Sexually transmitted infections (STI) caused by Neisseria gonorrhoeae (NG) present a high global incidence and significant associated morbidity. Furthermore, NG has developed resistance to all antibiotics prescribed for its treatment.1 In the last years treatment failures with third generation cephalosporins have been reported which may lead to untreatable gonorrhea in the near future.1 In fact, the latest report from the European Gonococcal Antimicrobial Surveillance Programme (Euro-GASP, 2013) identified a high proportion (4.7%) of NG isolates with decreased susceptibility to cefixime and 7 isolates with decreased susceptibility to ceftriaxone. Rates of ciprofloxacin, penicillin (high-level resistance) and azithromycin resistance were also too high (53%, 12.9% and 5.4%, respectively) to recommend as first-line therapies.2 However, few data regarding risk factors associated with antibiotic resistant-NG are available in Europe.3 Our aims were to study the susceptibility of NG isolates obtained in our center and determine a possible link between epidemiological and behavioral characteristics of patients infected and the antimicrobial susceptibility profile of their NG strains.

From June 2009 to December 2014, 286 NG isolates were obtained. We included 110 samples of NG infection for which epidemiological and behavioral data were available.

These samples were from 101 patients. Five patients suffered 2 NG infections, and 2 patients 3 different events. All these cases were sufficiently separated in time to consider them as independent infections.

Table 1 shows the socio-demographic, clinical, and behavioral data of the cases included. Mean age was 31.4 years and 96.4% (n=106) were male. Men who have sex with men (MSM) represented 73.3% (n=66) of patients and 41% (n=45) were infected with human immunodeficiency virus (HIV). Samples were collected from urethral 85.9% (n=98), 8.7% rectal (n=10), 1.7% pharyngeal (n=2), and 2.6% vaginal sites (n=3). When comparing characteristics of patients according to their HIV status (see Table 1), we found that among our patients with gonococcal infection, concomitant HIV infection was significantly associated with age (7.1% vs 8.2%, p<0.001), MSM (61.3% vs 38.7%, p<0.001) and history of previous STI (76.7% vs 23.3%, p<0.001). Risky sexual behavior such as sexual activity in foreign countries (46.0% vs 16.3%, p=0.004) and use of cocaine (24.4% vs 3.5%, p=0.001) or cannabis (20.0% vs 5.2% p=0.02) before sexual intercourse were also significantly associated with HIV infection.

Unprotected sex before symptoms appeared in 88.1% (n=89) of the patients and drug use before having sex within the last 12 months before diagnosis in 48.2% (n=42). Coinfection with other STI (different from HIV) at the time of diagnosis was found in 22.6% (n=24) while 57.0% (n=53) had been previously diagnosed with another STI (see Table 1).

A particular finding from our study sample of NG infection cases is the high prevalence of foreign patients, MSM, patients engaging in unsafe sexual behavior and HIV patients compared to previous studies on these topics.3 A recent official report on gonococcal surveillance in our region5 observed that 85% of infections occurred in men (compared to 96.4% in our study); 46% were MSM (73.3% in our study); 19% were HIV+ (41% in our study), and 26% were born out of Spain (41% in our study). Our STI Unit is part of a tertiary care hospital with an important HIV department, located in the downtown area of a large city. The origin of our patients may explain the lack of representativeness of the general population. However, we consider that these differences do not affect the main findings of the study.

In our unit we attend patients with symptomatic STI, which explains that most of our samples were collected from urethral site as most cases of pharyngeal and anorectal NG infection are asymptomatic.

One striking point is the significant increase of STI incidence in MSM with a high HIV coinfection rate, a worrisome problem previously reported in our city,6 corroborated by the high incidence of non-protected sex reported among patients included in our study. In fact, MSM as a vulnerable population for STI and HIV infection in major European cities is currently a primary concern to public health.7

Our data showed a significant association between heterosexual men and being a carrier of ciprofloxacin resistant or any AMR strains. Recent studies have linked AMR gonococcal infections with both heterosexual and MSM networks across Europe and USA.2,3,8 An association between AMR gonococcal infections and heterosexual men in European countries has been recently reported.3 We consider that associations between AMR isolates and HIV are likely confounded by MSM.

Our results also reveal an association between AMR to 3rd generation cephalosporins and unsafe sexual behavior. Several studies have previously linked AMR-NG infection with risky sexual behavior such as sex with sex workers and recent foreign travel.8 Concurrent STI was also associated with resistance to cefotaxime. We can presume that patients engaging in risky sex behavior and concurrent infections might have been previously been infected with others STI and therefore treated with antibiotics which could have led to the development of a resistant infection. Accordingly, carriers of AMR strains were associated with previous NG infection.

We also found a significant association between age and being carriers of ciprofloxacin and cefotaxime resistant isolates or any AMR strains which has previously been reported.3,7,9

Our main limitation is the relatively low number of patients included in the study. Selection and information bias may have been introduced by excluding patients from whom data were not available and by using confidential interviews as the data collection method. We consider that these limitations do not invalidate the main objective of the study which was to determine epidemiological and behavioral risk factors for acquiring AMR NG.

Most of our results support previous data recently reported on this issue2,3,7,8 including the European guidelines recommendation2,10 to avoid ciprofloxacin, azithromycin and penicillin as empirical treatment for gonorrhea in our patients. This study also underlines the need to implement effective interventions to control the extension of STI through core groups of MSM, especially those coinfected with HIV, in large cities of Western Europe.

We consider that improved data about risk factors linked with AMR gonococcal infection are required to identify evidence-based risk groups. Accessible and high quality STI services for these key groups are essential to control this infection.

Drs. Fuertes and Baliu had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Drs. Fuertes, and Bosch. Acquisition of data: Drs. Fuertes, Vergara and Alsina. Analysis and interpretation of data: Drs. Fuertes, Baliu and Vallés. Drafting of the manuscript: Drs. Fuertes, Alsina and Bosch. Critical revision of the manuscript for important intellectual content: Drs. Fuertes, Bosch and Alsina. Statistical analysis: Drs. Fuertes and Baliu.

This study was supported in part by the Hospital Clinic de Barcelona. The sponsors had no role in the design and conduct of the study; in the collection, analysis, and interpretation of data; or in the preparation, review, or approval of the manuscript.

None reported.

None declared.