site | Google Scholar
M. Heep, D. Beck, E. Bayerdörffer, and N. Lehn, “Rifampin and rifabutin resistance mechanism in Helicobacter pylori,” Antimicrobial Agents and Chemotherapy, vol. 43, no. 6, pp. 1497–1499, 1999.
View at: Publisher Site | Google Scholar
D. Y. Graham and M. P. Dore, “Update on the use of vonoprazan: a competitive acid blocker,” Gastroenterology, vol. 154, no. 3, pp. 462–466, 2018.
View at: Publisher Site | Google Scholar
H. K. Jung, S. J. Kang, Y. C. Lee et al., “Evidence-based guidelines for the treatment of Helicobacter pylori infection in Korea 2020,” Liver, vol. 15, no. 2, pp. 168–195, 2021.
View at: Publisher Site | Google Scholar
P. Malfertheiner, F. Megraud, T. Rokkas et al., “Management of Helicobacter pylori infection: the Maastricht VI/Florence consensus report,” Gut, vol. 71, no. 9, pp. 1724–1762, 2022.
View at: Publisher Site | Google Scholar
A. Mestrovic, N. Perkovic, J. Bozic et al., “Randomised clinical trial comparing concomitant and hybrid therapy for eradication of Helicobacter pylori infection,” PLoS One, vol. 15, no. 12, article e0244500, 2020.
View at: Publisher Site | Google Scholar
H. Taguchi, S. Kanmura, T. Maeda et al., “Helicobacter pylori eradication improves the quality of life regardless of the treatment outcome: a multicenter prospective cohort study,” Medicine, vol. 96, no. 52, article e9507, 2017.
View at: Publisher Site | Google Scholar
P. Roszczenko-Jasinska, M. I. Wojtys, and E. K. Jagusztyn-Krynicka, “Helicobacter pylori treatment in the post-antibiotics era-searching for new drug targets,” Applied Microbiology and Biotechnology, vol. 104, no. 23, pp. 9891–9905, 2020.
View at: Publisher Site | Google Scholar
B. G. Zhou, L. X. Chen, B. Li, L. Y. Wan, and Y. W. Ai, “Saccharomyces boulardii as an adjuvant therapy for Helicobacter pylori eradication: a systematic review and meta-analysis with trial sequential analysis,” Helicobacter, vol. 24, no. 5, article e12651, 2019.
View at: Publisher Site | Google Scholar
Z. Lv, B. Wang, X. Zhou et al., “Efficacy and safety of probiotics as adjuvant agents for Helicobacter pylori infection: a meta-analysis,” Experimental and Therapeutic Medicine, vol. 9, no. 3, pp. 707–716, 2015.
View at: Publisher Site | Google Scholar
Q. Ma, H. Li, J. Liao, Z. Cai, and B. Zhang, “Tailored therapy for Helicobacter pylori eradication: a systematic review and meta-analysis,” Frontiers in Pharmacology, vol. 13, article 908202, 2022.
View at: Publisher Site | Google Scholar
S. K. Ogata, A. C. Gales, and E. Kawakami, “Antimicrobial susceptibility testing for Helicobacter pylori isolates from Brazilian children and adolescents: comparing agar dilution, E-test, and disk diffusion,” Brazilian Journal of Microbiology, vol. 45, no. 4, pp. 1439–1448, 2014.
View at: Publisher Site | Google Scholar
R. Gingold-Belfer, Y. Niv, H. Schmilovitz-Weiss, Z. Levi, and D. Boltin, “Susceptibility-guided versus empirical treatment for Helicobacter pylori infection: a systematic review and meta-analysis,” Journal of Gastroenterology and Hepatology, vol. 36, no. 10, pp. 2649–2658, 2021.
View at: Publisher Site | Google Scholar
B. G. Nezami, M. Jani, D. Alouani, D. D. Rhoads, and N. Sadri, “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, vol. 57, no. 7, 2019.
View at: Publisher Site | Google Scholar
R. J. Gong, C. X. Xu, H. Li, and X. M. Liu, “Polymerase chain reaction-based tests for detecting Helicobacter pylori clarithromycin resistance in stool samples: a meta-analysis,” World Journal of Clinical Cases, vol. 9, no. 1, pp. 133–147, 2021.
View at: Publisher Site | Google Scholar
D. Y. Graham and S. F. Moss, “Antimicrobial susceptibility testing for Helicobacter pylori is now widely available: when, how, why,” The American Journal of Gastroenterology, vol. 117, no. 4, pp. 524–528, 2022.
View at: Publisher Site | Google Scholar
S. Suzuki, M. Esaki, C. Kusano, H. Ikehara, and T. Gotoda, “Development of Helicobacter pylori treatment: how do we manage antimicrobial resistance?” World Journal of Gastroenterology, vol. 25, no. 16, pp. 1907–1912, 2019.
View at: Publisher Site | Google Scholar

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Copyright © 2023 Samina Khan Bashir and Muhammad Bashir Khan. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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