Testing for pharyngeal gonorrhoea in heterosexual men: should we revisit national guidelines?

Abstract

Pharyngeal testing for Neisseria gonorrhoeae (gonorrhoea) in heterosexual men is not currently recommended in UK guidelines; however, it was being undertaken in a service in the North East of England for those presenting with urethral infection or as contacts of gonorrhoea. This service evaluation was performed to see if this practice should continue, or cease in line with national recommendations. The results revealed that 10% of contacts were positive in the pharynx only. Had this test not been performed, it would have left these patients without any treatment, as the current guidelines now discourage epidemiological treatment of contacts. Twenty-seven per cent of all heterosexual men diagnosed with urethral infection also had oropharyngeal gonorrhoea, with implications for persistent infection, had testing not been performed followed by a test of cure.

Keywords

heterosexual men

Introduction

Pharyngeal testing of gonorrhoea in heterosexual men used to be recommended in UK national guidelines in men with urethral gonococcal infection (suspected on urethral microscopy or laboratory confirmation) and those presenting as contacts of gonorrhoea. This changed in 2011¹ when pharyngeal testing in men was no longer recommended; no reason was given for this, and it was not mentioned in the ‘Changes since 2005 Guideline’ section at the start of the guideline. As this change was not highlighted, a level 3 service in North East England continued this practice. Current UK guidelines now state that extragenital testing should be ‘guided by an assessment of risk and symptoms’ in people who are not women or men who have sex with men (MSM).² Following this oversight being highlighted, a service evaluation was undertaken to assess if the practice should continue, or stop in-line with national recommendations. Rectal swabs have never been performed in heterosexual men in this service.

Methods

The service sees approximately 2600 heterosexual men per year and is situated in a major city. The prevalence of gonorrhoea in the local population is 75 per 100,000, with an overall increase in the North East of 23% between 2014 and 2018.³ The local database (Lilie) was searched for all men with a diagnostic code for gonorrhoea (B) or contact of gonorrhoea (PNG) between 1 August 2016 and 31 July 2018, as these were the only heterosexual men who should have had a pharyngeal swab (following local guidelines). Patients’ sexual orientation was self-reported. There is a local code, M, denoting MSM, and these were excluded from analysis. Electronic medical notes were then reviewed, sexuality was confirmed, and it was recorded whether a pharyngeal swab had been taken; the pharyngeal swab result; and the proportion of contacts that were positive for gonorrhoea. The assay used to test the swabs was the Cobas® 4800 CT/NG Test (Roche Molecular Systems, Branchburg, NJ, USA), which is a nucleic acid amplification test (NAAT).

Results

A total of 232 heterosexual men were coded as B or PNG; 131 men had a diagnosis of gonorrhoea in the urethra, either through microscopy or asymptomatic screening (excluding those presenting as contacts). In these patients, 80.9% (106/131) then had a pharyngeal swab performed, and 33% (35/106) of these pharyngeal swabs were positive for gonorrhoea (see Table 1). One patient had failed treatment and remained positive on the NAAT in the pharynx, despite clearing the urethral infection.

Table 1.

Summary of results.

	Number	% Pharyngeal swab performed (n)	% Positive in both urethra and pharynx (n)	% Urethra positive only (n)	% Pharyngeal positive only (n)
GC identified by NAAT/microscopy in the urethra	131	86% (106/131)	33% (35/106)^a	67% (71/106)^a	n/a
Contact of GC	101	85.1% (86/101)	8.1% (7/86)^b	80.2% (69/86)^b	11.6% (10/86)^b
Total	232	82.8%	21.9%	72.9%	11.6%

NAAT: nucleic acid amplification test; GC: Gonorrhoea.

Of those that had a pharyngeal swab, these patients already had a diagnosis of urethral gonorrhoea.

Of those that had a pharyngeal swab, this number may be underestimated.

A total of 101 men presented as contacts of gonorrhoea, with an overall positivity rate of 35.6% (36/101) (urethral and/or pharyngeal). A pharyngeal swab was performed in 85.1% (86/101) of patients, with 19.8% (17/86) being positive; 58.8% (10/17) of these patients were only positive in the pharynx; this represented 11.6% (10/86) of all pharyngeal swabs taken, 9.9% (10/101) of all contacts and 27.7% (10/36) of all positive gonorrhoea diagnoses in those presenting as contact of infection (see Table 1).

Overall, 22.4% (52/232) in both groups (urethral infection and/or presenting as contact), and 26.8% (42/157) of those with urethral infection, had oropharyngeal infection.

Discussion

Current national guidelines do not make any recommendations that heterosexual men should have pharyngeal swabs taken, unless they have a resistant strain isolated from the urethra, or it is suspected they acquired the infection in the Asia-Pacific region.² In this review, had the pharyngeal swabs not been taken, one in ten of all contacts would have gone undiagnosed, and in all heterosexual men with urethral infection, over one in four would have been unaware they had pharyngeal gonococcal infection. Had all in this review had a pharyngeal swab performed, these results may have been even higher.

The Cobas® 4800 CT/NG Test was the assay used to test the swabs. This assay has a specificity of 100% and a sensitivity of 99.7%.⁴ It should be noted that this test has not been validated for use within the European Economic Area (EEA) for testing at extra-genital sites, but has been internally validated in the laboratory and found to be suitable.

One patient (who only had a pharyngeal swab taken at his test of cure) failed treatment and remained positive in the pharynx by NAAT; unfortunately it could not be cultured. The urethral infection had cleared at test of cure. The infection in his oropharynx could have led to onward transmission, highlighting the need to ensure any oropharyngeal infection is identified and then cleared. It is well documented that oropharyngeal infection is more difficult to treat^5–8 and the national guidelines emphasise that those with oropharyngeal infection have a test of cure. Latest changes in the UK national recommendations state that epidemiological treatment is no longer routine²; therefore, had those presenting as contacts not been tested at the pharynx, they would be unaware and untreated, with missed opportunities for partner notification and prevention of onward transmission.

In recent years, there is a strong body of evidence for gonorrhoea transmission through kissing, and through the orogenital and ororectal route.^9–12 Some researchers have specifically looked at heterosexual men, finding up to 89% of contacts of gonorrhoea having solitary oropharyngeal infection,¹³ and 36% of all heterosexual men found positive for gonorrhoea, were only infected in the oropharyrnx.¹⁴ The majority of research has been performed in MSM, but the principals remain the same if the urogenital route of transmission is removed. These data were not specifically collected from this cohort of patients. The bacterial load in saliva has been found to be no different from that in the pharynx, regardless of culture positivity or negativity,¹⁵ meaning that heterosexual men have the same risk for acquiring oropharyngeal gonorrhoea as MSM and women. A study published in 2018 identified a ‘sexual network’ in Australia.¹⁶ It found that there was a disproportionately high incidence of oropharyngeal gonorrhoea in the absence of urogenital infection. There was a similar strain found in the pharynx of two people, separated in the network by two other participants, strongly suggesting that these infections were transmitted within the network as opposed to sexual contact with others.

As with any study, there are limitations to this service evaluation. Firstly, no specific behavioural data were collected from this cohort of patients, such as rimming or kissing. Also, we have to assume that the patients are being truthful when they state that they have had no sexual contact with men. The assay used, although internally validated as reliable, is not approved within the EEA for testing specimens from extragenital sites. None of the pharyngeal swabs taken for culture were positive. On one hand, this may not be surprising, given that gonorrhoea culture of the pharynx is only around 50% sensitive,^17–19 but it cannot be ruled out that some of these tests could be false positive results.

This service evaluation showed that pharyngeal testing in heterosexual men presenting as contacts of gonorrhoea, or positive for gonorrhoea in the urethra, is warranted and we plan to continue our current practice.

Footnotes

Acknowledgments

We wish to thank Dr Andrew Berrington, Consultant Microbiologist, Sunderland Hospital, for his advice and review of this article.

Declaration of conflicting interests

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

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Melissa Dresser

References

Bignell

Fitzgerald

UK national guideline for the management of gonorrhoea in adults. Int J STD AIDS 2011; 22: 541–547.

Fifer

, Saunders J, Soni S, et al. British Association for Sexual Health and HIV national guideline for the management of infection with Neisseria gonorrhoeae, ww.bashhguidelines.org/media/1208/gc-2019.pdf (2019, accessed 6 March 2020).

Public Health England. Spotlight on sexually transmitted infections in the North East. 2018 data, https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/828578/2019-08-20_NE_STISpot2019__1_.pdf (2018, accessed 6 March 2020).

cobas® 4800 CT/NG Test, Kit Insert Doc Rev. 14.0. Available from Roche®.

Moran

Levine

WC.

Drugs of choice for the treatment of uncomplicated gonococcal infections. Clin Infect Dis 1995; 20: S47–S65.

Eyre DW, Sanderson ND, Lord E, et al. Gonorrhoea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018. Euro Surveill 2018; 23: 1800323.

Fifer

Natarajan

Jones

, et al. Failure of dual antimicrobial therapy in treatment of gonorrhea. N Engl J Med 2016; 374: 2504–2506.

Moran

JS.

Treating uncomplicated Neisseria gonorrhoeae infections: is the anatomic site of infection important?

Sex Transm Dis 1995; 22: 39–47.

Fairley

Hocking

Zhang

, et al. Frequent transmission of gonorrhea in men who have sex with men. Emerging Infect Dis 2017; 23: 102–104.

10.

Cornelisse

Chow

Huffam

, et al. Increased detection of pharyngeal and rectal gonorrhea in men who have sex with men after transition from culture to nucleic acid amplification testing. Sex Transm Dis 2017; 44: 114–117.

11.

Barbee

Dombrowski

Kerani

, et al. Effect of nucleic acid amplification testing on detection of extragenital gonorrhea and chlamydial infections in men who have sex with men sexually transmitted disease clinic patients. Sex Transm Dis 2014; 41: 168–172.

12.

Chow

EPF

Cornelisse

Williamson

, et al. Kissing may be an important and neglected risk factor for oropharyngeal gonorrhoea: a cross-sectional study in men who have sex with men. Sex Transm Infect 2019; 95: 516–521.

13.

Chow

EPF

Chen

, Williamson DA, et al. Oropharyngeal and genital gonorrhea infections among women and heterosexual men reporting sexual contact with partners with gonorrhea: implication for oropharyngeal testing of heterosexual gonorrhea contacts. Sex Transm Dis 2019; 46: 743–747.

14.

Bamberger

Graham

Dennis

, et al. Extragenital gonorrhea and chlamydia among men and women according to type of sexual exposure. Sex Transm Dis 2019; 46: 329–334.

15.

Chow

Tabrizi

Phillips

, et al. Neisseria gonorrhoeae bacterial DNA load in the pharynges and saliva of men who have sex with men. J Clin Microbiol 2016; 54: 2485–2490.

16.

Cornelisse

Bradshaw

Chow

, et al. Oropharyngeal gonorrhea in absence of urogenital gonorrhea in sexual network of male and female participants, Australia, 2018. Emerging Infect Dis 2019; 25: 1373–1376.

17.

Bissessor

Whiley

Lee

, et al. Detection of Neisseria gonorrhoeae isolates from tonsils and posterior oropharynx. J Clin Microbiol 2015; 53: 3624–3626.

18.

Bachmann

Johnson

Cheng

, et al. Nucleic acid amplification tests for diagnosis of Neisseria gonorrhoeae oropharyngeal infections. J Clin Microbiol 2009; 47: 902–907. doi:10.1128/JCM.01581-08

19.

Page Shafer

Graves

Kent

, et al. Increased sensitivity of DNA amplification testing for the detection of pharyngeal gonorrhea in men who have sex with men. Clin Infect Dis 2002; 34: 173–176.