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Helicobacter pylori: Antibiotic Resistance and Treatment

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A special issue of Antibiotics (ISSN 2079-6382). This special issue belongs to the section "Antibiotic Therapy in Infectious Diseases".

Deadline for manuscript submissions: closed (31 August 2021) | Viewed by 34179

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Special Issue Editors

Dr. Ilaria Maria Saracino

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Department of Experimental, Diagnostic and Specialty Medicine, School of Specialization in Microbiology and Virology, University of Bologna, 40138 Bologna, Italy
Interests: H.pylori infection; gastrointestinal microbiota; antimicrobial agents; antibiotic resistance; resistome

Dr. Matteo Pavoni

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Department of Surgical and Medical Sciences, University of Bologna, 40138 Bologna, Italy
Interests: H.pylori infection management; antibiotic resistance; gastrointestinal microbiota; use of probiotics in public health; epidemiology

Special Issue Information

Dear Colleagues,

H. pylori infection is correlated to upper gastrointestinal diseases such as peptic ulcer, MALT lymphoma, and gastric cancer. CDC states that around two-thirds of the world’s population are actually infected. In 2017, the World Health Organization categorized clarithromycin-resistant pylori as a “high-priority” bacterium.

Treatments of H. pylori infection have been complicated by the increasing trends in antimicrobial resistance worldwide, primarily due to the overuse/misuse of antibiotics and the consequent selection of resistant clones. The role played by the frequent onset of adverse events during H. pylori therapies (that lead to low compliance) should not be underestimated, either.

It is fundamental to carry out periodic assessments of H. pylori antibiotic resistance rates and to monitor treatments’ efficacy. The development of new diagnostic tools (i.e., molecular methods to detect gene mutations related to antibiotic resistance) is a very interesting field to further explore. Last but not least, integration of probiotics or other co-adjuvants during antibiotic therapy seems to have a positive impact on therapy outcome. This Special Issue seeks manuscripts that improve our understanding of antimicrobial resistance in H pylori. Submissions regarding resistance mechanisms, new methods, and new therapeutic approaches are especially encouraged.

Dr. Ilaria Maria Saracino
Dr. Matteo Pavoni
Guest Editors

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Keywords

H. pylori infection
antibiotic resistance mechanisms
antibiotic resistance rates
eradication rates new diagnostic tools
use of coadjuvants for antibiotic treatments
epidemiology

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Published Papers (7 papers)

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Research

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11 pages, 1234 KiB

Open AccessArticle

Therapeutic Potential of Sitafloxacin as a New Drug Candidate for Helicobacter Eradication in Korea: An In Vitro Culture-Based Study

by Youn I Choi, Sung Min Lee, Jun-Won Chung, Kyoung Oh Kim, Kwang An Kwon, Yoon Jae Kim, Jung Ho Kim, Sun Mi Lee, Jin-Yong Jeong and Dong Kyun Park

Antibiotics 2021, 10(10), 1242; https://doi.org/10.3390/antibiotics10101242 - 13 Oct 2021

Cited by 2 | Viewed by 2497

Abstract

Background: Increased prevalence of antibiotic resistance to Helicobacter pylori (H. pylori) infection worldwide has driven the search for a new therapeutic candidate. Recently, sitafloxacin, a novel 4-quinolone agent, has emerged as a new therapeutic option for H. pylori eradication, in Japan. However, data on its efficacy for H. pylori eradication in Korea are limited. Therefore, we aimed to investigate the therapeutic potential of sitafloxacin as a first-line treatment for patients with Helicobacter infection through gastric tissue culture-based studies. Materials and Methods: We prospectively enrolled treatment-naïve patients with H. pylori infection who visited the Gil Medical Center between March 2015 and March 2018. After obtaining written informed consent from patients, a total of 121 H. pylori strains were collected. We tested the susceptibility of these strains to sitafloxacin, and other antibiotics for Helicobacter eradication, including clarithromycin (CLR), metronidazole (MTZ), amoxicillin (AMX), tetracycline (TET), levofloxacin (LEV), and ciprofloxacin (CIP) using the agar dilution technique. The minimum inhibitory concentration (MIC) of these antibiotics against H. pylori strains were determined. Results: None of the H. pylori strains obtained were resistant to sitafloxacin (MIC > 1, n = 0), while other conventional eradication drugs including CLR, MTZ, AMX, and TET showed 24.8% (n = 30), 30.6% (n = 37), 5.0% (n = 6), and 0.8% (n = 1) resistance, respectively. Compared to the resistance rates of other quinolones (LEV [36.4%, n = 44] and CIP [37.2%, n = 45]), sitafloxacin showed the best antibiotic performance against Helicobacter strains (0%, n = 0). Furthermore, sitafloxacin also inhibited the growth of 14 H. pylori strains (12.4%), which were resistant to both of clarithromycin, and metronidazole, and 27 strains (22.3%) with multidrug resistance. Conclusions: Sitafloxacin might be a new promising candidate for Helicobacter eradication where antibiotic resistance for Helicobacter is an emerging medical burden, such as in Korea. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

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11 pages, 626 KiB

Open AccessArticle

Antibiotic Resistance Prevalence and Trends in Patients Infected with Helicobacter pylori in the Period 2013–2020: Results of the European Registry on H. pylori Management (Hp-EuReg)

by Luis Bujanda, Olga P. Nyssen, Dino Vaira, Ilaria M. Saracino, Giulia Fiorini, Frode Lerang, Sotirios Georgopoulos, Bojan Tepes, Frederic Heluwaert, Antonio Gasbarrini, Theodore Rokkas, Dmitry Bordin, Sinead Smith, Vincent Lamy, María Caldas, Elena Resina, Raquel Muñoz, Ángel Cosme, Ignasi Puig, Francis Megraud, Colm O’Morain, Javier P. Gisbert and on behalf of the Hp-EuReg Investigators Show full author list Hide full author list

Antibiotics 2021, 10(9), 1058; https://doi.org/10.3390/antibiotics10091058 - 1 Sep 2021

Cited by 74 | Viewed by 7654

Abstract

Background: Bacterial antibiotic resistance changes over time depending on multiple factors; therefore, it is essential to monitor the susceptibility trends to reduce the resistance impact on the effectiveness of various treatments. Objective: To conduct a time-trend analysis of Helicobacter pylori resistance to antibiotics in Europe. Methods: The international prospective European Registry on Helicobacter pylori Management (Hp-EuReg) collected data on all infected adult patients diagnosed with culture and antimicrobial susceptibility testing positive results that were registered at AEG-REDCap e-CRF until December 2020. Results: Overall, 41,562 patients were included in the Hp-EuReg. Culture and antimicrobial susceptibility testing were performed on gastric biopsies of 3974 (9.5%) patients, of whom 2852 (7%) were naive cases included for analysis. The number of positive cultures decreased by 35% from the period 2013–2016 to 2017–2020. Concerning naïve patients, no antibiotic resistance was found in 48% of the cases. The most frequent resistances were reported against metronidazole (30%), clarithromycin (25%), and levofloxacin (20%), whereas resistances to tetracycline and amoxicillin were below 1%. Dual and triple resistances were found in 13% and 6% of the cases, respectively. A decrease (p < 0.001) in the metronidazole resistance rate was observed between the 2013–2016 (33%) and 2017–2020 (24%) periods. Conclusion: Culture and antimicrobial susceptibility testing for Helicobacter pylori are scarcely performed (<10%) in Europe. In naïve patients, Helicobacter pylori resistance to clarithromycin remained above 15% throughout the period 2013–2020 and resistance to levofloxacin, as well as dual or triple resistances, were high. A progressive decrease in metronidazole resistance was observed. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

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8 pages, 253 KiB

Open AccessArticle

Rescue Therapy with Furazolidone in Patients with at Least Five Eradication Treatment Failures and Multi-Resistant H. pylori infection

by Elena Resina and Javier P. Gisbert

Antibiotics 2021, 10(9), 1028; https://doi.org/10.3390/antibiotics10091028 - 24 Aug 2021

Cited by 8 | Viewed by 3667

Abstract

Helicobacter pylori infection may persist after multiple eradication treatments. The aim of this study was to evaluate the efficacy and safety of a furazolidone-based rescue regimen in hyper-refractory patients. A unicentre, prospective study was designed. Patients in whom five or more treatments had consecutively failed were included. All patients had previously received bismuth and key antibiotics, such as amoxicillin, clarithromycin, metronidazole, levofloxacin, tetracycline, and rifabutin, and had positive H. pylori culture, demonstrating resistance to clarithromycin, metronidazole, and levofloxacin. A quadruple regimen with furazolidone (200 mg), amoxicillin (1 g), bismuth (240 mg), and esomeprazole (40 mg) was prescribed twice a day for 14 days. Eradication was confirmed by the stool antigen test. Compliance was determined through questioning, and adverse effects using a questionnaire. Eight patients (mean age 56 years, 63% men, 38% peptic ulcer disease, 12% gastric cancer precursor lesions, and 50% functional dyspepsia) were included. Per-protocol and intention-to-treat eradication rates were 63%. Compliance was 100%. Adverse effects were reported in two (25%) patients, and all were mild. Even after five or more previous H. pylori eradication failures, and a multi-resistant infection, rescue treatment with furazolidone may be effective in approximately two-thirds of the cases, constituting a valid strategy after multiple previous eradication failures with key antibiotics such as clarithromycin, metronidazole, tetracycline, levofloxacin, and rifabutin. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

24 pages, 1684 KiB

Open AccessArticle

The Role of Statins on Helicobacter pylori Eradication: Results from the European Registry on the Management of H. pylori (Hp-EuReg)

by María Caldas, Ángeles Pérez-Aisa, Bojan Tepes, Alma Keco-Huerga, Luis Bujanda, Alfredo J. Lucendo, Luis Rodrigo, Dino Vaira, Luis Fernández-Salazar, Jose M. Huguet, Jorge Pérez-Lasala, Natasa Brglez Jurecic, Galina Fadeenko, Jesús Barrio, Miguel Areia, Juan Ortuño, Rinaldo Pellicano, Marcis Leja, Javier Molina-Infante, Pavel Bogomolov, Sergey Alekseenko, Manuel Domínguez-Cajal, Judith Gómez-Camarero, Vassiliki Ntouli, Samuel J. Martínez-Domínguez, Rafael Ruiz-Zorrilla, Oscar Núñez, Aiman Silkanovna Sarsenbaeva, Pedro Almela, Perminder Phull, Marta Espada, Ignasi Puig, Olga P. Nyssen, Francis Mégraud, Colm O’Morain, Javier P. Gisbert and on behalf of the Hp-EuReg Investigators Show full author list Hide full author list

Antibiotics 2021, 10(8), 965; https://doi.org/10.3390/antibiotics10080965 - 11 Aug 2021

Cited by 9 | Viewed by 4996

Abstract

Statins could increase the effectiveness of Helicobacter pylori eradication therapies due to their anti-inflammatory effect. The aim of this study was to analyze the impact of this therapeutic association in real life. This is a multicenter, prospective, non-interventional study aimed at evaluating the management of H. pylori by European gastroenterologists. Patients were registered in an e-CRF by AEG-REDCap from 2013 to 2020. The association between statin use and H. pylori eradication effectiveness was evaluated through multivariate analysis. Overall, 9988 and 705 patients received empirical and culture-guided treatment, respectively. Overall, statin use was associated with higher effectiveness in the empirical group (OR = 1.3; 95%CI = 1.1–1.5), but no association was found with first-line treatment effectiveness (N = 7738); as an exception, statin use was specifically associated with lower effectiveness of standard triple therapy (OR = 0.76; 95%CI = 0.59–0.99). In the rescue therapy empirical group (N = 2228), statins were associated with higher overall effectiveness (OR = 1.9; 95%CI = 1.4–2.6). However, sub-analyses by treatment schemes only confirmed this association for the single-capsule bismuth quadruple therapy (OR = 2.8; 95%CI = 1.3–5.7). No consistent association was found between statin use and H. pylori therapy effectiveness. Therefore, the addition of statins to the usual H. pylori treatment cannot be currently recommended to improve cure rates. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

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15 pages, 910 KiB

Open AccessArticle

European Registry on Helicobacter pylori Management: Effectiveness of First and Second-Line Treatment in Spain

by María Caldas, Ángeles Pérez-Aisa, Manuel Castro-Fernández, Luis Bujanda, Alfredo J. Lucendo, Luis Rodrigo, Jose M. Huguet, Jorge Pérez-Lasala, Javier Molina-Infante, Jesús Barrio, Luis Fernández-Salazar, Ángel Lanas, Mónica Perona, Manuel Domínguez-Cajal, Juan Ortuño, Blas José Gómez-Rodríguez, Pedro Almela, Josep María Botargués, Óscar Núñez, Inés Modolell, Judith Gómez, Rafael Ruiz-Zorrilla, Cristóbal De la Coba, Alain Huerta, Eduardo Iyo, Liliana Pozzati, Rosario Antón, Mercé Barenys, Teresa Angueira, Miguel Fernández-Bermejo, Ana Campillo, Javier Alcedo, Ramón Pajares-Villaroya, Marianela Mego, Fernando Bermejo, José Luis Dominguez-Jiménez, Llúcia Titó, Nuria Fernández, Manuel Pabón-Carrasco, Ángel Cosme, Pilar Mata-Romero, Noelia Alcaide, Inés Ariño, Tommaso Di Maira, Ana Garre, Ignasi Puig, Olga P. Nyssen, Francis Megraud, Colm O’Morain and Javier P. Gisbert Show full author list Hide full author list

Antibiotics 2021, 10(1), 13; https://doi.org/10.3390/antibiotics10010013 - 25 Dec 2020

Cited by 19 | Viewed by 4794

Abstract

The management of Helicobacter pylori infection has to rely on previous local effectiveness due to the geographical variability of antibiotic resistance. The aim of this study was to evaluate the effectiveness of first and second-line H. pylori treatment in Spain, where the empirical prescription is recommended. A multicentre prospective non-interventional registry of the clinical practice of European gastroenterologists concerning H. pylori infection (Hp-EuReg) was developed, including patients from 2013 until June 2019. Effectiveness was evaluated descriptively and through a multivariate analysis concerning age, gender, presence of ulcer, proton-pump inhibitor (PPI) dose, therapy duration and compliance. Overall, 53 Spanish hospitals were included, and 10,267 patients received a first-line therapy. The best results were obtained with the 10-day bismuth single-capsule therapy (95% cure rate by intention-to-treat) and with both the 14-day bismuth-clarithromycin quadruple (PPI-bismuth-clarithromycin-amoxicillin, 91%) and the 14-day non-bismuth quadruple concomitant (PPI-clarithromycin-amoxicillin-metronidazole, 92%) therapies. Second-line therapies were prescribed to 2448 patients, with most-effective therapies being the triple quinolone (PPI-amoxicillin-levofloxacin/moxifloxacin) and the bismuth-levofloxacin quadruple schemes (PPI-bismuth-levofloxacin-amoxicillin) prescribed for 14 days (92%, 89% and 90% effectiveness, respectively), and the bismuth single-capsule (10 days, 88.5%). Compliance, longer duration and higher acid inhibition were associated with higher effectiveness. “Optimized” H. pylori therapies achieve over 90% success in Spain. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

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Review

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15 pages, 316 KiB

Open AccessReview

Next Generation Sequencing for the Prediction of the Antibiotic Resistance in Helicobacter pylori: A Literature Review

by Ilaria Maria Saracino, Matteo Pavoni, Angelo Zullo, Giulia Fiorini, Tiziana Lazzarotto, Claudio Borghi and Dino Vaira

Antibiotics 2021, 10(4), 437; https://doi.org/10.3390/antibiotics10040437 - 14 Apr 2021

Cited by 32 | Viewed by 5187

Abstract

Background and aims: Only a few antimicrobials are effective against H. pylori, and antibiotic resistance is an increasing problem for eradication therapies. In 2017, the World Health Organization categorized clarithromycin resistant H. pylori as a “high-priority” bacterium. Standard antimicrobial susceptibility testing can be used to prescribe appropriate therapies but is currently recommended only after the second therapeutic failure. H. pylori is, in fact, a “fastidious” microorganism; culture methods are time-consuming and technically challenging. The advent of molecular biology techniques has enabled the identification of molecular mechanisms underlying the observed phenotypic resistance to antibiotics in H. pylori. The aim of this literature review is to summarize the results of original articles published in the last ten years, regarding the use of Next Generation Sequencing, in particular of the whole genome, to predict the antibiotic resistance in H. pylori.Methods: a literature research was made on PubMed. The research was focused on II and III generation sequencing of the whole H. pylori genome. Results: Next Generation Sequencing enabled the detection of novel, rare and complex resistance mechanisms. The prediction of resistance to clarithromycin, levofloxacin and amoxicillin is accurate; for other antimicrobials, such as metronidazole, rifabutin and tetracycline, potential genetic determinants of the resistant status need further investigation. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

Other

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8 pages, 866 KiB

Open AccessPerspective

Rescue Therapies for H. pylori Infection in Italy

by Vincenzo De Francesco, Angelo Zullo, Luigi Gatta, Raffaele Manta, Matteo Pavoni, Ilaria Maria Saracino, Giulia Fiorini and Dino Vaira

Antibiotics 2021, 10(5), 525; https://doi.org/10.3390/antibiotics10050525 - 3 May 2021

Cited by 4 | Viewed by 3250

Abstract

Background/Aims: Curing Helicobacter pylori infection remains challenging for clinicians, as no proposed first-line therapy achieves bacterial eradication in all treated patients so that several patients need two or more consecutive treatments. Bacterial culture with antibiotics susceptibility testing is largely unachievable in Italy, and empiric second-line and rescue therapies are generally used. This study aimed to identify what eradication regimens perform better in Italy, following first-line therapy failure. Methods: We performed a literature search on PubMed for studies on standard therapy regimens used as second-line or rescue treatments performed in adult patients. Studies including modified drug combinations were not considered. Both intention-to-treat and per- protocol analyses were computed for each therapy subgroup. Results: Data from 35 studies with a total of 4830 patients were eventually considered. As a second-line therapy, Pylera^® (90.6%) and a sequential regimen (89.8%) achieved eradication rates significantly higher than other therapies. For third-line therapy, a levofloxacin-based regimen and Pylera^® achieved comparable eradication rates (88.2% vs. 84.7%; p = 0.2). Among therapies used as fourth (or more) attempts, Pylera^® and a rifabutin-based therapy achieved 77.4% and 66.4% cure rates, respectively (p = 0.013). A therapy sequence based on the type of first-line therapy used was proposed. Conclusions: Data obtained through our review indicate that standard therapies for H. pylori eradication can be used when following an appropriate sequence, allowing clinicians to improve the cure rate without resorting to bacterial culture. Full article

(This article belongs to the Special Issue Helicobacter pylori: Antibiotic Resistance and Treatment)

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