Abstract
Data on the geographic prevalence of Helicobacter pylori iceA and babA alleles in Eastern Europe are still relatively scant. The aim of this study was to evaluate the prevalence of iceA and babA genotypes in Bulgarian symptomatic patients. The iceA and babA genotypes were evaluated by PCR with pure cultures in strains from 196 and 181 patients, respectively. Mixed infections were found in 10.2% of all 196 patients. Prevalence of H. pylori genotypes in patients with single-strain infections was 69.3% for iceA1, 30.7% for iceA2, 82.4% for cagA +, 89.2% for vacA s1, 10.8% for vacA s2, 39.8% for vacA m1, 60.2% for vacA m2 and 48.8% for babA2. Within the iceA1 positive strains, 94.3% and 88.5% were also vacA s1a and cagA positive, respectively. Of the babA2 positive strains, 100.0%, 92.4% and 72.2% were also vacA s1a, cagA and iceA1 positive, respectively. Ulcer patients had more often strains with cagA positive status and vacA s1a allele. Although neither iceA1 nor babA2 were more common in ulcer patients, the combination of both alleles was more frequent (48.1%) in the ulcer patients than in the rest (28.7%). Clarithromycin susceptible strains had more often iceA1 allele (74.4%) than the resistant strains (55.3%). In conclusion, the results demonstrated a high prevalence of virulent H. pylori in Bulgaria. Both iceA1 and babA2 genotypes were associated with other virulence factors of H. pylori and, in addition, the iceA1 allele was associated with the strain susceptibility.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Apostolopoulos P, Vafiadis-Zouboulis I, Tzivras M, Kourtessas D, Katsilambros N, Archimandritis A (2002) Helicobacter pylori (H pylori) infection in Greece: the changing prevalence during a ten-year period and its antigenic profile. BMC Gastroenterol 16:11
Ashour AA, Collares GB, Mendes EN, de Gusmão VR, Queiroz DM, Magalhães PP, de Carvalho AS, de Oliveira CA, Nogueira AM, Rocha GA, Rocha AM (2001) iceA genotypes of Helicobacter pylori strains isolated from Brazilian children and adults. J Clin Microbiol 39:1746–1750
Baglan PH, Bozdayi G, Ozkan M, Ahmed K, Bozdayi AM, Ozden A (2006) Clarithromycin resistance prevalence and iceA gene status in Helicobacter pylori clinical isolates in Turkish patients with duodenal ulcer and functional dyspepsia. J Microbiol 44:409–416
Boyanova L, Andreev N, Bouchard S, Megraud F (1994) Helicobacter pylori seroprevalence in Bulgaria. Med Microbiol Lett 3:107–113
Boyanova L, Gergova G, Nikolov R, Davidkov L, Kamburov V, Jelev C, Mitov I (2008) Prevalence and evolution of Helicobacter pylori resistance to 6 antibacterial agents over 12 years and correlation between susceptibility testing methods. Diagn Microbiol Infect Dis 60:409–415
Boyanova L, Markovska R, Yordanov D, Marina M, Ivanova K, Panayotov S, Gergova G, Mitov I (2009) High prevalence of virulent Helicobacter pylori strains in symptomatic Bulgarian patients. Diagn Microbiol Infect Dis 64:374–380
Caner V, Yilmaz M, Yonetci N, Zencir S, Karagenc N, Kaleli I, Bagci H (2007) H. pylori iceA alleles are disease-specific virulence factors. World J Gastroenterol 13:2581–2585
Chiarini A, Cala C, Bonura C, Gullo A, Giuliana G, Peralta S, D’Arpa F, Giammanco A (2009) Prevalence of virulence-associated genotypes of Helicobacter pylori and correlation with severity of gastric pathology in patients from western Sicily, Italy. Eur J Clin Microbiol Infect Dis 28:437–446
CLSI-National Committee for Clinical Laboratory Standards (CLSI-NSSLS) (2000) Performance standards for antimicrobial susceptibility testing. Tenth informational supplement. Approved standard M100-S10. M7, NCCLS, Wayne, PA
Erzin Y, Koksal V, Altun S, Dobrucali A, Aslan M, Erdamar S, Dirican A, Kocazeybek B (2006) Prevalence of Helicobacter pylori vacA, cagA, cagE, iceA, babA2 genotypes and correlation with clinical outcome in Turkish patients with dyspepsia. Helicobacter 11:574–580
Fujimoto S, Olaniyi O, Arnqvist A, Wu JY, Odenbreit S, Haas R, Graham DY, Yamaoka Y (2007) Helicobacter pylori BabA expression, gastric mucosal injury, and clinical outcome. Clin Gastroenterol Hepatol 5:49–58
Gong YH, Wang Y, Yuan Y (2005) Distribution of Helicobacter pylori in north China. World J Gastroenterol 11:3523–3527
Homan M, Luzar B, Kocjan BJ, Orel R, Mocilnik T, Shrestha M, Kveder M, Poljak M (2009) Prevalence and clinical relevance of cagA, vacA, and iceA genotypes of Helicobacter pylori isolated from Slovenian children. J Pediatr Gastroenterol Nutr 49:289–296
Kusters JG, van Vliet AH, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19:449–490
Lehours P, Ménard A, Dupouy S, Bergey B, Richy F, Zerbib F, Ruskoné-Fourmestraux A, Delchier JC, Mégraud F (2004) Evaluation of the association of nine Helicobacter pylori virulence factors with strains involved in low-grade gastric mucosa-associated lymphoid tissue lymphoma. Infect Immun 72:880–888
Lin HJ, Perng CL, Lo WC, Wu CW, Tseng GY, Li AF, Sun IC, Ou YH (2004) Helicobacter pylori cagA, iceA and vacA genotypes in patients with gastric cancer in Taiwan. World J Gastroenterol 10:2493–2497
Lu H, Yamaoka Y, Graham DY (2005) Helicobacter pylori virulence factors: facts and fantasies. Curr Opin Gastroenterol 21:653–659
Mattar R, dos Santos AF, Eisig JN, Rodrigues TN, Silva FM, Lupinacci RM, Iriya K, Carrilho FJ (2005) No correlation of babA2 with vacA and cagA genotypes of Helicobacter pylori and grading of gastritis from peptic ulcer disease patients in Brazil. Helicobacter 10:601–608
Megraud F (2004) H pylori antibiotic resistance: prevalence, importance, and advances in testing. Gut 53:1374–1384
Megraud F, Lehours P (2007) Helicobacter pylori detection and antimicrobial susceptibility testing. Clin Microbiol Rev 20:280–322
Megraud F, Lehn N, Lind T, Bayerdörffer E, O’Morain C, Spiller R, Unge P, van Zanten SV, Wrangstadh M, Burman CF (1999) Antimicrobial susceptibility testing of Helicobacter pylori in a large multicenter trial: the MACH 2 study. Antimicrob Ag Chemother 43:2747–2752
Miciuleviciene J, Calkauskas H, Jonaitis L, Kiudelis G, Tamosiūnas V, Praskevicius A, Kupcinskas L, Berg D (2008) Helicobacter pylori genotypes in Lithuanian patients with chronic gastritis and duodenal ulcer. Medicina (Kaunas) 44:449–454
Olfat FO, Zheng Q, Oleastro M, Voland P, Boren T, Karttunen R, Engstrand L, Rad R, Prinz C, Gerhard M (2005) Correlation of the Helicobacter pylori adherence factor BabA with duodenal ulcer disease in four European countries. FEMS Immunol Med Microbiol 44:151–156
Peek RM Jr, Thompson SA, Donahue JP, Tham KT, Atherton JC, Blaser MJ, Miller GG (1998) Adherence to gastric epithelial cells induces expression of a Helicobacter pylori gene, iceA that is associated with clinical outcome. Proc Assoc Am Physicians 110:531–544
Podzorski RP, Podzorski DS, Wuerth A, Tolia V (2003) Analysis of the vacA, cagA, cagE, iceA, and babA2 genes in Helicobacter pylori from sixty-one pediatric patients from the Midwestern United States. Diagn Microbiol Infect Dis 46:83–88
Romano M, Cuomo A (2004) Eradication of Helicobacter pylori: a clinical update. MedGenMed 6:19
Sgouros SN, Bergele C (2006) Clinical outcome of patients with Helicobacter pylori infection: the bug, the host, or the environment? Postgrad Med J 82:338–342
Smith SI, Oyedeji KS, Arigbabu AO, Cantet F, Megraud F, Ojo OO, Uwaifo AO, Otegbayo JA, Ola SO, Coker AO (2004) Comparison of three PCR methods for detection of Helicobacter pylori DNA and detection of cagA gene in gastric biopsy specimens. World J Gastroenterol 10:1958–1960
Torres LE, Melian K, Moreno A, Alonso J, Sabatier CA, Hernandez M, Bermudez L, Rodriguez BL (2009) Prevalence of vacA, cagA and babA2 genes in Cuban Helicobacter pylori isolates. World J Gastroenterol 15:204–210
van Doorn LJ, Figueiredo C, Sanna R, Plaisier A, Schneeberger P, de Boer W, Quint W (1988) Clinical relevance of the cagA, vacA, and iceA status of Helicobacter pylori. Gastroenterology 115:58–66
Wen S, Velin D, Felley CP, Du L, Michetti P, Pan-Hammarström Q (2007) Expression of Helicobacter pylori virulence factors and associated expression profiles of inflammatory genes in the human gastric mucosa. Infect Immun 75:5118–5126
Yamaoka Y (2008a) Roles of the plasticity regions of Helicobacter pylori in gastroduodenal pathogenesis. J Med Microbiol 57:545–553
Yamaoka Y (2008b) Roles of Helicobacter pylori BabA in gastroduodenal pathogenesis. World J Gastroenterol 14:4265–4272
Yamaoka Y, Kodama T, Gutierrez O, Kim JG, Kashima K, Graham DY (1999) Relationship between Helicobacter pylori iceA, cagA, and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol 37:2274–2279
Acknowledgements
This study was supported by grants from the Medical University of Sofia (Council of Medical Science), project No. 17/2006, grant No. 23/2006 and project No. 20/2007, grant No. 22/2007 and Project N0. 5/2009, grant No. 8/2009.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Boyanova, L., Yordanov, D., Gergova, G. et al. Association of iceA and babA genotypes in Helicobacter pylori strains with patient and strain characteristics. Antonie van Leeuwenhoek 98, 343–350 (2010). https://doi.org/10.1007/s10482-010-9448-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-010-9448-y