Pakistan Journal of Medical Sciences

Published by : PROFESSIONAL MEDICAL PUBLICATIONS

ISSN 1681-715X

HOME   |   SEARCH   |   CURRENT ISSUE   |   PAST ISSUES

-

ORIGINAL ARTICLE

-

Volume 24

January - March 2008

Number  1


 

Abstract
PDF of this Article

Prevalence and antibiotic resistance among helicobacter pylori
clinical isolates from main Hospitals in the
Western Region of Saudi Arabia

Aiman M. Momenah1, Atif H. Asghar2

ABSTRACT

Objective: The aim of this study was to evaluate the antimicrobial susceptibility patterns amongst H. pylori clinical strains isolated from the main hospitals in the western region of Saudi Arabia.

Methodology: Antimicrobial susceptibility testing was performed for 137 clinical isolates of H. pylori recovered from 368 Saudi patients undergoing endoscopic examination. The antibiotics used were amoxicillin, tetracycline, clarithromycin and metronidazole.

Results: A high percentage of resistance were observed against metronidazole (48.2%) followed by clarithromycin (27.7%), amoxicillin (14.6%) and tetracycline (9.5%). A total of 12 (8.8%) multidrug-resistant H. pylori isolates were observed in this study. Moreover, a warning sign of emerging resistance to amoxicillin, tetracycline and clarithromycin were noted.

Conclusion: The clinician need to be aware about resistance pattern in their region when they select empiric antibiotics regimen for H. pylori.

KEYWORDS: Helicobacter pylori, Antibiotic resistance, Gastritis, Peptic ulcer, Gastric cancer.

Pak J Med Sci    January - March 2008    Vol. 24 No. 1    100-103


1. Aiman M. Momenah,
Assistant Prof. of Med Microbiology,
Department of Medical Microbiology,
Faculty of Medicine and Medical Sciences,
2. Atif H. Asghar,
Associate Prof. of Med Microbiology,
Department of Environmental and Health Research,
The Custodian of the two Holly Mosques
Institute for Hajj Research,
1-2: Umm Al-Qura University,
Makkah- Saudi Arabia.

Correspondence

Dr. Atif H. Asghar,
Umm Al-Qura University,
The Custodian of the Two Holy Mosques,
Institute for Hajj research, P.O. Box: 6287
Makkah, Saudi Arabia.
E-mail: asghar1000@hotmail.com

* Received for Publication: January 15, 2007

* Revision Accepted: December 1, 2007


INTRODUCTION

Helicobacter pylori is recognized as a major cause of human gastritis and peptic ulcer as well as an important risk factor for gastric cancer. Eradication of this organism is indicated in all patients with active or recurrent peptic ulceration.1 Combined therapy (dual or triple) including two of the following antibiotics- amoxicillin, tetracycline, metronidazole or clarithromycin, plus a proton pump inhibitor (bismuth salt or ranitidine bismuth citrate) is the therapy most frequently used to eradicate H. pylori.2

During recent years, antibiotic resistance among H. pylori is considered the most common reason for eradication failure in most of the reports.2,3 Several international studies demonstrated that high resistant rates among H. pylori clinical isolates especially metronidazole has emerged being a major factor for treatment failure.3,4 However, resistance to some antibiotics such as amoxicillin is still absent or low.4 Virtually, no treatment regimen has achieved a 100% cure rate, which makes it important to evaluate the antimicrobial susceptibility pattern of H. pylori strains in every geographical region.5

The updated antimicrobial susceptibility pattern of H. pylori strains in Saudi Arabia and particularly in the western region is not available. Present study was therefore conducted to asses the prevalence of resistance among the four main antibiotics (amoxicillin, tetracycline, metronidazole and clarithromycin) currently in use for H. pylori infections treatment.

MATERIALS AND METHODS

During October 2004 to May 2005, a total of 1104 gastric biopsies from 368 Saudi patients (3 biopsies from each patient) who presented with symptoms suggestive of chronic gastritis or peptic ulcer disease (PUD) were taken from antrum. Hospitals which participated in this study were; Al-Noor specialist hospital- Makkah (560 bed), King Abdul-Aziz hospital- Makkah (272 bed), General King Fahad hospital-Jeddah (710 bed), King Abdul-Aziz hospital and Oncology Centre-Jeddah (425 bed) and King Faisal hospital-Makkah (221 bed). Two hundred and eighty four (77.2%) of patients were suffering from various gastric pathologies, 264 (71.7%) with gastritis, 18 (4.9%) with gastric ulcer and two (0.5%) with tumor) while the remaining 84 (22.8%) had normal endoscopic results. Patients with a history of previous H. pylori treatment were excluded from the present study.

Gastric biopsies were transported in a 0.5 ml Brucella broth media (Oxoid, UK).6 These gastric biopsies were obtained from each patient; one was used for rapid CLO test (Rapid Urease Test or Campylobacter like Organism for determination of urease activity) (Oxoid, UK) and the remaining two biopsies were cultured on H. pylori selective agar (Oxoid, UK) and incubated at 37C in a BBL GasPak (Becton-Dickinson, USA) containing a Campy-Pak Plus microaerophilic system generator (Becton-Dickinson, USA) and incubated for 7 days. The identity of H. pylori clinical isolates were confirmed by colonial morphology, Gram-stain (curved Gram-negative bacilli) and positive reaction for oxidase, catalase & urease tests.6-8

Antibiotic susceptibility was examined by the disk diffusion method, according to a standard protocol.9 Briefly, bacterial suspensions were adjusted to the 0.5McFarl and standard (equivalent to 1-2 x 108cfu/ml) and were used to inoculate Muller Hinton agar plates. Antimicrobial disks (amoxicillin, tetracycline, metronidazole and clarithromycin) were applied and the plates were incubated under microaerophilic conditions at 35oC for 16-18 hour. The zones of growth inhibition produced by each antibiotic were measured and interpreted by standard procedure, to determine the susceptibility or resistance.

RESULTS

This study included three hundred sixty eight patients i.e. 64 (46.7%) male and 73 (53.3%) female. Age ranged between 16-90 years, majority (34.3%) were between 31-45 years (Fig-1). With culture technique 137 (37.2%) were positive. In comparison to culture test the direct CLO test showed lower positive results with only 128 (34.7%) samples being positive. (Fig-1)

According to the endoscopic findings, the presence of H. pylori in normal, gastritis, gastric ulcer and malignant cases were 22.6% (31 out of 137), 70.8% (97), 6.6% (9), and 0%, respectively (Figure-2).

The antimicrobial resistance patterns of H. pylori isolates are shown in Table-I. Results demonstrated that among the tested isolates, 13 (9.5%), 20 (14.6%), 38 (27.7%), and 66 (48.2%) strains were resistant to tetracycline, amoxicillin, clarithromycin and metronidazole, respectively. Results revealed that a total of 12 (8.8%) H. pylori isolates were multidrug-resistant (i.e. resistant to metronidazole, clarithromycin and amoxicillin).

DISCUSSION

Present study demonstrated 37.2% prevalence rate for H. pylori in the patient population tested. The results are much lower than compared to what has been reported elsewhere in Saudi Arabia with prevalence rates of 54.9% and 63% in southern and eastern regions, respectively.10,11 This difference in prevalence rates could be attributable to the different detection methods in each study, different demographic distribution of the bacteria among various regions and previous antibiotic consumption.2,12-14

In this study, the prevalence rate of H. pylori in patients with gastritis was 70.8% which is much higher when compared to the results obtained by Ayoola et al., reporting a percentage of 55%.10 The prevalence of H. pylori among gastric ulcer and control cases in this study were 50% and 22.6%, respectively, which is comparable with the results achieved by Ayoola et al., who reported a percentage of 53.6% and 43.6% in gastric ulcer and normal cases, respectively.10 Interestingly, two earlier studies from Saudi Arabia detected the organism in only 9% and 13%, respectively, in normal controls in comparison to 22.6% obtained in the present study, reflecting an increase in the carrier rate of this organism.15,16

The status of metronidazole resistance (48.2%) obtained in this study is much lower than what has been reported by Al-Qurashi et al. in other region of Saudi Arabia who reported an increase of metronidazole resistance among H. pylori clinical isolates from 35.2% to 78.5% in period between 1988 to 1996.17 However the rate of metronidazole resistance in our study is much higher than what has been reported in other studies with resistance percentage of 16% to 90%.2,3,18-21 The variation in the resistance rates obtained in this study compared to other studies may indicate the differences in metronidazole misuse in different regions. Resistance to clarithromycin was significantly higher in this study (27.7%) compared to the recent reports from the United States (13%) and Italy (23.4%).19,20

This study showed that 13 isolates were resistant to tetracycline in comparison to only a single isolate in other region of Saudi Arabia in a study performed in the period 1990-1996 and none in the period 1987-1988 indicating a gradual tetracycline emerging resistance among H. pylori clinical isolates.17 Similarly, the resistance rate to amoxicillin in this study (14.6%) was much higher than what has been reported elsewhere.12,18,22 We conclude that, the clinicians need to be aware about antibiotic resistance pattern in their region when they select empiric antibiotics regimen for H. pylori.

ACKNOWLEDGMENTS

We thank The Custodian of The Two Holy Mosques Institute for Hajj Research-Umm Al-Qura University for supporting this project. We are grateful to Algawhara Al-Gethami, Menna Amin, Ommaima Al-Haj and Reham Al-Shareef for their assistant in samples collection. We also thank all the hospitals participated in this study.

Source of funding: The Custodian of the Two Holy Mosques Institute for Hajj Research- Umm Al-Qura University.

REFERENCES

1. Dunn B, Cohen H, Blaser M. Helicobacter pylori. Clin Microbiol Rev 1997;10:720-41.

2. Cabrita J, Oleastro M, Matos, Manhente A, Cabral J, Barros R, et al. Features and trends in Helicobacter pylori antibiotic resistance in Lisbon area, Portugal 1990-1999. J Antimicrob Chemother 2000;46:1029-31.

3. Megraud F. Resistance of Helicobacter pylori to antibiotics: The main limitation of current proton-pump inhibitor triple therapy. Eur J Gastroenterol Hepatol 1999;11:35-7.

4. De Korwin JD. Helicobacter pylori infection and antimicrobial agents resistance. Rev Med Interne 2004;25:54-64.

5. Keller G, Vamderhulst R, Rauws E, Tytgac G. Treatment of Helicobacter pylori Infection. Review of the world 1996;6-19.

6. Harris A, Misiewicz J. Helicobacter pylori. Blackwell Science, Tokyo 1996;5-33.

7. Murray P, Baron E, Pfaller M, Tenover F, Yolken R. Manual of Clinical Microbiology, ASM, Washington 1999;227-33.

8. Collee J, Fraser A, Marmion B, Simmons A. Practical Medical Microbiology, Churchill Livingstone, New York 1996;439-41.

9. National committee for clinical laboratory standards. Performance standards for antimicrobial disk susceptibility tests. Approved standard, 5thed. Document M2-A5. NCCLS, Villanova, PA, USA. 1999.

10. Ayoola AE, Ageely HM, Gadour MO, Pathak VP. Prevalence of Helicobacter pylori infection among patients with dyspepsia in South-Western Saudi Arabia. Saudi Med J 2004;25:1433-8.

11. Nkrumah K. Endoscopic evaluation of upper abdominal symptoms in adult patients, Saudi Aramco-Al Hasa Health Center, Saudi Arabia. West Afr J Med 2002;21:1-4.

12. Duck M, Wang Y. Stool Antigen Assay can effectively screen Helicobacter pylori infection. Gastroenterology 2001;98-103.

13. Tsukada K, Miyazaki T, Katoh H, Masuda N, Oiima H, Fukai Y, et al. Seven- day triple therapy with omeprazol, amoxycillin and clarithromycin for Helicobacter pylori infection in haemodialysis patients. Scand J Gastroenterol 2002;37:1265-8.

14. Bazzoli M, Al-Qurain A. Campylobacter pylori in Saudi Arabia under upper gastrointestinal endoscopy. Saudi Med J 1989;516-8.

15. Novis B, Gabay G, Naftali T. Helicobacter pylori: the Middle East scenario. Yale J Biol Med 1998;71:135-41.

16. Zaman R, Hossain J, Zawawi T, Thomas J, Gilpin C, Dibb W. Diagnosis of Helicobacter pylori. Saudi Med J 1995;552-5.

17. Al-Qurashi A, El-Morsy F, Al-Quorain A. Evolution of metronidazole and tetracycline susceptibility pattern in Helicobacter pylori at a hospital in Saudi Arabia. Int J Antimicrob Agents 2001;17:233-6.

18. Nahar S, Mukhopadhyay A, Khan R, Ahmad M, Datta S, Chattopadhyay S, et al. Antimicrobial susceptibility of Helicobacter pylori strains isolated in Bangladesh. J Clin Microbiol 2004;42:4856-8.

19. Toracchio S, Marzio L. Primary and secondary antibiotic resistance of Helicobacter pylori strains isolated in central Italy during the years 1998-2002. Dig Liver Dis 2003;35:541-5.

20. Duck W, Sobel J, Pruckler J, Song O, Swerdlow D, Friedman C, et al. Antimicrobial resistance incidence and risk factors among helicobacter pylori infected persons, United States. Emerg Infect Dis 2004;10:1088-94.

21. Banatvala N, Davies G, Abdi Y, Clements L, Rampton D, Hardie J, et al. High prevalence of Helicobacter pylori metronidazole resistance in migrants to East London: Relation with previous nitroimidazole exposure and gastroduodenol disease. Gut 1994;35:1562-6.

22. Sherif M, Mohran Z, Fathy H, Rockabrand D, Rozmaizl P, Frenek R. Universal high-level primary metronidazole resistance in Helicobacter pylori isolated from children in Egypt. J Clin Microbiol 2004;42:4832-4.


HOME   |   SEARCH   |   CURRENT ISSUE   |   PAST ISSUES