Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2017, Article ID 5430723, 9 pages
https://doi.org/10.1155/2017/5430723
Research Article

Helicobacter pylori from Peptic Ulcer Patients in Uganda Is Highly Resistant to Clarithromycin and Fluoroquinolones: Results of the GenoType HelicoDR Test Directly Applied on Stool

1Department of Medical Microbiology, Makerere University College of Health Sciences, P.O. Box 7072, Kampala, Uganda
2Department of Midwifery, Faculty of Health Sciences, Lira University, P.O. Box 1035, Lira, Uganda
3Department of Medicine, Makerere University College of Health Sciences, P.O. Box 7072, Kampala, Uganda
4MBN Clinical Laboratories, Plot 28 Nakasero Road, Kampala, Uganda

Correspondence should be addressed to Freddie Bwanga; ude.esac@81bxf

Received 30 September 2016; Revised 13 January 2017; Accepted 13 February 2017; Published 7 May 2017

Academic Editor: Frederick Adzitey

Copyright © 2017 Denish Calmax Angol et al. 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.

Linked References

  1. R. J. Owen, “Helicobacter—species classification and identification,” British Medical Bulletin, vol. 54, no. 1, pp. 17–30, 1998. View at Publisher · View at Google Scholar · View at Scopus
  2. R. N. Ndip, A. E. Malange Takang, J. E. A. Ojongokpoko et al., “Helicobacter pylori isolates recovered from gastric biopsies of patients with gastro-duodenal pathologies in Cameroon: current status of antibiogram,” Tropical Medicine and International Health, vol. 13, no. 6, pp. 848–854, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. N. F. Tanih, L. M. Ndip, A. M. Clarke, and R. N. Ndip, “An overview of pathogenesis and epidemiology of helicobacter pylori infection,” African Journal of Microbiology Research, vol. 4, no. 6, pp. 426–436, 2010. View at Google Scholar · View at Scopus
  4. C. Vu and Y. Y. Ng, “Prevalence of Helicobacter pylori in Peptic Ulcer Disease in a Singapore Hospital,” Singapore Medical Journal, vol. 41, no. 10, pp. 478–481, 2000. View at Google Scholar
  5. C. S. Goodwin, M. M. Mendall, and T. C. Northfield, “Helicobacter pylori infection,” Lancet, vol. 349, no. 9047, pp. 265–269, 1997. View at Publisher · View at Google Scholar · View at Scopus
  6. M. Go, “Natural history and epidemiology of Helicobacter pylori infection,” Alimentary Pharmacology & Therapeutics, vol. 16, pp. 3–15, 2002. View at Google Scholar
  7. J. G. Kusters, A. H. M. 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 · View at Google Scholar · View at Scopus
  8. D. Asrat, I. Nilsson, Y. Mengistu et al., “Prevalence of Helicobacter pylori infection among adult dyspeptic patients in Ethiopia,” Annals of Tropical Medicine and Parasitology, vol. 98, no. 2, pp. 181–189, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. R. N. Ndip, A. E. Malange, J. F. T. Akoachere, W. G. Mackay, V. P. K. Titanji, and L. T. Weaver, “Helicobacter pylori antigens in the faeces of asymptomatic children in the Buea and Limbe health districts of Cameroon: a pilot study,” Tropical Medicine and International Health, vol. 9, no. 9, pp. 1036–1040, 2004. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Dube, T. Nkosi, A. Clarke, N. Mkwetshana, E. Green, and R. Ndip, “Helicobacter pylori in an asymptomatic population of Eastern Cape Province, South Africa: public health implication,” Reviews on Environmental Health, vol. 24, no. 3, pp. 249–255, 2009. View at Publisher · View at Google Scholar
  11. C. Holcombe, “Helicobacter pylori: the African enigma,” Gut, vol. 33, no. 4, pp. 429–431, 1992. View at Publisher · View at Google Scholar · View at Scopus
  12. J. W. Lee, N. Kim, J. M. Kim et al., “Prevalence of primary and secondary antimicrobial resistance of Helicobacter pylori in Korea from 2003 through 2012,” Helicobacter, vol. 18, no. 3, pp. 206–214, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. W. Kumala and A. Rani, “Patterns of Helicobacter pylori isolate resistance to fluoroquinolones, amoxicillin, clarithromycin and metronidazoles,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 37, no. 5, pp. 970–974, 2006. View at Google Scholar · View at Scopus
  14. V. Cattoir, J. Nectoux, C. Lascols et al., “Update on fluoroquinolone resistance in Helicobacter pylori: new mutations leading to resistance and first description of a gyrA polymorphism associated with hypersusceptibility,” International Journal of Antimicrobial Agents, vol. 29, no. 4, pp. 389–396, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. J. Tankovic, D. Lamarque, C. Lascols, C. J. Soussy, and J. C. Delchier, “Clarithromycin resistance of Helicobacter pylori has a major impact on the efficacy of the omeprazole-amoxicillin-clarithromycin therapy,” Pathologie Biologie, vol. 49, no. 7, pp. 528–533, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. N. Broutet, F. Guillon, E. Sauty, D. Lethuaire, and F. Mégraud, “Survey of the in vitro susceptibility of Helicobacter pylori to antibiotics in France-Preliminary results (abstr),” Gastroenterology, vol. 43, supplement 2, p. A11, 1998. View at Publisher · View at Google Scholar
  17. F. Megraud, S. Coenen, A. Versporten et al., “Helicobacter pylori resistance to antibiotics in Europe and its relationship to antibiotic consumption,” Gut, vol. 62, no. 1, pp. 34–42, 2013. View at Publisher · View at Google Scholar
  18. R. P. H. Logan and M. M. Walker, “Epidemiology and diagnosis of Helicobacter pylori infection,” British Medical Journal, vol. 323, no. 7318, pp. 920–922, 2001. View at Publisher · View at Google Scholar
  19. C. Ricci, J. Holton, and D. Vaira, “Diagnosis of Helicobacter pylori: invasive and non-invasive tests,” Best Practice & Research: Clinical Gastroenterology, vol. 21, no. 2, pp. 299–313, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. S. M. Smith, C. O'Morain, and D. McNamara, “Antimicrobial susceptibility testing for Helicobacter pylori in times of increasing antibiotic resistance,” World Journal of Gastroenterology, no. 29, pp. 9912–9921, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. HainLifescience, “GenoType HelicoDR: Molecular Genetic Assay for Identification of Resistance to Fluoroquinolones and Clarithromycin of Helicobacter pylori from Culture and Biopsy Samples,” http://www.hain-lifescience.de/en/products/microbiology/helicobacter/genotype-helicodr.html.
  22. E. Cambau, V. Allerheiligen, C. Coulon et al., “Evaluation of a new test, GenoType HelicoDR, for molecular detection of antibiotic resistance in Helicobacter pylori,” Journal of Clinical Microbiology, vol. 47, no. 11, pp. 3600–3607, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Lottspeich, A. Schwarzer, K. Panthel, S. Koletzko, and H. Rüssmann, “Evaluation of the novel Helicobacter pylori ClariRes real-time PCR assay for detection and clarithromycin susceptibility testing of H. pylori in stool specimens from symptomatic children,” Journal of Clinical Microbiology, vol. 45, no. 6, pp. 1718–1722, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. TaytecEnterprises, “Helicobcter pylori stool antigen test,” Ontario, Canada, 2009, http://www.taytec.ca.
  25. Qiagen, “QIAamp® DNA stool handbook for DNA purification from stool samples,” in Sample & Assay Technologies, Qiagen, Hilden, Germany, 2010. View at Google Scholar
  26. D. E. Brennan, J. Omorogbe, M. Hussey et al., “Molecular detection of Helicobacter pylori antibiotic resistance in stool vs biopsy samples,” World Journal of Gastroenterology, vol. 22, no. 41, p. 9214, 2016. View at Publisher · View at Google Scholar
  27. C. Schabereiter-Gurtner, A. M. Hirschl, B. Dragosics et al., “Novel real-time PCR assay for detection of Helicobacter pylori infection and simultaneous clarithromycin susceptibility testing of stool and biopsy specimens,” Journal of Clinical Microbiology, vol. 42, no. 10, pp. 4512–4518, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. J. P. Gisbert, F. De La Morena, and V. Abraira, “Accuracy of monoclonal stool antigen test for the diagnosis of H. pylori infection: a systematic review and meta-analysis,” American Journal of Gastroenterology, vol. 101, no. 8, pp. 1921–1930, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Makristathis and A. M. Hirschl, “Detection and clarithromycin susceptibility testing of Helicobacter pylori in stool specimens by real-time PCR: how to get accurate test results,” Journal of Clinical Microbiology, vol. 45, no. 8, pp. 2756–2757, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. P. Malfertheiner, F. Megraud, C. A. O'Morain et al., “Management of Helicobacter pylori infection—the Maastricht IV/ Florence consensus report,” Gut, vol. 61, no. 5, pp. 646–664, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Nishizawa, H. Suzuki, and T. Hibi, “Quinolone-based third-line therapy for Helicobacter pylori eradication,” Journal of Clinical Biochemistry and Nutrition, vol. 44, no. 2, pp. 119–124, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Rajper, E. Khan, Z. Ahmad, S. M. Z. Alam, A. Akbar, and R. Hasan, “Macrolide and fluoroquinolone resistance in Helicobacter pylori isolates: an experience at a tertiary care centre in Pakistan,” Journal of the Pakistan Medical Association, vol. 62, no. 11, pp. 1140–1144, 2012. View at Google Scholar
  33. F. Mégraud, “Antibiotic resistance in Helicobacter pylori infection,” British Medical Bulletin, vol. 54, no. 1, pp. 207–216, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. I. Kobayashi, K. Murakami, M. Kato et al., “Changing antimicrobial susceptibility epidemiology of Helicobacter pylori strains in Japan between 2002 and 2005,” Journal of Clinical Microbiology, vol. 45, no. 12, pp. 4006–4010, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Vecsei, A. Kipet, A. Innerhofer et al., “Time trends of Helicobacter pylori resistance to antibiotics in children living in Vienna, Austria,” Helicobacter, vol. 15, no. 3, pp. 214–220, 2010. View at Publisher · View at Google Scholar
  36. J. M. Meyer et al., “Evaluation of risk factors in The Surveillance of Helicobacter pylori Antimicrobial Resistance Partnership (SHARP) in the United States from 1993–1999,” Gastroenterology, vol. 118, supplement, article A677, 2000. View at Google Scholar
  37. J. V. Solnick, “Editorial response: antibiotic resistance in Helicobacter pylori,” Clinical Infectious Diseases, vol. 27, no. 1, pp. 90–92, 1998. View at Publisher · View at Google Scholar · View at Scopus
  38. L. J. Xiong, Y. Tong, Z. Wang, and M. Mao, “Detection of clarithromycin-resistant helicobacter pylori by stool PCR in children: a comprehensive review of literature,” Helicobacter, vol. 18, no. 2, pp. 89–101, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Nishizawa and H. Suzuki, “Mechanisms of Helicobacter pylori antibiotic resistance and molecular testing,” Frontiers in Molecular Biosciences, vol. 1, p. 19, 2014. View at Publisher · View at Google Scholar
  40. Y. J. Yang, J. C. Yang, Y. M. Jeng, M. H. Chang, and Y. H. Ni, “Prevalence and rapid identification of clarithromycin-resistant Helicobacter pylori isolates in children,” Pediatric Infectious Disease Journal, vol. 20, no. 7, pp. 662–666, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. R. A. Moore, B. Beckthold, S. Wong, A. Kureishi, and L. E. Bryan, “Nucleotide sequence of the gyrA gene and characterization of ciprofloxacin-resistant mutants of Helicobacter pylori,” Antimicrobial Agents and Chemotherapy, vol. 39, no. 1, pp. 107–111, 1995. View at Publisher · View at Google Scholar · View at Scopus
  42. N. Umegaki, T. Shimoyama, D. Nishiya, T. Suto, S. Fukuda, and A. Munakata, “Clarithromycin-resistance and point mutations in the 23S rRNA gene in Helicobacter pylori isolates from Japan,” Journal of Gastroenterology and Hepatology (Australia), vol. 15, no. 8, pp. 906–909, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. K.-H. Hung, B.-S. Sheu, W.-L. Chang, H.-M. Wu, C.-C. Liu, and J.-J. Wu, “Prevalence of primary fluoroquinolone resistance among clinical isolates of Helicobacter pylori at a University Hospital in Southern Taiwan,” Helicobacter, vol. 14, no. 1, pp. 61–65, 2009. View at Publisher · View at Google Scholar · View at Scopus