The Efficacy of Moxifloxacin-containing Triple Therapy after Hybrid Therapy Failure in Helicobacter pylori Eradication

Soohoon Kwon; Dong Ho Lee; Jae Bin Kang; Nayoung Kim; Young Soo Park; Cheol Min Shin; Hyuk Yoon; Yoon Jin Choi

doi:10.4166/kjg.2017.70.2.72

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Kwon, Lee, Kang, Kim, Park, Shin, Yoon, and Choi: The Efficacy of Moxifloxacin-containing Triple Therapy after Hybrid Therapy Failure in Helicobacter pylori Eradication

Original Article

Korean J Gastroenterol 2017;70(2):72-80.

Published online: 4 October 2017

DOI: https://doi.org/10.4166/kjg.2017.70.2.72

The Efficacy of Moxifloxacin-containing Triple Therapy after Hybrid Therapy Failure in Helicobacter pylori Eradication

Soohoon Kwon¹, Dong Ho Lee^1,^2,, Jae Bin Kang¹, Nayoung Kim^1,², Young Soo Park^1,², Cheol Min Shin¹, Hyuk Yoon¹, Yoon Jin Choi¹

¹Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea

²Department of Internal Medicine and Liver Research Institute, Seoul National University College of Medicine, Seoul, Korea

Correspondence to: Dong Ho Lee, Department of Internal Medicine, Seoul National University Bundang Hospital, 82 Gumi-ro 173beon-gil, Bundang-gu, Seongnam 13620, Korea. Tel: +82-31-787-7008, Fax: +82-31-787-4051, E-mail: dhljohn@yahoo.co.kr

Received 21 February 2017 Accepted 22 March 2017

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background/Aims

Hybrid therapy was successful in eradicating Helicobacter pylori (H. pylori) according to previous reports. However, to the best of our knowledge, there have only been a few studies evaluating the optimal choice after hybrid failure. Hence, we aimed to evaluate the efficacy of moxifloxacin-containing triple therapy after hybrid therapy failure in H. pylori eradication.

Methods

Between January 2013 and March 2016, we retrospectively reviewed patients who underwent failed hybrid therapy, as first line treatment, in eradicating H. pylori (rabeprazole and amoxicillin b.i.d for 14 days, in addition to clarithromycin and metronidazole b.i.d for final 7 days). Then, we investigated the eradication rates of moxifloxacin-containing triple therapy (rabeprazole, amoxicillin b.i.d and moxifloxacin qd) as the second line of treatment. Intention-to-treat (ITT) and per-protocol (PP) analyses were used to determine the eradication rate. We evaluated the status of H. pylori by using ¹³ C-urea breath test 6 weeks after the final treatment. Moreover, compliance and adverse effects of each patient were analyzed.

Results

Among those who failed the initial hybrid therapy, 11 patients received moxifloxacin-containing triple therapy. The overall eradication rates, as determined by ITT and PP, were 72.7% (n=8/11) and 80% (n=8/10), respectively. The compliance rate was 100%, and there were no serious adverse effects.

Conclusions

Moxifloxacin-containing triple therapy can be used as a second line therapy in case of hybrid therapy failure. A large scale study is necessary to confirm the findings of this study and establish clinical evidence.

Keywords: Helicobacter pylori, Therapy, Hybrid, Moxifloxacin

References

1. Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med. 2002; 347:1175–1186.

2. Kim JH, Kim HY, Kim NY, et al. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol. 2001; 16:969–975.

3. Yim JY, Kim N, Choi SH, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter. 2007; 12:333–340.

4. Lim SH, Kwon JW, Kim N, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol. 2013; 13:104.

5. Lee JY, Kim N. Future trends of Helicobacter pylori eradication therapy in Korea. Korean J Gastroenterol. 2014; 63:158–170.

6. Jung KW, Won YJ, Kong HJ, et al. Cancer statistics in Korea: abdominal, mortality, survival, and prevalence in 2012. Cancer Res Treat. 2015; 47:127–141.

7. Kim SG, Jung HK, Lee HL, et al. Guidelines for the diagnosis and treatment of Helicobacter pylori infection in Korea, 2013 revised edition. Korean J Gastroenterol. 2013; 62:3–26.

8. Graham DY, Shiotani A. New concepts of resistance in the abdominal of Helicobacter pylori infections. Nat Clin Pract Gastroenterol Hepatol. 2008; 5:321–331.

9. Gumurdulu Y, Serin E, Ozer B, et al. Low eradication rate of Helicobacter pylori with triple 7–14 days and quadriple therapy in Turkey. World J Gastroenterol. 2004; 10:668–671.

10. De Francesco V, Margiotta M, Zullo A, et al. Prevalence of primary clarithromycin resistance in Helicobacter pylori strains over a 15 year period in Italy. J Antimicrob Chemother. 2007; 59:783–785.

11. Kim SE, Park MI, Park SJ, et al. Trends in Helicobacter pylori abdominal rates by first-line triple therapy and related factors in abdominal therapy. Korean J Intern Med. 2015; 30:801–807.

12. Hsu PI, Wu DC, Wu JY, Graham DY. Modified sequential Helicobacter pylori therapy: proton pump inhibitor and amoxicillin for 14 days with clarithromycin and metronidazole added as a quadruple (hybrid) therapy for the final 7 days. Helicobacter. 2011; 16:139–145.

13. Hsu PI, Lin PC, Graham DY. Hybrid therapy for Helicobacter pylori infection: a systemic review and metaanalysis. World J Gastroenterol. 2015; 21:12954–12962.

14. Bago P, Vcev A, Tomic M, Rozankovic M, Marusić M, Bago J. High eradication rate of H. pylori with moxifloxacin-based treatment: a randomized controlled trial. Wien Klin Wochenschr. 2007; 119:372–378.

15. Cheon JH, Kim N, Lee DH, et al. Efficacy of moxifloxacin-based triple therapy as second-line treatment for Helicobacter pylori infection. Helicobacter. 2006; 11:46–51.

16. Bago J, Pevec B, Tomić M, Marusić M, Bakula V, Bago P. Second-line treatment for Helicobacter pylori infection based on moxifloxacin triple therapy: a randomized controlled trial. Wien Klin Wochenschr. 2009; 121:47–52.

17. Hwang JJ, Lee DH, Lee AR, et al. Efficacy of 14-d vs 7-d moxi-floxacin-based triple regimens for second-line Helicobacter abdominal eradication. World J Gastroenterol. 2015; 21:5568–5574.

18. Lee JY, Kim N, Kim MS, et al. Factors affecting first-line triple abdominal of Helicobacter pylori including CYP2C19 genotype and abdominal resistance. Dig Dis Sci. 2014; 59:1235–1243.

19. Chuah SK, Tsay FW, Hsu PI, Wu DC. A new look at anti-Helicobacter pylori therapy. World J Gastroenterol. 2011; 17:3971–3975.

20. Perri F, Villani MR, Festa V, Quitadamo M, Andriulli A. Predictors of failure of Helicobacter pylori eradication with the standard ‘Maastricht triple therapy’. Aliment Pharmacol Ther. 2001; 15:1023–1029.

21. Basu PP, Rayapudi K, Pacana T, Shah NJ, Krishnaswamy N, Flynn M. A randomized study comparing levofloxacin, omeprazole, ni-tazoxanide, and doxycycline versus triple therapy for the abdominal of Helicobacter pylori. Am J Gastroenterol. 2011; 106:1970–1975.

22. Oh HS, Lee DH, Seo JY, et al. Ten-day sequential therapy is more effective than proton pump inhibitor-based therapy in Korea: a prospective, randomized study. J Gastroenterol Hepatol. 2012; 27:504–509.

23. Nishizawa T, Suzuki H, Suzuki M, Takahashi M, Hibi T. Proton pump inhibitor-amoxicillin-clarithromycin versus proton pump inhibitor-amoxicillin-metronidazole as first-line Helicobacter abdominal eradication therapy. J Clin Biochem Nutr. 2012; 51:114–116.

24. Boyanova L, Mitov I. Geographic map and evolution of primary Helicobacter pylori resistance to antibacterial agents. Expert Rev Anti Infect Ther. 2010; 8:59–70.

25. Lee JW, Kim N, Kim JM, et al. Prevalence of primary and abdominal antimicrobial resistance of Helicobacter pylori in Korea from 2003 through 2012. Helicobacter. 2013; 18:206–214.

26. Houben MH, van de Beek D, Hensen EF, de Craen AJ, Rauws EA, Tytgat GN. A systematic review of Helicobacter pylori eradication therapy–the impact of antimicrobial resistance on eradication rates. Aliment Pharmacol Ther. 1999; 13:1047–1055.

27. Hwang TJ, Kim N, Kim HB, et al. Change in antibiotic resistance of Helicobacter pylori strains and the effect of A2143G point abdominal of 23S rRNA on the eradication of H. pylori in a single center of Korea. J Clin Gastroenterol. 2010; 44:536–543.

28. Gong EJ, Yun SC, Jung HY, et al. Meta-analysis of first-line triple therapy for helicobacter pylori eradication in Korea: is it time to change? J Korean Med Sci. 2014; 29:704–713.

29. Current European concepts in the management of Helicobacter pylori infection. The Maastricht consensus report. European Helicobacter Pylori Study Group. Gut. 1997; 41:8–13.

30. Jafri NS, Hornung CA, Howden CW. Meta-analysis: sequential therapy appears superior to standard therapy for Helicobacter pylori infection in patients naive to treatment. Ann Intern Med. 2008; 148:923–931.

31. Zullo A, De Francesco V, Hassan C, Morini S, Vaira D. The abdominal therapy regimen for Helicobacter pylori eradication: a pooled-data analysis. Gut. 2007; 56:1353–1357.

32. Vakil N, Vaira D. Treatment for H. pylori infection: new challenges with antimicrobial resistance. J Clin Gastroenterol. 2013; 47:383–388.

33. Suzuki T, Matsuo K, Ito H, et al. Smoking increases the treatment failure for Helicobacter pylori eradication. Am J Med. 2006; 119:217–224.

34. Essa AS, Kramer JR, Graham DY, Treiber G. Meta-analysis: four-drug, three-antibiotic, non-bismuth-containing "concomitant therapy" versus triple therapy for Helicobacter pylori eradication. Helicobacter. 2009; 14:109–118.

35. McNicholl AG, Marin AC, Molina-Infante J, et al. Randomised abdominal trial comparing sequential and concomitant therapies for Helicobacter pylori eradication in routine clinical practice. Gut. 2014; 63:244–249.

36. Huang YK, Wu MC, Wang SS, et al. Lansoprazole-based abdominal and concomitant therapy for the first-line Helicobacter pylori eradication. J Dig Dis. 2012; 13:232–238.

37. Wu DC, Hsu PI, Wu JY, et al. Sequential and concomitant therapy with four drugs is equally effective for eradication of H pylori infection. Clin Gastroenterol Hepatol. 2010; 8:36–41.e1.

38. Graham DY, Lee YC, Wu MS. Rational Helicobacter pylori therapy: evidencebased medicine rather than medicine-based evidence. Clin Gastroenterol Hepatol. 2014; 12:177–186.e3; Discussion e12-e13.

39. Hsu PI, Wu DC, Chen WC, et al. Randomized controlled trial abdominal 7-day triple, 10-day sequential, and 7-day concomitant therapies for Helicobacter pylori infection. Antimicrob Agents Chemother. 2014; 58:5936–5942.

40. Liou JM, Chen CC, Chen MJ, et al. Sequential versus triple therapy for the first-line treatment of Helicobacter pylori: a multicentre, open-label, randomised trial. Lancet. 2013; 381:205–213.

41. Wu JY, Hsu PI, Wu DC, Graham DY, Wang WM. Feasibility of abdominal 14-day hybrid therapy while maintaining an excellent Helicobacter pylori eradication rate. Helicobacter. 2014; 19:207–213.

42. Sardarian H, Fakheri H, Hosseini V, Taghvaei T, Maleki I, Mokhtare M. Comparison of hybrid and sequential therapies for Helicobacter pylori eradication in Iran: a prospective randomized trial. Helicobacter. 2013; 18:129–134.

43. Zullo A, Scaccianoce G, De Francesco V, et al. Concomitant, abdominal, and hybrid therapy for H. pylori eradication: a pilot study. Clin Res Hepatol Gastroenterol. 2013; 37:647–650.

44. De Francesco V, Hassan C, Ridola L, Giorgio F, Ierardi E, Zullo A. Sequential, concomitant and hybrid first-line therapies for Helicobacter pylori eradication: a prospective randomized study. J Med Microbiol. 2014; 63(Pt 5):748–752.

45. Oh DH, Lee DH, Kang KK, et al. Efficacy of hybrid therapy as first-line regimen for Helicobacter pylori infection compared with sequential therapy. J Gastroenterol Hepatol. 2014; 29:1171–1176.

46. Molina-Infante J, Romano M, Fernandez-Bermejo M, et al. Optimized nonbismuth quadruple therapies cure most patients with Helicobacter pylori infection in populations with high rates of abdominal resistance. Gastroenterology. 2013; 145:121–128.e1.

47. Hojo M, Miwa H, Nagahara A, Sato N. Pooled analysis on the abdominal of the second-line treatment regimens for Helicobacter abdominal infection. Scand J Gastroenterol. 2001; 36:690–700.

48. Gisbert JP, Pajares JM. Review article: Helicobacter pylori "rescue" regimen when proton pump inhibitor-based triple therapies fail. Aliment Pharmacol Ther. 2002; 16:1047–1057.

49. Kim JM, Kim JS, Kim N, Kim SG, Jung HC, Song IS. Comparison of primary and secondary antimicrobial minimum inhibitory abdominal for Helicobacter pylori isolated from Korean patients. Int J Antimicrob Agents. 2006; 28:6–13.

50. Keating GM, Scott LJ. Moxifloxacin: a review of its use in the abdominal of bacterial infections. Drugs. 2004; 64:2347–2377.

51. Edlund C, Beyer G, Hiemer-Bau M, Ziege S, Lode H, Nord CE. Comparative effects of moxifloxacin and clarithromycin on the normal intestinal microflora. Scand J Infect Dis. 2000; 32:81–85.

52. Kang JM, Kim N, Lee DH, et al. Second-line treatment for Helicobacter pylori infection: 10-day moxifloxacin-based triple therapy versus 2-week quadruple therapy. Helicobacter. 2007; 12:623–628.

53. Wu C, Chen X, Liu J, Li MY, Zhang ZQ, Wang ZQ. Moxifloxacin-containing triple therapy versus bismuth-containing quadruple abdominal for second-line treatment of Helicobacter pylori infection: a metaanalysis. Helicobacter. 2011; 16:131–138.

54. Kang KK, Lee DH, Oh DH, et al. Helicobacter pylori eradication with moxifloxacin-containing therapy following failed first-line therapies in South Korea. World J Gastroenterol. 2014; 20:6932–6938.

55. Malfertheiner P, Megraud F, O'Morain CA, et al. Management of Helicobacter pylori infection–the Maastricht IV/ Florence abdominal report. Gut. 2012; 61:646–664.

Fig. 1.

Eradication rates of the overall and 14-days moxifloxacin-containing triple therapy as the second line therapy after hybrid therapy failure. It is presented by intention-to-treat (ITT) and per-protocol (PP) analyses.

Table 1.

Baseline Characteristics of Enrolled Patients

Patient number	Sex	Age	Alcohol	Current smoker	Underlying diseases	EGD findings	Time intervals (days)^a	Treatment duration (days)^b	Treatment results ^b	Compliance ^b	Adverse events^b
1	F	66	No	No	Osteoporosis	Gastritis	47	14	Eradicated	100%	None
2	F	71	No	No	HTN	Gastritis	84	7	Eradicated	100%	None
3	M	63	Yes	No	DM/HTN	Gastritis	129	14	Eradicated	100%	None
4	M	46	Yes	Yes	None	Gastric ulcer	97	14	Eradicated	100%	None
5	M	62	Yes	No	DM/HTN	Gastritis	46	14	Eradicated	100%	None
6	F	75	No	No	None	Gastritis	53	14	Eradicated	100%	None
7	M	64	Yes	No	DM/ALD	Gastritis	102	14	Follow up loss
8	F	60	No	No	None	Gastritis	61	14	Not eradicated	100%	None
9	M	67	No	No	HTN/BPH	Not done	45	14	Not eradicated	100%	None
10	F	66	No	No	None	Duodenal ulcer	41	14	Eradicated	100%	Loose stool
11	F	57	No	No	None	Gastritis	399	14	Eradicated	100%	None

EGD, esophagogastroduodenoscopy; F, female; M, male; HTN, hypertension; DM, diabetes mellitus; ALD, alcoholic liver disease; BPH, benign prostate hyperplasia.

^a Time intervals between first and second treatment; ^b Moxifloxacin-containing triple therapy.

Table 2.

Comparison of Eradicated and Not Eradicated Groups

Variable	Total (n=11)	Eradicated (n=8)	Not eradicated (n=2)	p-value
Age	63.36±2.28	63.25±3.13	63.50±3.5	0.971
Sex				0.491
Male	5 (45.5)	3 (37.5)	1 (50)
Female	6 (54.5)	5 (62.5)	1 (50)
Current smoker	1 (9.1)	1 (12.5)	0	0.814
Alcohol consumption	4 (36.4)	3 (27.5)	0	0.235
EGD findings				0.481
Gastritis	8 (72.7)	6 (75)	1 (50)
Gastric ulcer	1 (9.1)	1 (12.5)	0
Duodenal ulcer	1 (9.1)	1 (12.5)	0
None^a	1 (9.1)	0	1 (50)
Underlying diseases				0.179
DM	3 (27.3)	3 (37.5)	0	0.461
HTN	4 (36.4)	3 (37.5)	1 (50)	0.692
Osteoporosis	1 (9.1)	1 (12.5)	0	0.814
BPH	1 (9.1)	0	1 (50)	0.084
ALD	1 (9.1)	1 (12.5)	0	0.814
Time intervals (days)^b	100±31.11	112±42.42	53±8	0.525
Treatment duration (days)^c
7	1 (9.1)	1 (100)
14	9 (81.8)	7 (77.8)	2 (22.2)	0.814
Adverse events^c
Loose stool	1 (9.1)	1 (100)

Values are presented as mean±standard deviation or n (%).

EGD, esophagogastroduodenoscopy; DM, diabetes mellitus; HTN, hypertension; BPH, benign prostate hyperplasia; ALD, alcoholic liver disease.

^a Performed only ¹³ C-UBT, because examed esophagogastroduodenoscopy in other hospital

^b Time intervals between first and second treatment; ^c Moxifloxacin-containing triple therapy.

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