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The Journal of Health, Population and Nutrition
icddr,b
ISSN: 1606-0997 EISSN: 2072-1315
Vol. 28, Num. 5, 2010, pp. 443-449

Journal of Health Population and Nutrition, Vol. 28, No. 5, September-October, 2010, pp. 443-449

Original Paper

Monitoring antimicrobial susceptibility of Neisseria gonorrhoeae isolated from Bangladesh during 1997- 2006: Emergence and pattern of drug-resistant isolates

1 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000; Institute of Food and Radiation Biology, Bangladesh; Atomic Energy Commission, GPO Box 3787, Dhaka 1000, Bangladesh,
2 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000, Bangladesh; Department of Medical Microbiology, University of Manitoba, Winnipeg, MB, Canada,
3 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000; Department of Life Sciences, North South University, Dhaka, Bangladesh,
4 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000, Bangladesh; Department of Microbiology, Biochemistry and Immunology, Morehouse School of Medicine, Atlanta, GA 30310, USA,
5 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000, Bangladesh,
6 M.A.G. Osmani Medical College, Sylhet, Bangkok,Thailand,
7 Laboratory Sciences Division, ICDDR,B, GPO Box 128, Dhaka 1000, Bangladesh; Laboratory Sciences Division, Family Health International, Asia Pacific Regional Office, Bangkok,Thailand,

Correspondence Address: Motiur Rahman, Associate Director, Laboratory Sciences Division, Family Health International, Asia Pacific Regional Office, 19th Floor, Tower 3, Sindhorn Building, 130-132 Wireless Road, Phatumwan, Bangkok 10330 , mrahman@fhi.org

Code Number: hn10058

Abstract

Gonorrhoea is one of the most common sexually transmitted infections (STIs) in developing countries, and the emergence of resistance to antimicrobial agents in Neisseria gonorrhoeae is a major obstacle in the control of gonorrhoea. Periodical monitoring of antimicrobial susceptibility of N. gonorrhoeae is essential for the early detection of emergence of drug resistance. In total, 1, 767 gonococcal strains isolated from males and females (general population and those with high-risk behaviour) from different parts of Bangla­desh were studied during 1997- 2006 . Minimum inhibitory concentrations of penicillin, tetracycline, cipro­floxacin, ceftriaxone, spectinomycin, and azithromycin for the isolates were determined by the agar dilu­tion method. Isolates resistant to three or more antimicrobial agents are considered multidrug-resistant. The prevalence of plasmid-mediated penicillinase-producing N. gonorrhoeae (PPNG) and plasmid-mediated tetracycline-resistant N. gonorrhoeae (TRNG) was determined. Nine percent of the isolates were resistant to ciprofloxacin in 1997 compared to 87% in 2006. Multidrug-resistant N. gonorrhoeae have emerged in 1997 , and 44% of the strains (n= 66) isolated during 2006 were multidrug-resistant. Forty-two percent of the isolates in 2006 were both PPNG- and TRNG-positive compared to none in 1997 . The rapidly-changing pattern of gonococcal antimicrobial susceptibility warrants the need for an antimicrobial susceptibility­monitoring programme, and periodical analysis and dissemination of susceptibility data are essential to guide clinicians and for successful STI/HIV intervention programmes.

Keywords: Drug resistance, Microbial; Gonorrhoea; Neisseria gonorrhoeae; Sexually transmitted infections; Surveillance; Bangladesh

Introduction

Gonorrhoea is one of the classical sexually transmit-ted infections (STIs) with humans as the only host for the causative agent Neisseria gonorrhoeae. Des-pite a sharp decline in the incidence of gonococ-cal infection in developed countries during the last decade, gonorrhoea still remains one of the most common STIs in developing countries and a global health problem [1] . The prevalence of gonococcal infection varies greatly among countries in the de-veloped and developing world, the highest be-ing in South and Southeast Asia, followed by sub-Saharan Africa and Latin America, where it contin-ues to be a major public-health problem. According to the World Health Organization (WHO), there are approximately 62 million new cases of gonorrhoea worldwide annually, and almost half of the cases are estimated to occur in Southeast Asia, including Bangladesh [2] .

In the absence of any effective vaccine against N. gonorrhoeae, control of gonococcal infection main-ly depends on the identification and treatment of infected individuals. An early and successful anti-biotic treatment of gonococcal infection is impor-tant for cure of the individual patient, preven-tion of complications, and reduction of transmis-sion [3] . Strategies for the control of gonorrhoea have relied on the use of highly-effective and often single-dose therapy administered at the time of di-agnosis [4] . Information on antimicrobial suscep-tibility of N. gonorrhoeae is, therefore, important for the selection of an appropriate antimicrobial agent [5] .

The versatile nature of the gonococcus and its ca-pacity to cope with changing conditions in micro-environment is a major challenge in the preven-tion and control of gonococcal infection [6] . The continuous emergence of resistance to antimi-crobial agents has made the treatment of gonor-rhoea expensive, prolonged, and unpredictable. The organism acquires resistance by spontane-ous mutation or by acquisition of new DNA via conjugation or transformation, and resistance may, thus, be chromosomal or plasmid-mediated [7] . A single organism can have both the mecha-nisms of resistance, and resistance to multiple antibiotics is often common [8],[9] .

The ability of N. gonorrhoeae to become resistant to cheap and effective antimicrobial agent is well-recognized since the introduction of sulphona-mide. Due to change in gonococcal antimicrobial susceptibility pattern and the emergence of peni-cillinase-producing N. gonorrhoeae (PPNG), plas-mid-mediated tetracycline-resistant N. gonorrhoeae (TRNG) and chromosomally-mediated resistance to penicillin and tetracycline in N. gonorrhoeae (CM-RNG PT ), and continuing development of fluoroqui-nolone resistance, the Centers for Disease Control and Prevention (CDC), Atlanta, GA, USA, recom-mends third-generation cephalosporins as the first-line therapy for uncomplicated gonorrhoea [10] .

Antimicrobial resistance in gonococci often spreads rapidly among countries, and infected travellers of-ten appear for treatment in countries distant from the source of infection [11] . Hence, data on local and regional antimicrobial resistance are impor-tant for the management and treatment of gonor-rhoea.

In Bangladesh, the national STI-management guideline recommended the use of ciprofloxacin as the first-line therapy for the treatment of uncom-plicated gonococcal infection during 1997- 2006, and there was no systematic antimicrobial suscep-tibility surveillance for N. gonorrhoeae in the coun-try. International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B) had initiated the antimicrobial susceptibility monitoring for N. gon-orrhoeae in Dhaka, the capital of Bangladesh, since 1997, and it was subsequently extended to three major cities (Chittagong, Jessore, and Sylhet). We report the antimicrobial susceptibility of N. gon-orrhoeae in Bangladesh during 1997- 2006 and, in particular, the emergence and spread of multidrug-resistant N. gonorrhoeae in Bangladesh.

Materials and Methods

Bacterial strain

All N. gonorrhoeae strains isolated from both male and female subjects from Dhaka and six major ci-ties (Chittagong, Sylhet, Faridpur, Mymensingh, Ba-risal, and Jessore) of Bangladesh during 1997- 2006 were studied. Isolates were collected as part of STI service-delivery programmes (for female sex work-ers in Dhaka and Jessore and for male having sex with male and male STI patients in Chittagong and Sylhet) established by ICDDR,B during 1997- 2003 or as part of different STI epidemiological studies conducted during 1997- 2006 in Dhaka, Jessore, Faridpur, Sylhet, Mymensingh, Chittagong, and Barisal. Isolates of N. gonorrhoeae were grown on modified Thayer-Martin medium (MTM) and incu-bated overnight at 37 0 C with 5- 10% CO 2 . All the isolates were identified as N. gonorrhoeae using con-ventional procedures, including colony morpho-logy, Gram-staining, oxidase and catalase tests, and carbohydrate-use test. Isolates were stored at - 86 0 C in tryptic soy-broth (TSB) with 20% glyce-rol until further study.

Minimum inhibitory concentrations

Minimum inhibitory concentrations (MICs) to penicillin, tetracycline, ciprofloxacin, ceftriaxone, spectinomycin, and azithromycin were deter-mined by an agar dilution method described ear-lier [12],[13] . The breakpoint criteria defined by the National Committee for Clinical Laboratory Stand-ards (NCCLS) were used for penicillin, tetracycline, ciprofloxacin, ceftriaxone, and spectinomycin, and the breakpoint criteria used for azithromycin were MIC of ≤ 0. 25 μg/mL for susceptible, ≥ 0. 5 of μg/mL for reduced susceptible, and ≥ 1 of μg/mL for resistance. Two-fold serial dilutions of antibi-otics were used: penicillin (Sigma, St. Louis, MO) 0. 06- 32 μg/mL, tetracycline (Sigma, St. Louis, MO) 0. 25- 64 μg/mL, ciprofloxacin (Bayer, Hampshire, United Kingdom) 0. 004- 32. 0 μg/mL, ceftriaxone (Sigma) 0. 004- 1. 0 μg/mL, spectinomycin (Upjohn, Puurs, Belgium) 8. 0- 128 μg/mL, and azithromy-cin (Pfizer Inc., Connecticus, USA) 0. 008- 1 μg/mL. Briefly, confluent overnight culture of N. gonor-rhoeae was suspended in TSB and adjusted to Mc- Farland turbidity 0. 5. Ten microlitre of the bacterial suspension ( 1x 104 cfu) was spotted on GC agar (Oxoid Ltd, Basingstoke, Hampshaire, UK) plates as recommended by the WHO, containing two-fold serial dilution of antimicrobial agents using a multi-point inoculator (Mast Diagnostic Ltd., SCAN 114). The quality control of the MIC test was ensured by including seven N. gonorrhoeae reference strains WHO A, B, C, D, E, G, and H with known MICs in each test, by repeating each test three times and by participating in the WPRO/SEARO GASP (West-ern Pacific Region Office/South-East Asia Regional Office/Gonococcal Antimicrobial Surveillance Pro-gramme) external quality-assurance programme (our data were in agreement with expected results for all antimicrobial agents during the study pe-riod).

Plasmid typing for PPNG and TRNG isolates

The plasmid type for the PPNG isolates was deter-mined by PCR detection of ( 3-lactamase-producing plasmid as described earlier [14] , and the plasmid type for the TRNG isolates was determined by PCR amplification of tetM gene in 25. 2-MDa conjuga-tive plasmid [15] . The primers for PPNG were de-signed to identify and distinguish Asia ( 7426)-, Africa ( 5599)-, and Toronto ( 5154)-type plasmid generating 4. 9 kb, 3. 1 kb, and 2. 6 kb amplicons res-pectively. The primers for TRNG were designed to identify and distinguish American and Dutch-type plasmids generating amplicon of 1600 bp and 700 bp respectively. PCR was carried out with boiled whole-cell suspension ( 1x 10 8 . CFU/mL) of N. gonorr hoeae grown overnight on MTM plate [14],[15] .

Phenotypic characterization

The criteria used for phenotypic characterization of N. gonorrhoeae were based on plasmid- and chromo-somally-mediated resistance to penicillin and tetra-cycline as described earlier [16] . Isolates resistant to three or more antimicrobial agents were considered multidrug-resistant N. gonorrhoeae.

Results

In total, 1, 767 gonococcal isolates were collected from males and females (population with high-risk behaviour and general population) from different parts of the country during 1997- 2006. In 1997, the antimicrobial susceptibility-monitoring programme for N. gonorrhoeae was introduced in Dhaka, the capital of Bangladesh, and was later ( 1999- 2003) extended to three major cities (Chittagong, Jessore, and Sylhet), in southeast, southwest and northeast parts of Bangladesh respectively. The programme was part of the STI service-delivery programme established by ICDDR,B. During 2004- 2006, the programme was implemented only in Dhaka. Be-sides this, N. gonorrhoeae isolates from different epi-demiological studies conducted during 1997- 2006 in Dhaka, Jessore, Faridpur, Mymensingh, and Ba-risal were also included in the study. The number, source, and year of isolation are shown in [Table - 1].

The MICs of penicillin, tetracycline, ciprofloxacin, ceftriaxone, spectinomycin, and azithromycin for all the isolates were determined. The antimicrobial susceptibility (resistant and reduced susceptible) of the isolates to penicillin, tetracycline, and cipro-floxacin during 1997- 2006 are shown in [Figure - 1] (a, b, and c). Approximately 9% of the isolates in 1997 were resistant to ciprofloxacin compared to 87% in 2006 with the highest ( 92%) resistance in 2003.

All the isolates were susceptible to ceftriaxone, azi-thromycin (MIC of ≤ 1 μg/mL), and spectinomycin, except that one isolate ( 0. 2%) in 2002 and one each isolate in 2003, 2005, and 2006 were resistant to azithromycin and spectinomycin respectively. The MIC at which 50% and 90% of the isolates were inhibited (MIC 50 and MIC 90 respectively) was determined for each year [Table - 2]. Although most isolates in the present study were susceptible to azithromycin, a gradual increase in MIC of azi-thromycin was observed during 2003- 2006 [Table - 2]. While none of the isolates had an MIC of ≥ 0. 25 μg/mL in 1997, approximately 25% of the isolates from 2003 had an MIC of ≥ 0. 25 μg/mL for azithro-mycin. No significant difference in resistance was observed among isolates collected from different populations and cities in a given year.

The presence of PPNG and TRNG among the iso-lates was determined by PCR. Approximately 14% of the isolates were PPNG in 1997 compared to 44% in 2006. Of the isolates from 1997, 20% were TRNG compared to 86% in 2006. None of the isolates was both PPNG and TRNG in 1997 and 1998 compared to 42% in 2006 [Figure - 2].

More than 90% of the isolates from 1997 to 2006 carried 3. 2-MDa African type PPNG plasmid. How-ever, 4. 5% ( 8/ 175) and 4. 5% ( 5/ 131) of the PPNG isolates of 2002 and 2003 respectively carried a Toronto-type plasmid respectively. Of the TRNG isolates, 11% ( 2/ 18), 2% ( 1/ 49), 7. 5% ( 9/ 119), 3. 2% ( 6/ 186), and 2% ( 5/ 252) in 1998, 1999, 2000, 2002, and 2003 carried 1600-bp American type tetM gene in the 25. 2-MDa conjugative plasmid respective-ly, and the remaining TRNG isolates carried 700 Dutch type tetM gene in the 25. 2-MDa conjugative plasmid (data not shown).

The prevalence of isolates resistant to three or more antimicrobial agents during 1997- 2006 was further determined. Six percent, 27%, 16%, 43%, 50%, 40%, 42%, 51%, 47%, and 44% of the isolates in 1997, 1998, 1999, 2000, 2001, 2002, 2003, 2004, 2005, and 2006 respectively were resistant to three or more antimicrobial agents. Of the multidrug-resistant isolates, none was both PPNG and TRNG in 1997 and 1998, and 33% ( 10/ 21), 62% ( 66/ 92), 61% ( 54/ 74), 66% ( 128/ 193), 64% ( 93/ 145), 59% ( 27/ 46), 63% ( 32/ 53), and 83% ( 24/ 29) of the isolates from 1999, 2000, 2001, 2002, 2003, 2004, 2005, and 2006 were both PPNG and TRNG respec-tively. One multidrug-resistant isolate from 2002 was both PPNG and TRNG and was resistant to cip-rofloxacin and azithromycin. Similarly, one multi-drug-resistant isolate from 2003 and one from 2005 were both PPNG and TRNG and were also resistant to ciprofloxacin and spectinomycin.

Discussion

The control of gonococcal infection is impor-tant considering the high incidence of acute infections, complications, and sequelae and its role in facilitating acquisition and transmission of HIV [17],[18] . The knowledge of antimicrobial susceptibility of N. gonorrhoeae is a prerequisite for the proper treatment and control of gonococ-cal infection. A regional programme for moni-toring gonococcal antimicrobial susceptibility has been established in developed countries, such as the USA, Canada, Australia, and The Nether-lands. However, in developing countries where the burden of disease is high and the resistance is the greatest, such activity rarely exists [2],[19],[20],[21] . In Bangladesh, there was no established antimicro-bial susceptibility surveillance for N. gonorrhoeae. In the absence of laboratory data and an estab-lished monitoring system, selection of appropri-ate antimicrobials for the empirical treatment of gonorrhoea is difficult. We initiated the anti-microbial susceptibility surveillance in Dhaka in 1997, and subsequently, the surveillance was ex-tended to three major cities.

We examined 1, 767 gonococcal isolates cultured from street-based, brothel-based, hotel-based fe-male sex workers, male STI patients, male having sex with male (MSM) population, male truckers, and male and female STI patients during 1997- 2006. Although the incidence of gonococcal infection among males and females with high-risk behaviour and from general population in Bang-ladesh is not known, the isolates could be reason-ably considered to be representative of gonococcal strains in the country based on the fact that the iso-lates tested in the study were cultured from differ-ent high-risk population and from different parts of the country.

A rapid increase in resistance to ciprofloxacin was observed during the study. Such increase in resist-ance has been documented in some Western pacif-ic countries, such as in China ( 85. 2%), Hong Kong ( 79. 5%, The Philippines ( 37. 9%), and Viet Nam ( 42. 7%) [2] . Ciprofloxacin has been extensively used in Bangladesh for the treatment of suspected gonorrhoea as it is relatively cheap and effective, and only a single oral dose is required. As a conse-quence of the long-time and large-scale use of this group of antimicrobial agents in areas where over-the-counter availability of drugs without prescrip-tion is common, a substantial increase in resistant strains may occur [22] . Data from the present study seem to reflect the consequence of the long-stand-ing usage of ciprofloxacin for the treatment of sus-pected gonorrhoea using syndromic management at STI clinics in Bangladesh.

Resistance to penicillin and tetracycline may be either chromosomally-mediated or plasmid-mediated. Chromosomally-mediated resistance to penicillin is of low-level resistance and results from additive effect of mutations at multiple loci, includ-ing penA, mtr, and penB while plasmid-mediated resistance is due to PPNG encoding a TEM- 1 type ( 3-lactamase. Approximately half of the isolates dur-ing the study were resistant to penicillin. Of the penicillin-resistant isolates, the prevalence of PPNG increased from 28% to 88% during 1997- 2006. Re-sults of plasmid analysis showed that most isolates carried an African type plasmid; however, isolates carrying Toronto-type plasmid were introduced in 2002, and there was a steady increase since then. All the isolates carrying Toronto-type PPNG plas-mid during 2002 were isolated from long-distance truck-divers, and in 2003, isolates carrying Toronto-type PPNG plasmid were isolated from sex workers in Dhaka. This might be due to acquisition of N. gonorrhoeae clone with Toronto-type PPNG plasmid by long-distance truckers and subsequent trans-mission to sex workers.

Although more than three-fourths of the isolates were resistant to tetracycline, it is not currently used for the treatment of gonorrhoea in Bangla-desh. This might be due to the fact that tetracycline is used for many other illnesses, and doxycycline is still used for the treatment of Chlamydia-associated infection in Bangladesh. High-level plasmid-medi-ated resistance to tetracycline is due to the acqui-sition of tetM gene by the conjugative plasmid of N. gonorrhoeae, resulting in a 25. 2-MDa plasmid. Tetracycline-resistant N. gonorrhoeae isolates are likely to spread more quickly than PPNG isolates because of the presence of tetM plasmid in other flora found in the genital tract that may act as a reservoir. Of the tetracycline-resistant isolates, the prevalence of TRNG increased from 30% to 95% during 1997- 2006. The increase in the prevalence of both PPNG and TRNG isolates might be due to acquisition of penicillinase plasmid in the TRNG isolates as transfer of penicillinase plasmid requires the presence of conjugative plasmid [23] .

The most striking finding of the present study is the emergence of isolates resistant to three or more antimicrobial agents. More than half of the isolates are resistant to three drugs, including ciprofloxacin, the first-line therapy for gonorrhoea. Of the multi-drug-resistant isolates, more then half were both PPNG and TRNG. Besides this, isolates resistant to four antimicrobial agents have also been identi-fied.

Antimicrobial susceptibility data play a major role in updating or revising the national guideline for the management of STIs. Based on our surveillance data, the National AIDS and STD Programme, Min-istry of Health and Family Welfare, Government of Bangladesh, has revised the national guidelines for the management of STIs in 2007 and recom-mended cefixime as the first-line therapy for gono-rrhoea. The current alternatives to quinolones for gonococcal infection are the extended spectrum or third-generation cephalosporins. All the isolates in the present study were susceptible to ceftriaxone and cefixime.

Considering the rapidly-changing pattern of gono-coccal antimicrobial susceptibility, it is important to maintain the antimicrobial susceptibility-moni-toring programme, periodical analysis of suscepti-bility data, and updating the treatment guidelines for successful STI/HIV intervention programmes.

Acknowledgements

This study was conducted at ICDDR,B with the support of Cooperative Agreement No. HRN-A- 00- 96- 90005- 00 from the United States Agency for International Development (USAID). ICDDR,B ac-knowledges with gratitude the commitment of US-AID to the Centre′s research efforts.

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