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Keikha M, Karbalaei M. Prevalence of antibiotic heteroresistance associated with Helicobacter pylori infection: A systematic review and meta-analysis. Microb Pathog 2022; 170:105720. [PMID: 35964816 DOI: 10.1016/j.micpath.2022.105720] [Citation(s) in RCA: 13] [Impact Index Per Article: 4.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/29/2022] [Revised: 08/05/2022] [Accepted: 08/08/2022] [Indexed: 10/15/2022]
Abstract
BACKGROUND Heteroresistance is a general term to describe diverse responses to specific antibiotics that can occur due to infection with either multiple bacterial strains or microevolution of a single strain during chronic infection. Due to limited information regarding heteroresistance Helicobacter pylori (H. pylori) infection, the current study was carried out to evaluate the prevalence of this phenomenon. METHODS For this study, all potential relevant studies were collected by searching international databases such as ISI Web of Science, PubMed, Scopus, ScienceDirect, ProQuest, Embase, DOAJ, China National Knowledge Infrastructure (CNKI), and Google Scholar. Finally, the frequency of heteroresistance H. pylori infection was measured using the event rate corresponding to 95% confidence intervals. RESULTS A total of 26 studies met our criteria; the eligible studies were related to the years 2001-2022. Our results showed that the prevalence of heteroresistance H. pylori strains was 60.1% to clarithromycin, 61.1% to metronidazole, 46.1% to levofloxacin, 3.8% to amoxicillin, and 21.1% to tetracycline. Our literature review also showed discrepancy of antimicrobial susceptibility test in strains isolated from different anatomical sites of the stomach. Heteroresistance H. pylori infection in developing countries is mostly due to infection with multiple H. pylori strains, while in developed countries it is due to microevolution of a single H. pylori strain in response to antibiotic pressure. CONCLUSIONS Heteroresistance H. pylori infection interferes with successful therapy and eventually can lead to the treatment failure. If a biopsy is taken from only one gastric site, resistant strains of H. pylori may be underestimated. Considering the role of heteroresistance H. pylori infection in treatment failure, it is very important for gastroenterologists to improve their knowledge about this fact. Regardingly, new guidelines should be developed and designed for the management and treatment of heteroresistance H. pylori infection.
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Affiliation(s)
- Masoud Keikha
- Department of Microbiology and Virology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
| | - Mohsen Karbalaei
- Department of Microbiology and Virology, School of Medicine, Jiroft University of Medical Sciences, Jiroft, Iran.
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Where to Biopsy to Detect Helicobacter pylori and How Many Biopsies Are Needed to Detect Antibiotic Resistance in a Human Stomach. J Clin Med 2020; 9:jcm9092812. [PMID: 32878081 PMCID: PMC7565078 DOI: 10.3390/jcm9092812] [Citation(s) in RCA: 12] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/24/2020] [Revised: 08/18/2020] [Accepted: 08/26/2020] [Indexed: 12/20/2022] Open
Abstract
This study aims to determine the gastric distribution, density, and diversity of Helicobacter pylori infection. Subtotal resection of the stomachs of three H. pylori-infected and asymptomatic obese patients were collected after a sleeve gastrectomy. Distribution and density of H. pylori were determined using culture and RT-PCR on multiple gastric sites (88, 176, and 101 biopsies per patient). Diversity of H. pylori strains was studied using antibiotic susceptibility testing, random amplified polymorphism DNA (RAPD) typing and cagA gene detection on single-colony isolates (44, 96, and 49 isolates per patient). H. pylori was detected in nearly all analyzed sites (354/365 biopsies, 97%). Antral density was higher in one patient only. The three stomachs were almost exclusively infected by an antibiotic-susceptible strain. One clarithromycin-resistant isolate in one biopsy was detected in two stomachs (1/44 and 1/49 isolates), while in the third one, eight (8/96 isolates) metronidazole-resistant isolates were detected. DNA typing showed infection with cagA-negative strains for one patient, cagA-positive strains for a second patient and the third patient was infected with two different strains of distinct cagA genotypes. Infection with H. pylori is shown to spread to the whole surface of the stomach, but a possibility of minor sub-population of antibiotic-resistant clones, undetectable in routine practice.
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Kocsmár É, Kocsmár I, Buzás GM, Szirtes I, Wacha J, Takáts A, Hritz I, Schaff Z, Rugge M, Fassan M, Kiss A, Lotz G. Helicobacter pylori heteroresistance to clarithromycin in adults-New data by in situ detection and improved concept. Helicobacter 2020; 25:e12670. [PMID: 31701608 DOI: 10.1111/hel.12670] [Citation(s) in RCA: 19] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/20/2019] [Revised: 09/16/2019] [Accepted: 10/07/2019] [Indexed: 01/06/2023]
Abstract
BACKGROUND Clarithromycin (Cla) heteroresistance of Helicobacter pylori (H pylori) infections is commonly assessed by comparing the resistance status of antrum and corpus biopsy samples and by demonstrating the discrepancy between them (interniche heteroresistance). However, fluorescence in situ hybridization (FISH) technique is capable of showing the synchronous presence of susceptible and resistant bacteria (intraniche heteroresistance), enabling the detection of heteroresistant H pylori populations within one biopsy sample. MATERIALS AND METHODS Antrum and corpus biopsy specimens of 305 H pylori-infected patients were investigated with an rRNA-targeted Cla-resistance FISH test. Anamnestic data were collected from the institutional electronic register. Prevalence rates of susceptible, homo- and heteroresistant cases were correlated with the anamnestic and clinicopathological data. RESULTS Overall Cla-resistance rate was 23.9% (73 cases), consisting of 35 (11.5%) homoresistant and 38 (12.5%) heteroresistant cases. Thirty-five patients had at least one biopsy site where susceptible and resistant bacteria were present simultaneously. From this subset, 20 cases demonstrated intraniche heteroresistance on both sites. Prior Cla-based eradication attempts were more frequent in homoresistant than in susceptible and heteroresistant cases (P < .001, P < .001, respectively). Cla-containing therapy eradicated heteroresistant infections at a significantly lower rate in comparison with susceptible cases (P = .0112), but more effectively than homoresistants (P = .0393). CONCLUSIONS The most frequent type of Cla-heteroresistance is the coexistence of susceptible and resistant H pylori bacteria in the same location (intraniche heteroresistance). A previous Cla-based eradication attempt predisposes patients to homoresistant infection. Heteroresistance is characterized by a non-eradication-related background and intermediate characteristics in many respects when compared to susceptible and homoresistant cases.
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Affiliation(s)
- Éva Kocsmár
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
| | - Ildikó Kocsmár
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
| | - György Miklós Buzás
- Department of Gastroenterology, Ferencváros Health Centre, Budapest, Hungary
| | - Ildikó Szirtes
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
| | - Judit Wacha
- First Department of Surgery, Semmelweis University, Budapest, Hungary
| | - Alajos Takáts
- First Department of Surgery, Semmelweis University, Budapest, Hungary
| | - István Hritz
- First Department of Surgery, Semmelweis University, Budapest, Hungary
| | - Zsuzsa Schaff
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
| | - Massimo Rugge
- Surgical Pathology & Cytopathology Unit, Department of Medicine (DIMED), University of Padua, Padua, Italy.,Veneto Tumor Registry (RTV), Veneto Regional Authority, Padova, Italy
| | - Matteo Fassan
- Surgical Pathology & Cytopathology Unit, Department of Medicine (DIMED), University of Padua, Padua, Italy
| | - András Kiss
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
| | - Gábor Lotz
- Second Department of Pathology, Semmelweis University, Budapest, Hungary
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Cho JH, Jeon SR, Kim HG, Jin SY, Park S. Factors for improving the diagnostic efficiency of the rapid urease test from the gastric corpus. Scand J Gastroenterol 2017; 52:1320-1325. [PMID: 28927301 DOI: 10.1080/00365521.2017.1378712] [Citation(s) in RCA: 9] [Impact Index Per Article: 1.1] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 02/04/2023]
Abstract
OBJECTIVE This study aimed to evaluate the optimal biopsy site for Helicobacter pylori detection by comparing the results of rapid urease test (RUT) between the gastric corpus and the antrum. METHODS A biopsy specimen from each subject was obtained from the corpus and from the antrum. For each subject, the two specimens were separately immersed in two different RUT kits. Positive reaction times were measured at 20 minutes and 1, 3, and 24 hours. If either of the two RUT kits showed a positive reaction, H. pylori infection was confirmed. RESULTS A total of 310 H. pylori-infected subjects were eligible for study inclusion. Compared with the antrum, positive RUT reaction times in the corpus were shorter when the degree of gastric atrophy was moderate or severe (p = .001 and p < .001, respectively). A multivariate analysis revealed that the factors resulting in a faster positive RUT reaction in the corpus were age ≥50 years (odds ratio [OR] = 1.84; 95% confidence interval [CI] = 1.10-3.08; p = .021) and severe gastric atrophy (OR = 2.41; 95% CI = 1.13-5.13; p = .023). Also, severe gastric atrophy was an independent factor associated with positive RUT reaction only in the corpus (OR = 5.12; 95% CI = 1.55-16.88; p = .007). CONCLUSIONS In subjects aged ≥50 years or with severe gastric atrophy, biopsy of the corpus mucosa optimized the efficiency of H. pylori detection through a faster positive RUT reaction.
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Affiliation(s)
- Jun-Hyung Cho
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - Seong Ran Jeon
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - Hyun Gun Kim
- a Digestive Disease Center , Soonchunhyang University Hospital , Seoul , Korea
| | - So-Young Jin
- b Department of Pathology , Soonchunhyang University Hospital , Seoul , Korea
| | - Suyeon Park
- c Department of Medical Biostatistics , Soonchunhyang University Hospital , Seoul , Korea
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Selgrad M, Tammer I, Langner C, Bornschein J, Meißle J, Kandulski A, Varbanova M, Wex T, Schlüter D, Malfertheiner P. Different antibiotic susceptibility between antrum and corpus of the stomach, a possible reason for treatment failure of Helicobacter pylori infection. World J Gastroenterol 2014; 20:16245-16251. [PMID: 25473179 PMCID: PMC4239513 DOI: 10.3748/wjg.v20.i43.16245] [Citation(s) in RCA: 59] [Impact Index Per Article: 5.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 11/14/2013] [Revised: 01/05/2014] [Accepted: 04/23/2014] [Indexed: 02/07/2023] Open
Abstract
AIM: To assess whether antibiotic resistance varies between the antrum and corpus of the stomach of patients that are either Helicobacter pylori (H. pylori) therapy-naive or pre-treated.
METHODS: H. pylori strains were isolated from antrum and corpus biopsies from 66 patients that received a diagnostic gastroduodenoscopy for variant clinical indications. Antimicrobial susceptibility to amoxicillin, clarithromycin, tetracycline, metronidazole, levofloxacin and rifabutin was tested with the E-test method on Iso-Sensitest agar with 10 vol% defibrinated horse blood. In patients with a different antibiotic susceptibility pattern between the isolates from the antrum and corpus, DNA fingerprinting via random amplified polymorphic DNA analysis was performed to detect differences among DNA patterns of H. pylori isolates.
RESULTS: Primary, secondary and tertiary resistance to clarithromycin was 6.9%, 53.8% and 83.3%, retrospectively. Metronidazole and levofloxacin resistance also increased according to the number of previous treatments (17.2%, 69.2%, 83.3%; 13.8%, 23.1%, 33.3%). Tertiary resistance to rifabutin was detected in 12.5% of patients. In none of the 66 patients a resistance against amoxicillin or tetracycline was detectable. Discordant antibiotic susceptibility between antrum and corpus isolates for different antibiotics was seen in 15.2% (10/66) of the patients. Two out of those ten patients were naive to any H. pylori antibiotic treatment. The remaining eight patients previously received at least one eradication therapy. DNA fingerprinting analysis revealed no substantial differences among DNA patterns between antrum and corpus isolates in the majority of patients suggesting an infection with a single H. pylori strain.
CONCLUSION: Different antibiotic susceptibility between antrum and corpus biopsies is a common phenomenon and a possible explanation for treatment failure. Resistant H. pylori strains may be missed if just one biopsy from one anatomic site of the stomach is taken for H. pylori susceptibility testing.
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Laine L, Sugg J, Suchower L, Neil G. Endoscopic biopsy requirements for post-treatment diagnosis of Helicobacter pylori. Gastrointest Endosc 2000; 51:664-9. [PMID: 10840297 DOI: 10.1067/mge.2000.105776] [Citation(s) in RCA: 13] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/10/2022]
Abstract
BACKGROUND Data on sensitivities of biopsy tests for Helicobacter pylori diagnosis after modern eradication therapy are limited. We assessed diagnostic yield of endoscopic biopsy tests before and after therapy in 2 U.S. multicenter double-blind trials of 10-day proton pump inhibitor-based triple therapy versus dual antibiotic therapy. METHODS Three hundred one patients with duodenal ulcer and H pylori infection had endoscopy at baseline and at 8 weeks. Four antral and 3 body biopsies were taken at both endoscopies: 1 antral biopsy for a rapid urease test (CLOtest), 2 antral and 2 body biopsies for histologic examination (Genta stain), and 1 antral and 1 body biopsy for culture. RESULTS The 2 same-site biopsies (antral or body) for histologic examination were in agreement in 97% of cases before treatment and 100% after triple therapy. Histologic examination of antral biopsies without body biopsies missed H pylori infection in 2% of patients before treatment and 5% after triple therapy. Posttreatment sensitivities for triple therapy were significantly lower than pretreatment sensitivities for all tests (e. g., 18% decrease in sensitivity in antral histology, 22% decrease in antral culture); decreases in sensitivity were greater after triple therapy than after the less effective dual therapy. CLOtest plus histology had a post-treatment sensitivity of 96% in the triple therapy group. CONCLUSIONS A single antral biopsy for histology provides excellent sensitivity for H pylori in untreated patients, but, after effective therapy, sensitivities of biopsy tests decrease. Use of more than one method of testing may increase diagnostic yield when assessing post-treatment H pylori status with endoscopy, whereas the addition of multiple biopsies for each type of test is of more limited value.
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Affiliation(s)
- L Laine
- USC School of Medicine, Los Angeles, California, and Astra Pharmaceuticals, Wayne, PA, USA
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Graham DY, Osato MS. Disinfection of biopsy forceps and culture of Helicobacter pylori from gastric mucosal biopsies. Am J Gastroenterol 1999; 94:1422-3. [PMID: 10235240 DOI: 10.1111/j.1572-0241.1999.01422.x] [Citation(s) in RCA: 9] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 12/11/2022]
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MacOni G, Vago L, Galletta G, Imbesi V, Sangaletti O, Parente F, Cucino C, Bonetto S, Bianchi Porro G. Is routine histological evaluation an accurate test for Helicobacter pylori infection? Aliment Pharmacol Ther 1999; 13:327-31. [PMID: 10102966 DOI: 10.1046/j.1365-2036.1999.00469.x] [Citation(s) in RCA: 26] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/13/2023]
Abstract
AIM To compare the diagnostic accuracy of routine histology for Helicobacter pylori infection, with histology by an expert pathologist, and to compare histology with the rapid urease test (RUT), 13C-urea breath test, IgG serology and culture of antrum and corpus specimens, in a consecutive series of untreated patients presenting for upper oesophago-gastro-duodenoscopy. MATERIALS AND METHODS One-hundred and fifteen consecutive patients underwent multiple tests for H. pylori infection: rapid urease test, 13C-urea breath test, IgG serology and histology and culture on antrum and corpus biopsy specimens. Histology was first evaluated by the pathologists in a routine examination, and then blindly reviewed by an expert pathologist with a special interest in gastrointestinal pathology. The patients were considered to be H. pylori-positive if two or more tests were positive. RESULTS Eighty-one patients (70.4%) were found to be H. pylori positive. 13C-urea breath test and IgG serology showed the best sensitivity and specificity (100%). Both the antral and body cultures, and the rapid urease test had the highest specificity (100%). Histological diagnosis after re-evaluation by an expert pathologist showed a high sensitivity (98. 8%) and specificity (100%), and was better than routine histology (sensitivity 92.6%; specificity 90.3%). The accuracy of the rapid urease test was greater than that of routine histology, and the combination of these two tests improved the sensitivity of H. pylori detection to up to 100%. CONCLUSION All diagnostic tests usually utilised in clinical practice have a sensitivity higher than 90%. In patients who were not pre-treated with antisecretory agents or antibiotics, the sensitivity of histological diagnosis, however, seems to be influenced by the accuracy of the histological examination. The sensitivity of routine histology, but not of revised histological diagnosis, is improved by an additional rapid urease test.
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Affiliation(s)
- G MacOni
- Department of Pathology, 'L. Sacco' University Hospital, Milan, Italy
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