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Published in: BMC Infectious Diseases 1/2023

Open Access 01-12-2023 | Levofloxacin | Research

Helicobacter pylori eradication rates using clarithromycin and levofloxacin-based regimens in patients with previous COVID-19 treatment: a randomized clinical trial

Authors: Ahmed Kamal, Ramy Mohamed Ghazy, Dalia Sherief, Aliaa Ismail, Walid Ismail Ellakany

Published in: BMC Infectious Diseases | Issue 1/2023

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Abstract

Background

Helicobacter pylori (H. pylori) is affecting half of the globe. It is considered a main causative organism of chronic gastritis, peptic ulcer disease, and different gastric maliganacies. It has been also correlated to extraintestinal diseases, including refractory iron deficiency anaemia, vitamin B12 deficiency, and immune thrombocytopenic purpura. The misuse of antibiotics during the coronavirus diseases 2019 (COVID-19) pandemic time can affect H. pylori eradication rates. Our aim was to compare the efficacy of clarithromycin versus levofloxacin-based regimens for H. pylori treatment in naïve patients after the COVID-19 pandemic misuse of antibiotics.

Methods

A total of 270 naïve H. pylori infected patients with previous treatment for COVID-19 more than 3 months before enrolment were recruited. Patients were randomized to receive either clarithromycin, esomeprazole, and amoxicillin, or levofloxacin, esomeprazole, and amoxicillin.

Results

A total of 270 naïve H. pylori infected patients with previous treatment for COVID-19 more than 3 months before enrolment were included, 135 in each arm. In total, 19 patients in the clarithromycin group and 18 patients in the levofloxacin group stopped treatment after 2–4 days because of side effects or were lost for follow-up. Finally, 116 subjects in the clarithromycin group and 117 in the levofloxacin group were assessed. The eradication rates in intention to treat (ITT) and per protocol (PP) analyses were: group I, 55.56% and 64.66%; and Group II, 64.44% and 74.36% respectively (p = 0.11).

Conclusion

As COVID-19 pandemic has moved forward fast, high resistance rates of H. pylori to both clarithromycin and levofloxacin were developed after less than two years from the start of the pandemic. Molecular & genetic testing is highly recommended to identify antimicrobial resistance patterns. Strategies to prevent antibiotic misuse in the treatment of COVID-19 are needed to prevent more antibiotic resistance.
Trial Registration: The trial was registered on Clinicaltrials.gov NCT05035186. Date of registration is 2-09-2021.
Literature
1.
go back to reference Huang Y, Wang Q-l, Cheng D-d, Xu W-T, Lu N-H. Adhesion and Invasion of gastric mucosa epithelial cells by Helicobacter pylori. Front Cell Infect Microbiol. 2016;6:159.CrossRef Huang Y, Wang Q-l, Cheng D-d, Xu W-T, Lu N-H. Adhesion and Invasion of gastric mucosa epithelial cells by Helicobacter pylori. Front Cell Infect Microbiol. 2016;6:159.CrossRef
2.
go back to reference Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Off J Am Coll Gastroenterology|ACG. 2017;112:212–39. Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG clinical guideline: treatment of Helicobacter pylori infection. Off J Am Coll Gastroenterology|ACG. 2017;112:212–39.
3.
go back to reference Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): european society of gastrointestinal endoscopy (ESGE), european Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy. 2019;51:365–88.CrossRef Pimentel-Nunes P, Libânio D, Marcos-Pinto R, Areia M, Leja M, Esposito G, et al. Management of epithelial precancerous conditions and lesions in the stomach (MAPS II): european society of gastrointestinal endoscopy (ESGE), european Helicobacter and Microbiota Study Group (EHMSG), European Society of Pathology (ESP), and Sociedade Portuguesa de Endoscopia Digestiva (SPED) guideline update 2019. Endoscopy. 2019;51:365–88.CrossRef
4.
go back to reference Banić M, Franceschi F, Babić Z, Gasbarrini A. Extragastric manifestations of Helicobacter pylori Infection. Helicobacter. 2012;17:49–55.CrossRef Banić M, Franceschi F, Babić Z, Gasbarrini A. Extragastric manifestations of Helicobacter pylori Infection. Helicobacter. 2012;17:49–55.CrossRef
5.
go back to reference Bilardi C, Dulbecco P, Zentilin P, Reglioni S, Iiritano E, Parodi A, et al. A 10-day levofloxacin-based therapy in patients with resistant Helicobacter pylori infection: a controlled trial. Clin Gastroenterol Hepatol. 2004;2:997–1002.CrossRef Bilardi C, Dulbecco P, Zentilin P, Reglioni S, Iiritano E, Parodi A, et al. A 10-day levofloxacin-based therapy in patients with resistant Helicobacter pylori infection: a controlled trial. Clin Gastroenterol Hepatol. 2004;2:997–1002.CrossRef
6.
go back to reference Peedikayil MC, AlSohaibani FI, Alkhenizan AH. Levofloxacin-based first-line therapy versus Standard First-Line therapy for Helicobacter pylori eradication: meta-analysis of randomized controlled trials. PLoS ONE. 2014;9:e85620.CrossRef Peedikayil MC, AlSohaibani FI, Alkhenizan AH. Levofloxacin-based first-line therapy versus Standard First-Line therapy for Helicobacter pylori eradication: meta-analysis of randomized controlled trials. PLoS ONE. 2014;9:e85620.CrossRef
7.
go back to reference O’Connor JPA, Taneike I, O’Morain C, Review. Improving compliance with Helicobacter pylori eradication therapy: when and how? Therap Adv Gastroenterol. 2009;273–9. O’Connor JPA, Taneike I, O’Morain C, Review. Improving compliance with Helicobacter pylori eradication therapy: when and how? Therap Adv Gastroenterol. 2009;273–9.
8.
go back to reference Li J, Deng J, Wang Z, Li H, Wan C. Antibiotic resistance of Helicobacter pylori strains isolated from pediatric patients in Southwest China. Front Microbiol. 2021;11:621791.CrossRef Li J, Deng J, Wang Z, Li H, Wan C. Antibiotic resistance of Helicobacter pylori strains isolated from pediatric patients in Southwest China. Front Microbiol. 2021;11:621791.CrossRef
9.
go back to reference Megraud F, Coenen S, Versporten A, Kist M, Lopez-Brea M, Hirschl AM, et al. Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut. 2013;62:34–42.CrossRef Megraud F, Coenen S, Versporten A, Kist M, Lopez-Brea M, Hirschl AM, et al. Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption. Gut. 2013;62:34–42.CrossRef
10.
go back to reference Butler CC, Dorward J, Yu L-M, Gbinigie O, Hayward G, Saville BR, et al. Azithromycin for community treatment of suspected COVID-19 in people at increased risk of an adverse clinical course in the UK (PRINCIPLE): a randomised, controlled, open-label, adaptive platform trial. Lancet. 2021;397:1063–74.CrossRef Butler CC, Dorward J, Yu L-M, Gbinigie O, Hayward G, Saville BR, et al. Azithromycin for community treatment of suspected COVID-19 in people at increased risk of an adverse clinical course in the UK (PRINCIPLE): a randomised, controlled, open-label, adaptive platform trial. Lancet. 2021;397:1063–74.CrossRef
11.
go back to reference Min J-Y, Jang YJ. Macrolide therapy in respiratory viral infections. Mediators Inflamm. 2012;2012:e649570.CrossRef Min J-Y, Jang YJ. Macrolide therapy in respiratory viral infections. Mediators Inflamm. 2012;2012:e649570.CrossRef
12.
go back to reference Taylor L. Covid-19: antimicrobial misuse in Americas sees drug resistant infections surge, says WHO. BMJ. 2021;375:n2845. Taylor L. Covid-19: antimicrobial misuse in Americas sees drug resistant infections surge, says WHO. BMJ. 2021;375:n2845.
13.
go back to reference Elsayed AA, Darwish SF, Zewail MB, Mohammed M, Saeed H, Rabea H. Antibiotic misuse and compliance with infection control measures during COVID-19 pandemic in community pharmacies in Egypt. Int J Clin Pract. 2021;75:e14081.CrossRef Elsayed AA, Darwish SF, Zewail MB, Mohammed M, Saeed H, Rabea H. Antibiotic misuse and compliance with infection control measures during COVID-19 pandemic in community pharmacies in Egypt. Int J Clin Pract. 2021;75:e14081.CrossRef
14.
go back to reference Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SS, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015;21:11221–35.CrossRef Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SS, et al. Diagnosis of Helicobacter pylori infection: current options and developments. World J Gastroenterol. 2015;21:11221–35.CrossRef
15.
go back to reference Ierardi E, Losurdo G, Fortezza RFL, Principi M, Barone M, Leo AD. Optimizing proton pump inhibitors in Helicobacter pylori treatment: old and new tricks to improve effectiveness. World J Gastroenterol. 2019;25:5097–104.CrossRef Ierardi E, Losurdo G, Fortezza RFL, Principi M, Barone M, Leo AD. Optimizing proton pump inhibitors in Helicobacter pylori treatment: old and new tricks to improve effectiveness. World J Gastroenterol. 2019;25:5097–104.CrossRef
16.
go back to reference Hafeez M, Qureshi ZA, Khattak AL, Saeed F, Asghar A, Azam K, et al. Helicobacter Pylori eradication therapy: still a challenge. Cureus. 2021;13:e14872. Hafeez M, Qureshi ZA, Khattak AL, Saeed F, Asghar A, Azam K, et al. Helicobacter Pylori eradication therapy: still a challenge. Cureus. 2021;13:e14872.
17.
go back to reference Peterson WL, Fendrick AM, Cave DR, Peura DA, Garabedian-Ruffalo SM, Laine L. Helicobacter pylori-related disease: guidelines for testing and treatment. Arch Intern Med. 2000;160:1285–91.CrossRef Peterson WL, Fendrick AM, Cave DR, Peura DA, Garabedian-Ruffalo SM, Laine L. Helicobacter pylori-related disease: guidelines for testing and treatment. Arch Intern Med. 2000;160:1285–91.CrossRef
18.
go back to reference Nayar DS. Current eradication rate of Helicobacter pylori with clarithromycin-based triple therapy in a gastroenterology practice in the New York metropolitan area. Infect Drug Resist. 2018;11:205–11.CrossRef Nayar DS. Current eradication rate of Helicobacter pylori with clarithromycin-based triple therapy in a gastroenterology practice in the New York metropolitan area. Infect Drug Resist. 2018;11:205–11.CrossRef
19.
go back to reference Yuan Y, Ford AC, Khan KJ, Gisbert JP, Forman D, Leontiadis GI, et al. Optimum duration of regimens for Helicobacter pylori eradication. Cochrane Database Syst Rev. 2013;2013:CD008337. Yuan Y, Ford AC, Khan KJ, Gisbert JP, Forman D, Leontiadis GI, et al. Optimum duration of regimens for Helicobacter pylori eradication. Cochrane Database Syst Rev. 2013;2013:CD008337.
20.
go back to reference Gatta L, Vakil N, Vaira D, Scarpignato C. Global eradication rates for Helicobacter pylori infection: systematic review and meta-analysis of sequential therapy. BMJ. 2013;347:f4587.CrossRef Gatta L, Vakil N, Vaira D, Scarpignato C. Global eradication rates for Helicobacter pylori infection: systematic review and meta-analysis of sequential therapy. BMJ. 2013;347:f4587.CrossRef
21.
go back to reference Azab ET, Thabit AK, McKee S, Al-Qiraiqiri A. Levofloxacin versus clarithromycin for Helicobacter pylori eradication: are 14 day regimens better than 10 day regimens? Gut Pathog. 2022;14:24.CrossRef Azab ET, Thabit AK, McKee S, Al-Qiraiqiri A. Levofloxacin versus clarithromycin for Helicobacter pylori eradication: are 14 day regimens better than 10 day regimens? Gut Pathog. 2022;14:24.CrossRef
22.
go back to reference Tai W-C, Chiu C-H, Liang C-M, Chang K-C, Kuo C-M, Chiu Y-C, et al. Ten-day versus 14-Day levofloxacin-containing triple therapy for second-line anti-Helicobacter pylori eradication in Taiwan. Gastroenterol Res Pract. 2013;2013:932478.CrossRef Tai W-C, Chiu C-H, Liang C-M, Chang K-C, Kuo C-M, Chiu Y-C, et al. Ten-day versus 14-Day levofloxacin-containing triple therapy for second-line anti-Helicobacter pylori eradication in Taiwan. Gastroenterol Res Pract. 2013;2013:932478.CrossRef
23.
go back to reference Elantouny NG, Abo Bakr AA, EL-Sokkary RH, Elshahat YE. Levofloxacin versus clarithromycin-based therapy for eradication of Helicobacter pylori infection: a comparative study. Zagazig Univ Med J. 2019;25:500–7.CrossRef Elantouny NG, Abo Bakr AA, EL-Sokkary RH, Elshahat YE. Levofloxacin versus clarithromycin-based therapy for eradication of Helicobacter pylori infection: a comparative study. Zagazig Univ Med J. 2019;25:500–7.CrossRef
24.
go back to reference Awad Y, Eldeeb M, Fathi M, Mahmoud N, Morsy R. Helicobacter pylori antibiotic resistance patterns among Egyptian children and predictors of resistance. QJM-Int J Med. 2020;113:hcaa063.021.CrossRef Awad Y, Eldeeb M, Fathi M, Mahmoud N, Morsy R. Helicobacter pylori antibiotic resistance patterns among Egyptian children and predictors of resistance. QJM-Int J Med. 2020;113:hcaa063.021.CrossRef
25.
go back to reference Ng YL, Salim CK, Chu JJH. Drug repurposing for COVID-19: approaches, challenges and promising candidates. Pharmacol Ther. 2021;228:23.CrossRef Ng YL, Salim CK, Chu JJH. Drug repurposing for COVID-19: approaches, challenges and promising candidates. Pharmacol Ther. 2021;228:23.CrossRef
26.
go back to reference Garg SK. Antibiotic misuse during COVID-19 pandemic: a recipe for disaster. Indian J Crit Care Med. 2021;25:617.CrossRef Garg SK. Antibiotic misuse during COVID-19 pandemic: a recipe for disaster. Indian J Crit Care Med. 2021;25:617.CrossRef
27.
go back to reference Nag VL, Kaur N. Superinfections in COVID-19 patients: role of antimicrobials. Dubai Med J. 2021;4:117–26.CrossRef Nag VL, Kaur N. Superinfections in COVID-19 patients: role of antimicrobials. Dubai Med J. 2021;4:117–26.CrossRef
28.
go back to reference Lai CC, Chen SY, Ko WC, Hsueh PR. Increased antimicrobial resistance during the COVID-19 pandemic. J Antimicrob Agents. 2021;57:106324.CrossRef Lai CC, Chen SY, Ko WC, Hsueh PR. Increased antimicrobial resistance during the COVID-19 pandemic. J Antimicrob Agents. 2021;57:106324.CrossRef
29.
go back to reference Fu Y, Yang Q, Xu M, Kong H, Chen H, Fu Y, et al. Secondary bacterial infections in critical Ill patients with Coronavirus Disease 2019. Open Forum Infect Dis. 2020;7:ofaa220.CrossRef Fu Y, Yang Q, Xu M, Kong H, Chen H, Fu Y, et al. Secondary bacterial infections in critical Ill patients with Coronavirus Disease 2019. Open Forum Infect Dis. 2020;7:ofaa220.CrossRef
30.
go back to reference Li J, Wang J, Yang Y, Cai P, Cao J, Cai X, et al. Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: a retrospective analysis. Antimicrob Resist Infect Control. 2020;9:153.CrossRef Li J, Wang J, Yang Y, Cai P, Cao J, Cai X, et al. Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: a retrospective analysis. Antimicrob Resist Infect Control. 2020;9:153.CrossRef
31.
go back to reference Flores-Treviño S, Mendoza-Olazarán S, Bocanegra-Ibarias P, Maldonado-Garza HJ, Garza-González E. Helicobacter pylori drug resistance: therapy changes and challenges. Expert Rev Gastroenterol Hepatol. 2018;12:819–27.CrossRef Flores-Treviño S, Mendoza-Olazarán S, Bocanegra-Ibarias P, Maldonado-Garza HJ, Garza-González E. Helicobacter pylori drug resistance: therapy changes and challenges. Expert Rev Gastroenterol Hepatol. 2018;12:819–27.CrossRef
32.
go back to reference Yacouba A, Olowo-Okere A, Yunusa I. Repurposing of antibiotics for clinical management of COVID-19: a narrative review. Ann Clin Microbiol. 2021;20:1–8. Yacouba A, Olowo-Okere A, Yunusa I. Repurposing of antibiotics for clinical management of COVID-19: a narrative review. Ann Clin Microbiol. 2021;20:1–8.
33.
go back to reference Bleyzac N, Goutelle S, Bourguignon L, Tod M. Azithromycin for COVID-19: more than just an Antimicrobial? Clin Drug Investig. 2020;40:683–6.CrossRef Bleyzac N, Goutelle S, Bourguignon L, Tod M. Azithromycin for COVID-19: more than just an Antimicrobial? Clin Drug Investig. 2020;40:683–6.CrossRef
34.
go back to reference Fass R. Erythromycin, clarithromycin, and azithromycin: use of frequency distribution curves, scattergrams, and regression analyses to compare in vitro activities and describe cross-resistance. Antimicrob Agents Chemother. 1993;37:2080–6.CrossRef Fass R. Erythromycin, clarithromycin, and azithromycin: use of frequency distribution curves, scattergrams, and regression analyses to compare in vitro activities and describe cross-resistance. Antimicrob Agents Chemother. 1993;37:2080–6.CrossRef
35.
go back to reference Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance from biology to clinical implications. Nat Rev Gastroenterol Hepatol. 2021;18:613–29.CrossRef Tshibangu-Kabamba E, Yamaoka Y. Helicobacter pylori infection and antibiotic resistance from biology to clinical implications. Nat Rev Gastroenterol Hepatol. 2021;18:613–29.CrossRef
36.
go back to reference Karampela I, Dalamaga M. Could respiratory Fluoroquinolones, Levofloxacin and Moxifloxacin, prove to be beneficial as an Adjunct Treatment in COVID-19? Arch Med Res. 2020;51:741–2.CrossRef Karampela I, Dalamaga M. Could respiratory Fluoroquinolones, Levofloxacin and Moxifloxacin, prove to be beneficial as an Adjunct Treatment in COVID-19? Arch Med Res. 2020;51:741–2.CrossRef
37.
go back to reference Alboraie M, Elhossary W, Aly OA, Abbas B, Abdelsalam L, Ghaith D, et al. Egyptian recommendations for management of Helicobacter pylori infection: 2018 report. Arab J Gastroenterol. 2019;20:175–9.CrossRef Alboraie M, Elhossary W, Aly OA, Abbas B, Abdelsalam L, Ghaith D, et al. Egyptian recommendations for management of Helicobacter pylori infection: 2018 report. Arab J Gastroenterol. 2019;20:175–9.CrossRef
38.
go back to reference Malfertheiner P, Megraud F, O’morain C, Gisbert J, Kuipers E, Axon A, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017;66:6–30.CrossRef Malfertheiner P, Megraud F, O’morain C, Gisbert J, Kuipers E, Axon A, et al. Management of Helicobacter pylori infection—the Maastricht V/Florence consensus report. Gut. 2017;66:6–30.CrossRef
39.
go back to reference Shah SC, Iyer PG, Moss SF. AGA clinical practice update on the management of refractory Helicobacter pylori infection: expert review. Gastroenterology. 2021;160:1831–41.CrossRef Shah SC, Iyer PG, Moss SF. AGA clinical practice update on the management of refractory Helicobacter pylori infection: expert review. Gastroenterology. 2021;160:1831–41.CrossRef
40.
go back to reference Taha SHN, Moawad AM, Ghazy RM, Abdelhalim WA. Assessment of self-treatment knowledge, beliefs and practice during COVID-19 pandemic among Egyptian population: a cross sectional study. Egypt J Hosp Med. 2022;89:4516–25.CrossRef Taha SHN, Moawad AM, Ghazy RM, Abdelhalim WA. Assessment of self-treatment knowledge, beliefs and practice during COVID-19 pandemic among Egyptian population: a cross sectional study. Egypt J Hosp Med. 2022;89:4516–25.CrossRef
41.
go back to reference Kazemi S, Tavakkoli H, Habizadeh MR, Emami MH. Diagnostic values of Helicobacter pylori diagnostic tests: stool antigen test, urea breath test, rapid urease test, serology and histology. J Res Med Sci. 2011;16:1097–104. Kazemi S, Tavakkoli H, Habizadeh MR, Emami MH. Diagnostic values of Helicobacter pylori diagnostic tests: stool antigen test, urea breath test, rapid urease test, serology and histology. J Res Med Sci. 2011;16:1097–104.
42.
go back to reference Redéen S, Petersson F, Törnkrantz E, Levander H, Mårdh E, Borch K. Reliability of diagnostic tests for Helicobacter pylori infection. Gastroenterol Res Pract. 2011;2011:940650.CrossRef Redéen S, Petersson F, Törnkrantz E, Levander H, Mårdh E, Borch K. Reliability of diagnostic tests for Helicobacter pylori infection. Gastroenterol Res Pract. 2011;2011:940650.CrossRef
Metadata
Title
Helicobacter pylori eradication rates using clarithromycin and levofloxacin-based regimens in patients with previous COVID-19 treatment: a randomized clinical trial
Authors
Ahmed Kamal
Ramy Mohamed Ghazy
Dalia Sherief
Aliaa Ismail
Walid Ismail Ellakany
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2023
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-023-07993-8

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