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Clinical

SHORT REPORT

Changing patterns of disseminated gonococcal

infection in France: cross-sectional data 2009–2011
Anna Belkacem,1 Eric Caumes,2 Jocelyne Ouanich,3,4 Vincent Jarlier,5 Sophie Dellion,1
Benoit Cazenave,1 Régis Goursaud,6 Flore Lacassin,6 Jacques Breuil,3,4 Olivier Patey,1
for the working group FRA-DGI
1
Department of Infectious and ABSTRACT The last two major reports on DGIs were pub-
Tropical Diseases, Centre Objectives Disseminated gonococcal infections (DGIs) lished in 1983 and 1994, and included 49 and 41
Hospitalier Intercommunal,
Villeneuve Saint Georges, are rare. We describe the characteristics of DGIs in patients, respectively.6 7 Therefore the question of
France France. modifications of DGI presentation during the last
2
Department of Infectious and Methods This is a 3-year retrospective analysis of DGI two decades can be raised. We evaluated the epi-
Tropical Diseases, Hopital cases collected through two networks of microbiologists demiological, clinical and microbiological features
Universitaire Pitié-Salpêtrière,
and infectious disease specialists in France between of DGI and the associated treatment and outcome.
University Pierre et Marie
Curie, Paris, France 2009 and 2011. DGI was defined either by the isolation
3
Department of Microbiology, of Neisseria gonorrhoeae from blood and synovial fluid
Centre Hospitalier or by the existence of a clinical syndrome consistent with MATERIALS AND METHODS
Intercommunal, Villeneuve DGI and the isolation of N gonorrhoeae from any site. We retrospectively studied cases of DGI observed in
Saint Georges, France France from 1 January 2009 to 31 December
4
College of Bacteriology,
We describe the epidemiological, clinical and
Virology and Hygiene Hospital microbiological characteristics and outcomes of DGIs. 2011. We asked the microbiologists of the ‘Collège
of Paris, Paris, France Results 21 patients (9 women, 12 men; 18–62 years de bacteriologie, virologie et d’hygiène hospitalière
5
Department of Microbiology, old) were diagnosed with DGI. The number of DGI cases de Paris’ (COL.BVH) and all the infectious disease
Hopital Universitaire Pitié- increased between 2009 and 2011. Two men who had (ID) specialists in France to report their cases. A
Salpêtrière, University Pierre et single anonymous questionnaire, filled out by one
Marie Curie, Paris, France sex with men were coinfected with HIV. We found 28
6
Department of Internal extragenital locations, including arthritis (14 cases), of the authors for patients hospitalised in the Paris
Medicine, Centre Hospitalier tenosynovitis (7), skin lesions (4), endocarditis (1), area or by the treating physician for patients in
Magenta, Nouvelle Calédonie prostatitis (1) and pelvic inflammatory disease (1). other areas, enabled data collection. DGI was
Correspondence to Genital signs were present in five patients. The diagnosis defined either by the isolation of N gonorrhoeae
Anna Belkacem, was confirmed by cultures in 20 patients—blood (4), from blood and synovial fluid or by the existence
Department of Infectious and synovial fluid (11), genital (3), throat (1), urine (1)—and of a clinical syndrome consistent with DGI and iso-
Tropical Disease, Hospital by molecular biology on a pharyngeal swab in 1 patient. lation of N gonorrhoea from a genital, oral, anal or
Villeneuve Saint Georges, 40
Seven cases were resistant to fluoroquinolones. The any other site. The diagnosis always relied on
Allée de la Source, Villeneuve
patients were treated with ceftriaxone, associated with culture or molecular biology based on the different
Saint Georges 94 195, France;
[email protected] corticosteroids (two cases) and surgery (six cases). Four infection site samples. Gonococcal isolates were
patients had joint sequelae. obtained after inoculation onto non-selective choc-
Received 4 March 2013 Conclusions DGIs are increasing. Men seem to be at olate agar and selective agar containing antimicro-
Revised 16 July 2013 bial agents that inhibit the growth of commensal
Accepted 20 July 2013 higher risk than women. Joint involvement was common.
Published Online First Microbiological diagnosis was based on culture, however bacteria and fungi and incubating them at 35–37°C
6 August 2013 molecular biology using pharyngeal swabs was helpful in a moist atmosphere enriched with CO2 for
when cultures were negative. 18–24 h.
We evaluated the epidemiological, clinical and
microbiological features, and the treatment admi-
nistered and the related outcome. The socio-
INTRODUCTION demographic information included age, sex, area of
Neisseria gonorrhoea infection was the second most residence in France and sexual orientation, such as
commonly declared sexually transmitted infection being a man having sex with a man (MSM).
(STI) in France in 2010.1 Moreover, according to History of STIs and antibiotics received during the
the monitoring networks RENAGO (Réseau previous 6 months were also evaluated. HIV infec-
National des gonocoques) and ResIST (Réseau de tion was systematically investigated. Behavioural
surveillance des Infections Sexuellement evaluation included the existence of a stable
Transmissibles),2 gonococcal infections are increas- partner or casual sex practices and recent travels.
ing in France and in other countries such as the We evaluated the following clinical items: body
USA3 and in Europe.4 temperature, skin manifestations, arthralgia, arth-
Disseminated gonococcal infection (DGI) has ritis, tenosynovotis, meningeal signs, dysuria, heart
been estimated to account for 0.5–3% of gonococ- involvement and any other signs.
To cite: Belkacem A, cal infections.5 DGI is usually referred to as a clin- Microbiological diagnosis was based on sample
Caumes E, Ouanich J, et al. ical triad with skin lesions, arthritis and cultures taken at different sites of infection or by
Sex Transm Infect tenosynovitis.6 7 Before the era of antibiotics, DGI molecular biology (PCR). The susceptibility of
2013;89:613–615. and gonococcal endocarditis were observed. N gonorrhoeae strains to different antibiotics

Belkacem A, et al. Sex Transm Infect 2013;89:613–615. doi:10.1136/sextrans-2013-051119 613

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Clinical

( penicillin, ceftriaxone, fluoroquinolones, spectinomycin, chlor- history of STIs (genital herpes, genital warts, Chlamydia tracho-
amphenicol and tetracycline) was evaluated with disc diffusion, matis, N gonorrhoeae and hepatitis B in two patients). One
as recommended by the national guidelines.8 Molecular strains MSM was HIV positive and efficiently treated with an undetect-
typing by N gonorrhoeae multiantigen sequence typing could able viral load. In addition, among the 20 remaining patients,
not be done. We assessed the antibiotic, need for surgery, use of one was found to be infected with HIV.
analgesics and anti-inflammatory drugs, treatment for coexisting Fourteen patients reported unprotected sex, including five
STIs and outcomes distinguishing clinical cure, relapse and with a steady partner and nine with casual partners, whereas the
sequelae. other seven patients did not specify this. Two patients had
sexual intercourse during recent travel abroad.
RESULTS Clinically, 28 extra genital locations were found: arthritis (14
Twenty-one cases of DGI were evaluated. There were 9 women cases), tenosynovitis (7), skin pustules or papules (4), aortic
and 12 men, including 5 MSM (table 1). The number of DGIs endocarditis (1), prostatitis (1) and pelvic inflammatory disease
increased from 2 in 2009 to 9 in 2010 and 10 in 2011. with septicaemia (1 case). Genital signs were observed in five
The median age was 30 years overall, 20 years in women patients, four men having urethritis and one woman with cervi-
(18–62 years) and 37 years in men (19–55 years). Ten patients citis. Among the five MSM, four had no genital symptoms.
lived in the Paris area and 11 elsewhere. Seven patients had a None were found with symptomatic pharyngitis.
Microbiological diagnosis relied on culture in 20 patients and
molecular biology in 1 patient. DGI diagnosis was based on 21
positive cultures from articular sites (11 cases), urethra (3),
Table 1 Epidemiological, clinical, and microbiological
throat (1), uterus (1), blood (4) and urine (1) as one patient had
characteristics of 21 French patients with DGI
a positive culture from a urethral swab and articular sample.
Years 2009 2010 2011 Total One MSM patient was diagnosed with molecular biology based
on a throat swab.
Patients (n) 2 9 10 21
Antibiograms revealed eight cases of resistance to penicillin
Epidemiological data
(38%), including three β-lactamase-producing strains. Five
Women 0 6 3 9 (43%)
strains were resistant to tetracycline and seven to fluoroquino-
Men 2 3 7 12 (57%)
lones (33%). All strains were susceptible to ceftriaxone, chlor-
MSM 1 1 3 5 (24%)
amphenicol and spectinomycin.
Median age (years) 54 20 35.5 30
Nineteen patients were initially treated with ceftriaxone,
Paris area 2 4 4 10
either prescribed alone with daily doses of 1 g (4 cases), 2 g (11
Other parts of France 0 5 6 11
cases) or 4 g (aortic endocarditis), or in combination with genta-
STI (excluding HIV) 0 5 1 6
micin (3 mg/kg/day for 5–7 days) in three patients (endocarditis,
HIV infected 0 0 2 2 (9.5%)
knee arthritis and temporo mandibular arthritis). Two patients
Clinical data
received treatment with amoxicillin (8 g/day for 7 days) and
Joints 1 7 6 14 (66%)
amoxicillin clavulanate (3 g/day). In two cases, ceftriaxone was
Knee 1 4 2 7
stopped due to fever with elevated liver enzyme rate, or neutro-
Elbow 1 1 0 2
paenia. The median treatment duration was 14 days and ranged
Ankle 0 1 1 2
from 1 week to 2 months (endocarditis). Six patients underwent
Wrist 0 0 2 2
surgery—there was one valve replacement and five cases of joint
Hand 0 0 2 2
lavage. Analgesics and corticosteroids were prescribed to two
Hip 0 1 0 1
patients with severe inflammatory synovitis while morphinics
TMJ 0 1 0 1
were prescribed in three other cases.
Skin 1 0 3 4 (19%)
Nine other STIs were treated, including eight, proven or
Tenosynovitis 1 1 5 7 (33%)
probable, infections due to Chlamydia trachomatis and treated
Hands 1 0 1 2
with a single dose of azithromycin or a 7-day course of doxy-
Leg 0 1 2 3
cycline. A patient with early latent syphilis received benzathine
Foot 0 0 1 1
benzyl penicillin.
Wrist 0 0 3 3
The overall outcome was good except for four patients with
Endocarditis 0 1 0 1 (4%)
articular sequelae (stiffness, oedema or residual pain) after a
Genital signs 0 3 2 5 (23%)
1-month follow-up.
Prostatitis 0 1 0 1 (4%)
PID 0 1 0 1 (4%)
DISCUSSION
Microbiologic data
This retrospective series points out a recent increase in DGI
Synovial fluid culture 1 4 6 11 (52%)
cases and highlights changes in the DGI presentation, such as
Blood culture 0 3 1 4 (19%)
male predominance, coinfection with HIV, the pharyngeal reser-
Pharynx culture 1 0 0 1 (4.7%)
voir and the high frequency of sequelae.
Urethra culture 0 3 2 5 (23%)
Obviously the number of DGI cases increased between 2009
Molecular biology pharynx 0 0 1 1 (4.7%)
and 2011. This increasing trend is consistent with data from the
Antibiotic resistance
Institut de Veille Sanitaire, showing that the number of declared
Penicillin 1 2 5 8 (38%)
cases of gonococcal infections went up from 397 in 2009 to
Fluoroquinolones 1 2 4 7 (33%)
534 in 2010 and 735 in 2011 in the ResIST network, and from
Ceftriaxone 0 0 0 0
1521 in 2009 to 1870 in 2010 and 1875 in 2011 in the
DGI, disseminated gonococcal infections; PID, pelvic inflammatory disease; STI, RENAGO network.2 This is similar to trends seen in the USA
sexually transmitted infection; TMJ, temporomandibular joint.
where the rate of gonorrhoeae for a population of 100 000

614 Belkacem A, et al. Sex Transm Infect 2013;89:613–615. doi:10.1136/sextrans-2013-051119

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Clinical

increased by 6% between 2009 and 2011,3 and in Europe (espe- considered in cases of arthritis in patients taking sexual risks.
cially in Finland, Portugal, Sweden, the UK) with an overall rate The diagnosis could benefit from the molecular biology tech-
of 10.4 per 100 000 population.4 nique applied to samples taken from all potential infection sites
The male predominance with a M:F sex ratio of 1:3 contrasts if cultures are negative, including the pharynx, which can be
with other large series of DGI cases. Indeed, in the two largest considered as a reservoir.
series, M:F sex ratios were estimated at 0.4 for patients included Handling editor Jackie A Cassell
between 1975 and 1982 and at 0.2 between 1985 and 1991.6 7 Acknowledgements We wish to thank the ‘Collège de bacteriologie, virologie et
Such a change is probably linked to modifications of sexual d’hygiène hospitalière de Paris’ (ColBVH) for assistance in identifying cases, and
behaviour, with increasing MSM corresponding to more than Maxime Romano for assistance in manuscript preparation.
50% of male patients, and fellatio as an important risk factor Handling editor Jackie A Cassell
for gonorrhoea as shown in other studies.9 In this study, DGI Collaborators Working Group FRA-DGI: Stéphane Jaureguiberry and Loic Epelboin
diagnosis was confirmed in two cases by throat swab, indicating (GH Pitié-Salpêtrière, Paris), Jean Luc Schmit (Amiens), Michèle Texereau (Niort),
the pharynx to be the forgotten reservoir for gonorrhoeae.9 Mickaël Meynard (Rennes), Valérie Zeller (Hopital de la Croix Saint Simon), Jean
Regarding the typical triad of arthritis, tenosynovitis and cutane- Beytout (Clermont Ferrand), Claudine Barbuat and Nicole Bouzigues (Nimes), Pierre
Delobel and Lydie Porte (Toulouse), Eric Auxenfants (Roubaix).
ous lesions, 4 patients had two of the triad signs and 14 had one
of the triad signs. Only one patient had all the triad signs whereas Contributors We guarantee that all authors have seen and approved the
manuscript.
the corresponding figure was not described in the two previous
studies.6 7 Of our 21 patients, 66% presented with arthritis Provenance and peer review Not commissioned; externally peer reviewed.
whereas joint involvement was diagnosed in 39% of 49 patients in Competing interests None.
Boston6 and 100% of 41 patients in North Carolina,7 but these Provenance and peer review Not commissioned; externally peer reviewed.
were the inclusion criteria in this latter study. Overall the most
commonly involved joint was the knee. In contrast, cutaneous
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Belkacem A, et al. Sex Transm Infect 2013;89:613–615. doi:10.1136/sextrans-2013-051119 615

 Downloaded from http://sti.bmj.com/ on June 2, 2015 - Published by group.bmj.com

Changing patterns of disseminated

gonococcal infection in France:
cross-sectional data 2009−2011
Anna Belkacem, Eric Caumes, Jocelyne Ouanich, Vincent Jarlier, Sophie
Dellion, Benoit Cazenave, Régis Goursaud, Flore Lacassin, Jacques
Breuil, Olivier Patey and for the working group FRA-DGI

Sex Transm Infect 2013 89: 613-615 originally published online August 6,
2013
doi: 10.1136/sextrans-2013-051119

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