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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

Chow, Eric P.F. PhD, MBiostat, MPH, MApplSc*,†; Chen, Marcus Y. PhD*,†; Williamson, Deborah A. PhD‡,§; Bradshaw, Catriona S. PhD*,†; Vodstrcil, Lenka A. PhD*,†; Trumpour, Sabrina MPA*,†; Howden, Benjamin P. PhD‡,§; Fairley, Christopher K. PhD*,†

doi: 10.1097/OLQ.0000000000001068
Original Studies
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Background There have been very limited studies of oropharyngeal gonorrhea in heterosexuals. Routine screening of oropharyngeal gonorrhea is not recommended in heterosexual contacts of gonorrhea. This study aimed to examine oropharyngeal gonorrhea positivity among heterosexuals reporting contact with a partner with gonorrhea.

Methods At the Melbourne Sexual Health Centre (MSHC), all heterosexual individuals reporting contact with sexual partners with gonorrhea are tested for genital gonorrhea. In May 2017, MSHC also included screening for oropharyngeal gonorrhea in heterosexual contacts of gonorrhea. All contacts of gonorrhea among women and heterosexual men between May 2017 and November 2018 were reviewed. Site-specific gonorrhea positivity was also calculated.

Results One hundred ninety-one gonorrhea contacts (102 heterosexual men and 89 women) were reviewed. The median age was 28 (interquartile range, 24–33) years. The gonorrhea positivity in males was significantly higher at the oropharynx compared with urethra (18%; 95% confidence interval [CI], 11% to 26% vs 2%; 95% CI, 0% to 7%; P < 0.001); and higher at the oropharynx compared with cervicovaginal site in women (46%; 95% CI, 35% to 57% vs 36%; 95% CI, 26% to 47%; P = 0.056). Of the 100 men who did not have genital gonorrhea, 17 (18%; 95% CI, 10% to 26%) tested positive at the oropharynx. Of the 55 women who did not have genital gonorrhea, 21 (24%; 95% CI, 15% to 34%) tested positive at the oropharynx. Infection at both the oropharynx and genital sites was not associated with sex worker status in women. Overall, 89% and 40% of gonorrhea in heterosexual men and women were only in the oropharynx, respectively.

Conclusions Oropharyngeal gonorrhea testing among heterosexual contacts of gonorrhea may be indicated given a substantial proportion of gonorrhea contacts are only infected at this site.

A study of heterosexuals reporting contact with a partner with gonorrhea at Melbourne Sexual Health Centre found that 18% of men and 46% of women had oropharyngeal gonorrhea.

From the *Melbourne Sexual Health Centre, Alfred Health

Central Clinical School, Monash University

Microbiological Diagnostic Unit Public Health Laboratory

§Doherty Applied Microbial Genomics, Department of Microbiology & Immunology, The University of Melbourne at The Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia

Acknowledgments: EPFC was supported by the National Health and Medical Research Council (NHMRC) Early Career Fellowship (GNT1091226). The authors would like to thank Afrizal Afrizal for his assistance with data extraction.

E.P.F.C., M.Y.C., and C.K.F. designed the study. E.P.F.C. performed the statistical analysis and wrote the first draft. S.T. performed the chart review. D.A.W. and B.P.H. contributed to the interpretation of laboratory results. All authors involved in data interpretation, critically revised the article for important intellectual content and approved the final version.

Conflict of interest: None declared.

Correspondence: Eric P.F. Chow, PhD, Melbourne Sexual Health Centre, Alfred Health, 580 Swanston Street, Carlton, VIC 3053, Australia. E-mail: eric.chow@monash.edu.

Received for publication April 2, 2019, and accepted September 4, 2019.

Online date: September 12, 2019

Gonorrhea is rising among gay, bisexual and other men who have sex with men (MSM) in many developed countries.1,2 In contrast, until relatively recently, it has been relatively uncommon among heterosexuals in those same countries.3–8 However, over the last 5 to 10 years, gonorrhea cases in heterosexuals have now also risen and antimicrobial resistance is increasing, meaning this is an emerging public health threat.9,10 For example, in Melbourne, the gonorrhea positivity by culture has increased significantly in women (from 0.3% to 1.2%) and heterosexual men (from 0.5% to 1.0%) attending a sexual health clinic between 2008 and 2015.8,11 It is hypothesized that the rise in gonorrhea may have been associated with the changes in sexual practice over time, but 2 large Australian community-based surveys suggest that there were no changes in consistent condom use and the number of sexual partners among heterosexuals during the same period.12 The reasons for the rising number of cases in heterosexuals remain unclear due to the lack of comprehensive longitudinal behavioral surveillance in Australia.

Key to implementing successful control programs for gonorrhea is determining which anatomical sites are commonly infected so they can be appropriated tested. In Australia and most countries, testing for gonorrhea at the urogenital site is recommended among heterosexuals reporting exposure to gonorrhea. Testing of the oropharynx is only specifically recommended in the United Kingdom and Australia, and it is for only women who have performed fellatio.13,14 Screening of the oropharynx is not recommended in heterosexual men or women who do not report performing fellatio with their sexual contact. A recommendation based on a specific sexual practice may be difficult to implement in primary care where cases are infrequently seen. Therefore, it is possible that some individuals with oropharyngeal gonorrhea infection would remain untreated if only genital screening is performed. This study aimed to examine the positivity of oropharyngeal gonorrhea among gonorrhea contacts in women and heterosexual men in a sexual health clinic setting.

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METHODS

This was a cross-sectional study conducted at the Melbourne Sexual Health Centre (MSHC), the largest publicly funded sexual health clinic, in Victoria, Australia. Before May 2017, women and heterosexual men attending MSHC who reported sexual contact with partners with gonorrhea (henceforth referred to as “contact”) were then tested for genital gonorrhea. In May 2017, MSHC began to include oropharyngeal gonorrhea testing among gonorrhea contacts in women and all men including heterosexual men on the day of the presentation.

As part of routine clinical management and care, oropharyngeal gonorrhea was tested by clinician-collected oropharyngeal swab; and genital gonorrhea was tested by first-void urine, or clinician-collected high-vaginal or cervical swabs in women. All samples were tested by the Aptima Combo 2 assay using the amplification technology of transcription-mediated amplification (Hologic Gen-Probe PANTHER System; San Diego, CA) during the study period.

The data of all gonorrhea contact cases in women and heterosexual men presented to MSHC between May 2017 and November 2018 were extracted from the clinic's database. We extracted demographic characteristics (eg, age, gender, and country of birth) and behavioral factors (eg, sex work status and sexual orientation) of the cases reporting contact with gonorrhea. Sexual orientation was categorized into heterosexual (ie, had sex with partners of the opposite gender only in the past 12 months) or homosexual/bisexual (ie, had sex with partners of the opposite and/or same gender in the past 12 months). For men, only heterosexual men were included in this analysis and homosexual/bisexual men were excluded. This study focused on heterosexuals because we have previously reported gonorrhea positivity by anatomical site among MSM and oropharyngeal gonorrhea screening is part of the routine sexually transmitted infections screening in all MSM.15,16 All women, regardless of their sexual orientation, were included in this analysis. Information on the symptoms among gonorrhea contacts was extracted from chart review. We only included individuals who were tested for both genital and oropharyngeal gonorrhea on the same day they presented at MSHC. The positivity of gonorrhea at the genital and oropharyngeal sites among gonorrhea contacts was calculated by gender. The proportion of oropharyngeal infections that would have been missed by genital-only testing was calculated. We also performed sensitivity analyses on the site-specific gonorrhea positivity by gender that restricted to asymptomatic contacts only. Ethical approval was obtained from the Alfred Hospital Ethics Committee, Melbourne, Australia (640/17).

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RESULTS

There were 46,480 clinical consultations for heterosexual men and women during the study period, including 242 consultations (138 men and 104 women) where a woman or heterosexual man reported contact with a sexual partner with gonorrhea. Of the 242 gonorrhea contacts, 191 (79%) individuals (102 men and 89 women) were tested for both genital and oropharyngeal gonorrhea on the same day they presented at MSHC and were included in the final analysis. There were 40 gonorrhea contacts (10 men and 30 women) who attended the clinic because of the presence of symptoms.

Table 1 shows the demographic characteristics of the heterosexual men and women who reported contact with a partner with gonorrhea. Heterosexual men were older than women (median age, 30 years vs 27 years; P = 0.003). The majority of women were born in Australia (60%) but the majority of heterosexual men were born overseas. Twenty-nine percent of women were bisexual or women who have sex with women only. All individuals were not living with human immunodeficiency virus. Women more commonly worked in the sex industry than men (18% vs 1%; P < 0.001). Of the 102 men and 89 women, 18% (95% confidence interval [CI], 11% to 26%; n = 18) and 46% (95% CI, 35% to 57%; n = 41) tested positive for gonorrhea at the oropharynx, respectively.

TABLE 1

TABLE 1

Of the 102 gonorrhea contacts in heterosexual men, gonorrhea positivity at the oropharynx (18%; 95% CI, 11% to 26%; n = 18) was 9 times as high as at the urethra (2%; 95% CI, 0% to 7%; n = 2; P < 0.001). Of the 92 asymptomatic gonorrhea contacts in heterosexual men, the gonorrhea positivity at the oropharynx was 18% (95% CI, 11% to 28%; n = 17) and at the urethra was 1% (95% CI, 0% to 6%; n = 1). Of the 2 men with urethral gonorrhea, 1 presented with urethral symptoms (ie, urethral discharge and dysuria for 3 days) but he tested negative for gonorrhea at the oropharynx; the other man was asymptomatic but tested positive for gonorrhea at the oropharynx and his female partner was also diagnosed with oropharyngeal gonorrhea when he first reported as a “gonorrhea contact” of this female partner. Of the 100 men who did not have genital gonorrhea, 17% (95% CI, 10% to 26%; n = 17) of men tested positive at the oropharynx.

Of the 89 gonorrhea contacts in women, gonorrhea positivity at the oropharynx was higher (46%; 95% CI, 35% to 57%; n = 41) than at the cervicovaginal site (36%; 95% CI, 26% to 47%; n = 32; P = 0.056). Of the 59 asymptomatic gonorrhea contacts in women, gonorrhea positivity at the oropharynx was 34% (95% CI, 22% to 47%; n = 20) and at the cervicovaginal site was 44% (95% CI, 31% to 58%; n = 26). Of the 55 women who did not have cervicovaginal gonorrhea, 38% (95% CI, 25% to 52%; n = 21) tested positive at the oropharynx. Women had a higher proportion of multiple-site infection compared with heterosexual men (23% vs 1%; P < 0.001).

Figure 1 shows that 89% (95% CI, 67% to 99%) of oropharyngeal gonorrhea cases would have been missed by genital-only testing among gonorrhea contacts in heterosexual men. Similarly, 40% (95% CI, 26% to 54%) of oropharyngeal gonorrhea cases would have been missed by genital-only testing among gonorrhea contacts in women, regardless of sexual orientation and sex workers status.

Figure 1

Figure 1

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DISCUSSION

In this study, we found that oropharyngeal gonorrhea was very common among women and heterosexual men who reported recent sexual contact with someone reporting to have gonorrhea. Importantly, most infections were detected at the oropharynx only. This finding suggests that testing heterosexual contacts for oropharyngeal gonorrhea should be routine practice which is not recommended in the current sexually transmitted infection management guidelines.14 The latest (2019) UK guidelines recommend gonorrhea treatment should only be given to contacts who test positive for gonorrhea.17 This means oropharyngeal gonorrhea cases among gonorrhea contacts in heterosexuals would be missed and left untreated if not tested for oropharyngeal gonorrhea. We found that oropharyngeal gonorrhea was common in gonorrhea contacts also raises the question of how common oropharyngeal gonorrhea might be relative to genital infection in the general heterosexual population given oropharyngeal gonorrhea is almost always asymptomatic and virtually never tested for.

This study has several limitations. Firstly, this study was conducted at a single sexual health clinic and if there was unrecognized bias operating the findings will not be representative of the populations at other clinical services. It is likely that sex workers and bisexual women were over-represented among women. More studies on gonorrhea contacts among heterosexuals in other settings are warranted. Secondly, our findings are dependent on the assumption that individuals accurately reported that they had been in contact with someone with gonorrhea because we could not independently verify this. Thirdly, data on sexual practices such as number of episodes, last sexual contact, kissing, and oral-genital sex were not collected as part of the routine clinical care at our clinic. Therefore, we were unable to identify the risk factors for the site-specific gonorrhea diagnoses.

Few studies have examined the prevalence of oropharyngeal gonorrhea in heterosexuals and most are restricted to women.18 A small Sydney-based study reported that 27% (9/33) of women had oropharyngeal gonorrhea among all gonorrhea cases between 2008 and 2012 but the authors did not report how many of the 33 women were tested for oropharyngeal gonorrhea.9 Both studies have found that the majority of cases did not involve sex workers. The lower proportion of oropharyngeal infection among cases of gonorrhea found in the Sydney study than we found could be explained because the Sydney study used culture which is much less sensitive than nucleic acid amplification test for the detection of oropharyngeal gonorrhea.19,20 It is also possible that the risk profile of women differ between the 2 studies. We are unable to make the comparison in heterosexual men because the Sydney study did not report the proportion of oropharyngeal gonorrhea in heterosexual men. Our findings are also consistent with a recent study in Melbourne showing gonorrhea is more common in the oropharynx (2%) than in the cervicovaginal site (1%) among female sex workers through 3-monthly screening.21

We found that 18% of heterosexual male gonorrhea contacts had oropharyngeal gonorrhea but only 2% had urethral gonorrhea. Studies in the 1970s estimated that 40% of asymptomatic male contacts had urethral gonorrhea,22 which contradicts to studies published in the 2010s estimating at least 90% of men develop symptoms in the urethra soon after infection with gonorrhea.23,24 It is, therefore, possible that men would develop urethral symptoms and attend a clinic for gonorrhea treatment before being informed by their female partners that they were a contact of gonorrhea.25 Handsfield and colleagues26 reported that 6% of the 177 heterosexual men with urethral gonorrhea also had oropharyngeal gonorrhea. Similarly, there were 81 heterosexual men with symptomatic urethral gonorrhea who were tested for oropharyngeal gonorrhea at our clinic during the same period, 20 (25%) men had oropharyngeal gonorrhea (unpublished data). In contrast, women are less likely to develop symptoms and may present later when their male partner has been already diagnosed and contacted them. This difference may explain why so few men, presenting as contacts had urethral infection and therefore why 89% of male cases were oropharyngeal infections. However, this contrasts with a study conducted by Thomson-Glover et al27 from a clinic in England where oropharyngeal gonorrhea testing is routinely done among heterosexual men diagnosed with urethral gonorrhea or who report contact with a female with gonorrhea. Authors have found that, of the 97 gonorrhea cases in heterosexual men, 9 (11%) cases had oropharyngeal gonorrhea and 2 (2%) men were positive for gonorrhea by culture at the oropharynx only but not at the urethra. The difference between the 2 studies may due to the different definition of gonorrhea contacts as Thomson-Glover et al also included men who were diagnosed with urethral gonorrhea by nucleic acid amplification test or culture. In addition, our data suggest that gonorrhea positivity at the cervicovaginal site was notably lower among symptomatic women compared with asymptomatic women, while gonorrhea positivity at the oropharynx was notably higher among women reporting symptoms compared with women not reporting symptoms. We do not have an explanation for this finding although we noted that that symptomatic women were more likely to be sex workers although these differences were not statistically significant. Further studies with a larger sample size will be required to confirm this observation.

Our study does not provide an answer to the question of whether heterosexuals in communities with a relatively low prevalence of gonorrhea should now be tested at the oropharynx as well as the generally recommended genital screening. This would require a separate study that carefully assesses the prevalence, the rate of false positive results and cost effectiveness of such a screening recommendation. However, our results do suggest that heterosexual male and female contacts of gonorrhea, should be tested for oropharyngeal gonorrhea routinely. Our study found that among contacts of gonorrhea most cases were oropharyngeal and not genital and would have been missed without oropharyngeal testing. Indeed this is now routine policy in our clinic.

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