Pharyngeal gonorrhoea in men who have sex with men

Abstract

Pharyngeal gonorrhoea is important in the transmission dynamics of gonorrhoea, and generation of antimicrobial resistance and the performing of culture remains vital. We reviewed the notes of men who have sex with men (MSM) presenting to our clinic with a positive pharyngeal NAAT for gonorrhoea between January and December 2019. There were 383 cases of NAAT-positive pharyngeal gonorrhoea, and 28 (7%, 95% CI = 5.11–10.36) reported sore throat at presentation. Pharyngeal cultures were taken from 270/383 (70%), and 73/270 (27%) were culture positive with available antimicrobial sensitivities. Overall, the presence of pharyngeal symptoms was not associated with pharyngeal chlamydia (OR = 1.6, CI = 0.19–13.32, p = 0.7), HIV status (OR = 1.1, CI = 0.47–2.57, p = 0.8), positive cultures (OR = 1.9, CI = 0.78–4.62, p = 0.2) or age (p = 0.3). Routine screening of MSM for pharyngeal gonorrhoea is important to maintain surveillance and measures need to be taken to improve pharyngeal culture sampling from MSM.

Keywords

men who have sex with men pharyngitis HIV sexually transmitted infections

Introduction

Pharyngeal gonorrhoea is important in the transmission dynamics of gonorrhoea and the generation of antimicrobial resistance (AMR), so accurate diagnosis and management are key.¹ Antimicrobial resistance in gonorrhoea is on the Centre for Disease Control (CDC) watch list as an urgent public health threat.² Most cases of pharyngeal gonorrhoea in MSM are asymptomatic.^3–5 Diagnosis is made using highly sensitive Nucleic Acid Amplification Test (NAAT) combined with traditional culture and antimicrobial sensitivity testing which may be used for both for clinical decision-making and AMR surveillance.³ Factors associated with pharyngeal symptoms in MSM with pharyngeal gonorrhoea are not well understood.^4,5

Aims and methods

We aimed to audit the culture sampling in MSM with positive gonorrhoea NAAT, measure the sensitivity of gonorrhoea culture in our clinic, evaluate any differences between HIV-positive and HIV-negative MSM with pharyngeal gonorrhoea and evaluate the prevalence of symptoms and any associated factors from our clinic-based population of MSM in Brighton, UK. In our centre during the study period, it was usual practice for clinicians to collect pharyngeal NAAT. Positive NAAT undergo confirmatory testing using a second NAAT platform. Men who have sex with men are invited to attend for a test-of-cure visit, although this did not form part of our analysis for this study. The British Association of Sexual Health & HIV (BASHH) and our clinic guidelines state that all MSM with a positive pharyngeal gonorrhoea NAAT and all MSM being treated for gonorrhoea should have a pharyngeal gonorrhoea culture specimen taken before antibiotic treatment is initiated.³ Culture specimens were taken from MSM who were going to be treated for gonorrhoea because they had symptoms, were a sexual contact of gonorrhoea or had a positive NAAT. Cultures samples were taken by clinicians and directly plated and stored in a CO₂ incubator in the clinic before transportation to the laboratory in CO₂ containers. All MSM were offered treatment with ceftriaxone 1 g intramuscularly as per clinic guidelines.

Using our electronic patient record, we reviewed the anonymous clinical records of MSM who attended between January and December 2019 with a positive pharyngeal gonorrhoea NAAT (BD Probetec©). We audited whether gonorrhoea culture specimens (modified Thayer Martin©) were taken before antimicrobial treatment was given and estimated the sensitivity of culture compared to NAAT. We did not collect data on the test of cure visits, and we excluded re-infections within the study period. We also collected data on throat symptoms (soreness) if present, demographic information, and data on simultaneous pharyngeal chlamydia and urethral and rectal gonorrhoea. We excluded repeat testers within three months of treatment including test of cure samples from the analysis.

Results

During the study period, there were 6613 individual MSM attendances for Sexually Transmitted Infection (STI) testing (including pharyngeal gonorrhoea testing) and 383/6613 (5.8%) had NAAT-positive pharyngeal gonorrhoea (Figure 1). The median age was 36 (IQR = 28–45) years, and 103/383(27%) were HIV positive. HIV-positive MSM with pharyngeal gonorrhoea were significantly older than HIV-negative MSM (p = 0.0001) (Table 1). Overall, pharyngeal cultures were taken from 270/383 (70%) patients, and of these 73/270 (27%) were culture positive with available antimicrobial sensitivities. The 197/270 negative pharyngeal culture specimens had no growth on the gonorrhoea culture plate. Culture samples were taken from 24/28 (86%) of symptomatic MSM and 246/355 (69%) of asymptomatic MSM. Eight of twenty-four (33%) of symptomatic MSM were culture positive, and 65/246(26%) of asymptomatic MSM were culture positive. All positive cultures had available antimicrobial sensitivity data available. On review of the notes, themes for culture samples inadvertently not being taken from MSM with positive pharyngeal NAAT were; management of contacts of gonorrhoea, MSM with symptomatic and smear-positive urethral gonorrhoea, routine screening of MSM for HIV monitoring or HIV PrEP monitoring. Twenty-eight (7%, 95% CI = 5.11–10.36) reported throat symptoms (sore throat) at presentation. Nine (2%) had pharyngeal chlamydia co-infection, 66 (17%) had rectal gonorrhoea and 35 (9%) had urethral gonorrhoea. The presence of pharyngeal symptoms was not associated with pharyngeal chlamydia (OR 1.6, CI = 0.19–13.32, p = 0.7), HIV status (OR 1.1, CI = 0.47–2.57, p = 0.8), positive cultures (OR = 1.9, CI = 0.78–4.62, p = 0.2) or age (median 38 years [IQR = 33–45] vs 36 years [IQR = 28–45], p = 0.3). Only 7/73 (10%) had a fully sensitive organism, 65/73 (89%) had penicillin intermediate resistance or resistance, 38/73 (52%) ciprofloxacin intermediate resistance or resistance and 1/73 (1%) had intermediate azithromycin resistance. All MSM were treated with ceftriaxone, and there were no cases of cephalosporin resistance found.

Figure 1.

Flow chart of cases of pharyngeal gonorrhoea.

Table 1.

Symptomatic pharyngeal gonorrhoea in MSM (N = 383).

		Crude odds ratio or Mann–Whitney U test^&	95% CI	p
Pharyngeal chlamydia
Symptomatic	1/28 (4%)	1.6	0.19–13.32	0.7
Asymptomatic	8/355 (2%)
HIV positive
Symptomatic	8/28 (29%)	1.1	0.47–2.57	0.8
Asymptomatic	95/355 (27%)
Positive gonorrhoea culture
Symptomatic	8/24 (33%)	1.9	0.78–4.62	0.2
Asymptomatic	65/246 (26%)
Age (median), years
Symptomatic (n = 28)	38	4348^&		0.3
Asymptomatic (n = 355)	36
HIV positive (n = 103)	42	8419^&		0.0001
HIV negative (n = 280)	34

MSM: men who have sex with men.

Discussion

We have shown in this large single-centre study of MSM with pharyngeal gonorrhoea that 7% of MSM present with pharyngeal symptoms and that symptoms are not associated with pharyngeal chlamydia, HIV status, a positive gonorrhoea culture or age. HIV-positive MSM with pharyngeal gonorrhoea are older than HIV-negative MSM. All HIV-positive MSM in our cohort are offered STI testing including pharyngeal NAAT testing at their HIV monitoring visits, whereas HIV-negative MSM attend for STI testing either because they are symptomatic, contacts of an STI, HIV PrEP monitoring or because they are advised or wish to test for STI regularly. Although HIV-positive testers are likely to be significantly older than HIV-negative testers due to the ageing HIV-positive MSM populations, this study highlights the importance of sustained frequent pharyngeal testing among an ageing cohort of MSM with HIV. Overall, pharyngeal culture specimens were taken for gonorrhoea in 70% of cases; however, the sensitivity of culture is our clinic-based study was only 27% compared with NAAT. Negative culture samples in MSM with positive pharyngeal NAAT could be caused by poor sampling techniques, inadequate transport conditions of culture specimens from the clinic to the laboratory, low pharyngeal bacterial loads, spontaneous resolution of gonorrhoea between NAAT testing and culture testing or inadvertent use of antibiotics.^5,6 It is important that clinicians maintain high rates of pharyngeal culture specimens and optimise culture sensitivity data on pharyngeal gonorrhoea in MSM to provide adequate AMR surveillance data for the prevention of transmission of extensively drug-resistant gonorrhoea. Furthermore, NAAT should be used for the screening MSM for pharyngeal gonorrhoea due to the poor sensitivity of culture-based testing as demonstrated in our study. As only 7% of MSM reported throat symptoms and most MSM with pharyngeal gonorrhoea are asymptomatic, routine screening of MSM for pharyngeal gonorrhoea is important to maintain surveillance. There are little data on symptomatic pharyngeal gonorrhoea, and the presence of symptoms in previous studies and our study may be caused by other factors including viral infections.^4,5 We did not find any associations with symptomatic pharyngeal gonorrhoea, and to our knowledge, there are no other data examining associations with pharyngeal symptoms. We did not examine for the presence of other pharyngeal infections such as viruses or whether the MSM with symptoms were smokers, and further research is needed to establish why some MSM are symptomatic.

There are several imitations to our study including this being a retrospective clinical population where evidence of symptoms relied on documentation of throat symptoms and lack of control of sampling methods of individual clinicians and not all MSM would have been directly asked about pharyngeal symptoms. As this was a clinic-based population, the direct questioning of pharyngeal symptoms was not done routinely and to estimate the true prevalence of pharyngeal symptoms, prospective research is required. We did not estimate the proportion of omitted culture samples within the different themes we only identified. However, this study raises some interesting issues confirming low prevalence of symptoms of pharyngeal gonorrhoea in MSM and the importance of taking gonorrhoea culture specimens for MSM with pharyngeal gonorrhoea. Furthermore, the poor sensitivity of gonorrhoea culture may suggest that further training is required of clinical staff to increase sensitivity of culture. Data from Australia have suggested that staff training including elicitation of the gag reflex, increasing the time and surface area of culture sampling and taking specimens from the tonsillar bed and oropharynx and using both clinician and self-taken samples increase the sensitivity of culture.^6,7 Locally, we aim to introduce a training package to standardise and improve the quality of pharyngeal sampling in MSM. The rates of AMR in this population were higher than those reported in the rest of England overall; however, the contribution of resistance at the pharynx of MSM is not delineated in national reporting.⁸ Overall, we have found that routine culture sampling in MSM with positive pharyngeal gonorrhoea NAAT is low and sensitivity of gonorrhoea culture is very low; we need to improve both the rates of culture specimens taken and the quality of sampling by clinicians using bespoke and ongoing training of sexual health clinicians.

Footnotes

Authors’ contribution

DR designed the study. AP, DT, KN, ZB and JD collected the data. DR analysed the data, and all authors contributed to the final manuscript. DR is responsible for the overall content.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship and/or publication of this article.

ORCID iDs

Daniel Richardson

Daniel Trotman

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