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Articles/Issue/22/1/Table-Of-Contents PREVENT Surveillance for Antimicrobial Drug–Resistant Neisseria gonorrhoeae through the Enhanced Gonococcal Antimicrobial Surveillance Program Emily J. Weston, Teodora Wi, John Papp Monitoring trends in antimicrobial drug–resistant Neisse- drug–resistant N. gonorrhoeae has outpaced novel treatment ria gonorrhoeae is a critical public health and global health options; the third-generation cephalosporin ceftriaxone is security activity because the number of antimicrobial drugs among the most recent drugs currently being prescribed for available to treat gonorrhea effectively is rapidly diminishing. treatment against gonorrhea. Gonococcal resistance to peni- Current global surveillance methods for antimicrobial drug– cillin and tetracycline was first reported in Asia during the resistant N. gonorrhoeae have many limitations, especially in 1970s; resistance became widespread in multiple regions of countries with the greatest burden of disease. The Enhanced Gonococcal Antimicrobial Surveillance Program is a collabo- the world during the early 1980s. High levels of resistance ration between the World Health Organization and the Cen- to quinolones (e.g., ciprofloxacin) developed by the mid- ters for Disease Control and Prevention. The program aims to 2000s; the US Centers for Disease Control and Prevention monitor trends in antimicrobial drug susceptibilities in N. gon- (CDC) removed these drugs from recommended treatment orrhoeae by using standardized sampling and laboratory pro- regimens for gonorrhea in 2007 (4). Public health agencies in tocols; to improve the quality, comparability, and timeliness of most countries and the World Health Organization (WHO) gonococcal antimicrobial drug resistance data across multiple recommend treating gonorrhea with ceftriaxone in combina- countries; and to assess resistance patterns in key popula- tion with azithromycin in an attempt to slow simultaneous tions at highest risk for antimicrobial drug–resistant gonorrhea emergence of AMR to 2 unrelated compounds (5–9). How- so country-specific treatment guidelines can be informed. ever, recent reports suggest that this combination is becom- ing less effective in treating gonorrhea 10,11( ). acterial infections can cause disease ranging in se- An estimated 357 million new STIs were reported Bverity from mild to life-threatening, and resistance to among adults 15–49 years of age in 2012; 78 million of antibiotics may hamper treatment. Neisseria gonorrhoeae those new cases were attributed to gonorrhea (12). For is a common, worldwide sexually transmitted infection 2012, the global incidence rate of gonorrhea among men (STI) that can lead to severe reproductive sequelae, such was 24 cases/1,000 (regional range 13–41 cases/1,000); as pelvic inflammatory disease, infertility, ectopic preg- among women, the incidence rate was 19 cases/1,000 nancy, and epididymitis. If left untreated or improperly (WHO regional range 8–37 cases/1,000). Among men, es- treated, gonococcal infections can become disseminated timates for the incidence rate were highest in the Western and cause sepsis (1,2). In addition, infection may also fa- Pacific Region and second highest in the Southeast Asia cilitate HIV transmission (3). Region. Among women, estimates of incidence rate were also found to be the highest in the Western Pacific Region Emerging Antimicrobial Drug–Resistant but were documented next highest in the African Region. N. gonorrhoeae Adding to global burden estimates, many countries, N. gonorrhoeae has adapted to treatment through all mecha- especially those that are resource poor, have been un- nisms of antimicrobial resistance (AMR). Antimicrobial able to readily implement or improve laboratory diag- nostics for gonorrhea; therefore, syndromic surveillance Author affiliations: Centers for Disease Control and Prevention, is often used. Among male patients, WHO recommends Atlanta, Georgia, USA (E.J. Weston, J. Papp); World Health monitoring trends in urethral discharge as an indicator Organization, Geneva, Switzerland (T. Wi) of an incident gonococcal infection (13). However, syn- dromic surveillance is limited in the ability to assess the DOI: https://doi.org/10.3201/eid2313.170443 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 23, Supplement to December 2017 S47 PREVENT occurrence of gonorrhea because the data are difficult to by participating countries. These susceptibility data have interpret; other organisms, such as Chlamydia tracho- provided evidence to inform national, regional, and global matis, may cause urethritis; and some symptomatic men treatment guidelines. may not seek care. Further, inconsistencies in reporting There are many challenges in the current GASP frame- among countries may lead to difficulties in comparing work. The cumulative number of countries reporting AMR estimates (13,14). As with all communicable diseases, data for any antibiotic increased from 56 in 2009 to 77 in critical infrastructure for accurate epidemiologic practic- 2014. However, the number of countries reporting suscep- es and laboratory testing for N. gonorrhoeae should be tibility data for >1 antibiotic each year shows a declining in place for high-quality surveillance, and the ultimate trend, from 56 countries in 2009 to 52 countries in 2014. goal should be to reduce the incidence of gonococcal In 2014, the WHO European Region (n = 24 countries) infections. Incorporating surveillance with both epide- accounted for most reports in GASP; only 2 countries in miologic practices and laboratory testing to replace syn- Africa and 1 country in the Eastern Mediterranean Region dromic surveillance further prepares against the threat of provided data to GASP. The lack of reports from some antimicrobial drug–resistant gonorrhea and is imperative regions reflects the financial and laboratory constraints of in enhancing global health security. countries in resource-poor settings to implement GASP. In addition, a recent WHO survey from 108 countries showed Global Surveillance Activities for Antimicrobial that only 46% had conducted AMR testing for gonorrhea Drug–Resistant N. gonorrhoeae during the past 5 years (13). The AMR data for gonorrhea CDC’s Gonococcal Isolate Surveillance Program (GISP), a from GASP may be reported from differing countries from surveillance system established in 1986 to monitor trends year to year, making interpretation of trends difficult13 ( ). of antimicrobial susceptibilities of N. gonorrhoeae in the Globally, some countries have suboptimal surveillance United States, has been instrumental in documenting AMR systems and laboratory diagnostics because of limited epi- patterns of gonorrhea and the spread of resistance among demiologic and laboratory capacity and lack of political will different drug classes. Laboratory and epidemiologic data and funding (4). Very often, countries rely on syndromic collected through GISP are analyzed to estimate the pro- management of STIs, which limits their collection of isolates portion of isolates with resistance or decreased susceptibil- for susceptibility monitoring. This results in a vicious cycle ity in key populations; findings are disseminated annually of limited laboratory capacity to conduct antimicrobial sus- (15). In 2014, for example, data from GISP demonstrated ceptibility testing (AST); thus, sample sizes for AMR sur- increases in the prevalence of reduced susceptibility to veillance are limited. As a result, some isolates obtained in azithromycin and to cefixime. Data from GISP were used GASP are not systematically collected but are convenience to modify and inform US sexually transmitted disease samples, making it difficult to generalize findings. treatment guidelines (6). In a different setting, many resource-rich organizations The Gonococcal Resistance to Antimicrobial Surveil- have used nucleic acid amplification tests (NAATs) for di- lance Programme (GRASP) in the United Kingdom and agnosis of gonorrhea, which has also limited the collection the Australian Gonococcal Surveillance Program (AGSP) of cultures for AST. NAATs in particular can detect non- have also established country-specific surveillance systems viable gonococci, have high sensitivity compared to other to monitor trends in susceptibility to antimicrobial drugs diagnostic methods (especially for rectal and oropharyn- for treatment of gonorrhea. Member states of the European geal specimens), can be self-collected, can detect multiple Union participate in the European Gonococcal Antimicro- pathogens in 1 test, and can provide results rapidly (4). As bial Surveillance Programme (Euro-GASP). Though the a result, some countries in the GASP network have not col- methodologies of each surveillance system differ, all 3 lected a minimum sample size of 100 isolates of urethral surveillance programs analyze and disseminate susceptibil- discharge as recommended by WHO to confidently detect ity trend data similar to GISP (16–18). Data from each of a 5% resistance, the typical cutoff point used to inform re- these countries have also been used to inform local treat- vision of treatment recommendations (19,20). These small ment guidelines (7–9). sample sizes ultimately do not support comparison of data On a more global scale, the WHO Gonococcal Anti- across countries and regions (13) and assessment of trends microbial Surveillance Program (GASP), which is not re- over time. There are also issues related to quality of labora- lated to the Euro-GASP surveillance, has been collecting tory testing. Variation in AST methods and limited capac- gonococcal
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