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ORIGINAL ARTICLE
Year : 2007  |  Volume : 25  |  Issue : 4  |  Page : 374-377
 

Antimicrobial susceptibility testing of Helicobacter pylori to selected agents by agar dilution method in Shiraz-Iran


1 Department of Medical Microbiology, Shiraz Medical School, Shiraz University of Medical Sciences, P.O. Box 71345 - 1945, Shiraz, Iran
2 Department of Gastroenterohepatology Research Center, Shiraz Medical School, Shiraz University of Medical Sciences, P.O. Box 71345 - 1945, Shiraz, Iran

Date of Submission06-Apr-2007
Date of Acceptance30-May-2007

Correspondence Address:
A Mobasser
Department of Medical Microbiology, Shiraz Medical School, Shiraz University of Medical Sciences, P.O. Box 71345 - 1945, Shiraz
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0255-0857.37342

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 ~ Abstract 

Purpose: To assess the pattern of antimicrobial susceptibility profile of Helicobacter pylori isolates from patients with gastritis, duodenal ulcer (DU) and gastroesophageal reflux disease (GERD) residing in Shiraz, Iran. Methods: One hundred and six H. pylori isolates from patients with gastritis, DU and GERD undergoing endoscopy at our university hospitals and clinics were analysed for their antimicrobial susceptibility to metronidazole, clarithromycin, amoxicillin, co-amoxiclav, tetracycline, ciprofloxacin and furazolidone. The minimum inhibitory concentrations were determined by agar dilution method. Results: Overall H. pylori resistance rate was 72.6% to metronidazole, 9.4% to clarithromycin and furazolidone, 20.8% to amoxicillin and 4.7% to tetracycline and ciprofloxacin. No resistance to co-amoxiclav was detected among H. pylori isolates. No significant differences between antimicrobial resistance and clinical outcome were detected. Conclusions: With regard to the increasing resistance of H. pylori isolates to various antibiotics, susceptibility testing of H. pylori isolates prior to the treatment of infection must be performed to achieve better eradication and to reduce the risk of selection of H. pylori resistant strains.


Keywords: Agar dilution, antimicrobial susceptibility test, Helicobacter pylori, Iran


How to cite this article:
Kohanteb J, Bazargani A, Saberi-Firoozi M, Mobasser A. Antimicrobial susceptibility testing of Helicobacter pylori to selected agents by agar dilution method in Shiraz-Iran. Indian J Med Microbiol 2007;25:374-7

How to cite this URL:
Kohanteb J, Bazargani A, Saberi-Firoozi M, Mobasser A. Antimicrobial susceptibility testing of Helicobacter pylori to selected agents by agar dilution method in Shiraz-Iran. Indian J Med Microbiol [serial online] 2007 [cited 2019 Aug 18];25:374-7. Available from: http://www.ijmm.org/text.asp?2007/25/4/374/37342


Helicobacter pylori is a gram-negative rod which is responsible for a spectrum of diseases in alimentary canal including chronic superficial gastritis, chronic atrophic gastritis, gastric and duodenal ulcers (GU & DU), gastric cancer and mucosa-associated lymphoid tissue lymphoma. [1] In general, combined therapy is used to eradicate H. pylori infection. [2] However, increase in the resistant isolates highlights the need for susceptibility testing of H. pylori isolates prior to the eradication of infection. [3]

There are several methods for susceptibility testing of H. pylori isolates including agar dilution, micro dilution, disc diffusion and E -test methods. Agar dilution is a gold standard method for susceptibility testing of H. pylori . This method is not always practical to perform in routine laboratories, but it is relatively inexpensive and H. pylori grows readily on solid media. The broth micro dilution method is limited by the difficulty in growing H. pylori in liquid media. Disc diffusion is easy to perform but does not give actual minimum inhibitory concentrations (MICs). The E -test is expensive and has been reported to give discrepancies in the interpretation of 'susceptible' or 'resistant' when testing for metronidazole. [4]

The objective of present investigation was to determine in-vitro antimicrobial susceptibility testing of H. pylori isolates from patients with gastritis, DU and gastroesophageal reflux disease (GERD) to the seven routinely used antimicrobial agents by agar dilution method and to determine their MICs. Statistical analysis was performed to determine significant differences between antimicrobial resistance patterns and clinical outcome.


 ~ Materials and Methods Top


H. pylori isolates

One hundred and six H. pylori isolates were recovered from gastric biopsies of patients with gastritis, DU and GERD undergoing endoscopy at the university hospitals and clinics, Iran, from September 2004 to August 2005. None of the patients had received antimicrobial therapy for at least 1 week prior to endoscopy. The specimens were placed in the sterile screw-capped tubes containing 3-4 mL brain heart infusion (BHI) broth (Merck Co, Germany) and transported to the microbiology laboratory at Shiraz Medical School, Iran, for isolation, diagnosis and antibiotic susceptibility tests within 4 h. The biopsies were ground in a tissue grinder. Using a pasture pipette, about two drops of homogenates were inoculated into  Brucella More Details agar (Merck Co, Germany) containing 10% horse blood, vancomycin, polymyxin B and amphotericin B and streaked with bacteriological loop. The inoculated culture media were transferred into the anaerobic jar (Merck Co, Germany) in which microaerophilic environment was achieved using grade C gas pack (Merck Co, Germany) and incubated at 37 °C for 7 days. Isolates that exhibited gram negative curved rods on Gram stain reaction and were positive for catalase, oxidase and urease tests were considered as H. pylori . The isolates were suspended in the Eppendorf tubes containing BHI broth with 30% glycerol and stored at -70 °C until used.

Susceptibility testing

The MICs were carried out by agar dilution method using Muller-Hinton agar (Merck Co, Germany) containing 5% heparinized horse blood and various concentrations of drugs. The ranges of antibiotic concentrations that were used in this study were as follows: Clarithromycin (CLA, 0.125-16 μg/mL), metronidazole (MTZ, 0.5-64 μg/mL), tetracycline (TET, 0.125-16 μg/mL), ciprofloxacin (CIP, 0.0625-8 μg/mL), amoxicillin (AMX, 0.03125-4 μg/mL), co-amoxiclav (CO-AMX, 0.03125-4 μg/mL) and furazolidone (FZD, 0.03125-4 μg/mL). All antimicrobial agents were purchased from Pakhsh-e-Hejrat, Iran.

Isolates were removed from freezer, thawed and subcultured on Brucella agar containing 10% horse blood without antibiotics and incubated under microaerophilic conditions at 37 °C for 3 days. After a lawn of growth appeared, bacterial colonies were suspended in sterile saline at a density equivalent to no. 3 McFarland's standard and 5 mL (10 6 colony forming unit/spot) of bacterial suspension was spot inoculated into susceptibility testing media. The spot inoculated plates were incubated under microaerophilic conditions. The MIC was defined as the lowest concentration of the antibiotic, which completely inhibited visible bacterial growth at 37 °C after 72 h. Resistance cutoff for the antibiotics were as follows: metronidazole (MIC > 8 μg/mL), clarithromycin (MIC > 1 μg/mL),[5] tetracycline and ciprofloxacin (MIC > 2 μg/mL) amoxicillin, co-amoxiclav and furazolidone (MIC > 0.5 μg/mL). [6],[7],[8],[9],[10]

Statistical analysis

The significance of the antibiotic resistance patterns between two groups of patients (GA and DU) was determined by Chi-square and Fisher's exact tests. SPSS, version 11.5 was used to perform statistical analysis.


 ~ Results Top


In this study, 106 patients with positive culture for H. pylori , 66 male, 40 female with the age range of 9-89 years were enrolled. Sixty-five (61.3%) of these patients suffered from gastritis, 33 (31.1%) had DU and 8 (7.5%) had gastroesophageal reflux disease. [Table - 1] summarizes the results of susceptibility of H. pylori isolates to the antimicrobial agents tested. Among 106 H. pylori isolates, 77 (72.6%) showed resistance to metronidazole, 10 (9.4%) to clarithromycin and furazolidone, 22 (20.8%) to amoxicillin, 5 (4.7%) to tetracycline and ciprofloxacin and none of the 106 isolates exhibited resistance to co-amoxiclav.

[Table - 2] summarizes the pattern of multi-drug resistant strains of H. pylori isolates, 25 (23.5%) elicited double, 4 (3.7%) triple and 1 (0.94%) quadruple drugs resistance and the overall multidrug resistance of H. pylori isolates was 28.1%. No significant differences were found between antimicrobial resistance patterns and the two groups of GA and DU patients ( P > 0.05). Since only eight patients were in GERD group they were not included in statistical analysis.


 ~ Discussion Top


The efficacy of the treatment of gastric H. pylori infection can be reduced by the occurrence of primary or acquired resistance to various drugs. [11] Therefore, susceptibility testing of H. pylori has been increasingly important for the eradication of this organism. An additional advantage of susceptibility testing is that it may reduce the risk of H. pylori resistance. [12]

In the present investigation, we tested the sensitivity and resistant pattern of H. pylori isolated from patients residing in Shiraz, Fars province, Iran, to seven routinely used drugs including amoxicillin, metronidazole, clarithromycin, co-amoxiclav, furazolidone, tetracycline and ciprofloxacin.

Worldwide resistance of H. pylori to metronidazole has been reported, with rates raging from 0 to 98%. [9],[10],[13] In the three studies carried out by Siavoshi et al. , [7] Nariman et al. [14] and Falsafi et al. , [15] in Tehran, Iran, the prevalence of metronidazole resistance were reported to be 37.5, 72 and 72-79%, respectively. We found 72.6% resistance among H. pylori isolates in Shiraz southern Iran. Metronidazole is a frequently used drug in Iran and therefore it is not unexpected to find such a high level of resistance. Metronidazole has been widely prescribed for the other infections like parasitic or genital infections and the use or abuse of this inexpensive drug may contribute to the increase in metronidazole resistance. The differences between the resistance rates may reflect the variation in metronidazole usage between countries.

Amoxicillin is the only β-lactam used to treat H. pylori infection and it is included in most current therapeutic regimens. Until recently, resistance to amoxicillin was considered to be absent or very rare; however, amoxicillin-resistant H. pylori strains have now been identified in different countries. [8],[9] The World-wide prevalence of resistance to amoxicillin is 0-41%. [10],[14],[16] In the two previous studies in Iran, investigators reported 7 and 27% amoxicillin resistance among H. pylori isolates. [7],[15] In the present study, the amoxicillin resistance was found to be 20.8% of isolates. The reason for this high level of amoxicillin resistance remain unclear, however, since no pharmaco-epidemilogical data regarding amoxicillin use in Iran exists, it may be speculated that this drug is used in a disproportionate manner.

All H. pylori isolates tested in this investigation were susceptible to co-amoxiclav. This high rate of susceptibility has also been reported by Piccolomini et al. , in Italy. [6] Co-amoxiclav is not used routinely in the common H. pylori infection therefore finding such a high level of susceptible H. pylori strains is not unexpected. With regard to high rate of amoxicillin resistance of H. pylori isolated from patients residing in Shiraz, Iran, co-amoxiclav may produce better eradication results if used in preference to amoxicillin. We recommend clinical trials with this antibiotic in our region.

Clarithromycin is a macrolide widely used in combination with a proton pump inhibitor with or without a second antibiotic. The worldwide rate of clarithromycin resistance ranges from 0 to 44.7%. [10],[13] In three separate studies performed in Iran, clarithromycin resistance of H. pylori isolates were reported 14.5, 21 and 23% of the isolates. [7],[14],[15] In our study, only 9.4% of the isolates were resistant to clarithromycin. Since high cost of clarithromycin limits the use of this drug in Iran, finding such resistant isolates may be partially explained by the primary resistance of H. pylori to clarithromycin. The differences between the resistance rates may reflect the variation in clarithromycin usage between countries.

Furazolidone has been used as an alternative to overcome metronidazole resistance strains. This compound has a good in vitro activity against H. pylori . Because of the high rates of metronidazole resistance in H. pylori in many areas and the preserved activity of furazolidone against metronidazole-resistant strains, this compound has been recommended as a possible alternative in H. pylori eradication regimens. Resistance to furazolidone was considered to be rare, but different studies showed resistance rates ranging from 0 to 13% among various countries. [7],[9] Siavoshi et al. , [7] reported furazolidone resistance among 5% of H . pylori isolates in Tehran, Iran, however in our study, we found 9.4% resistance rate. Although furazolidone is cost effective and has good effect against H. pylori infection, a major problem with furazolidone at the standard dose of 200 mg BD is the high rate of severe adverse effects which limit the use of this drug.

Tetracyclines are currently used for treatment of H. pylori infection as part of quadruple therapy. Overall resistance of H. pylori to tetracycline has been found to be low and is estimated to be less than 2%. [17] However, higher resistance rates, up to 20%, have been reported in other studies from different countries. [9],[15] The prevalence of tetracycline resistance of H. pylori isolates in Iran is 20%, [17] but our study shows a low resistance of 4.7% indicating the importance of this drug in eradicating H. pylori . We found no resistance to tetracycline among H. pylori isolates from patients with DU. This drug is not routinely used in H. pylori eradication regimens, therefore finding such a low resistance rate is not unexpected.

Ciprofloxacin is a fluoroquinolone that inhibit A subunit of the DNA gyrase. Although ciprofloxacin is not the drug of choice for H. pylori infection, 0-20% resistance to this antibiotic has been reported in different countries. [6],[14] We found only 4.7% ciprofloxacin resistance among H. pylori isolates. Falsafi et al. , [15] have previously reported 20% resistance to ciprofloxacin among H. pylori isolated from patients in Tehran. The higher level of resistance among H. pylori isolates in Tehran in comparison with H. pylori isolates from Shiraz shows that our H. pylori isolates may be more susceptible than those in Tehran.

Data obtained in this investigation revealed that 23.5% of H. pylori strains were resistance to two antibacterial agents, 3.7% isolates to three drugs and 0.94% to four antibiotics. Torres et al. , [18] from Mexico have reported 30.7% double resistance and 8.7% triple resistance among H. pylori isolates. H. pylori resistance to these antimicrobials may be partially explained by the high prevalence of these bacteria in our population. In our study, similar to that reported by Wolle et al. , [17] we found no significant differences in the prevalence of seven antibiotics resistance between H. pylori isolates from patients with gastritis and DU.

Metronidazole and amoxicillin in combination with a proton pump-inhibitor were used for treatment of H. pylori infection with eradication rate of 80% in Europe. [19] However, this triple therapeutic regimen was found to be less than 60% efficient among Iranian population. [20] In this study, 72.6% of H. pylori isolates were resistance to metronidazole and therefore, recurrence of the infection with H. pylori could be expected among patients receiving the above mentioned triple therapy. Considering the low percentage resistance of H. pylori to ciprofloxacin (4.7%), one may substitute metronidazole by ciprofloxacin to achieve a better eradication rate.

We suggest that culture and antimicrobial susceptibility testing of H. pylori must be performed in patients who have failed the metronidazole based triple therapy.


 ~ Acknowledgement Top


The authors would like to thank the Vice-Chancellor for Research, Shiraz University of Medical Sciences, for financial support of this project (Grant No: 82-1775).

 
 ~ References Top

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    Tables

  [Table - 1], [Table - 2]

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