Razali, Mohamed F.*; Fairley, Christopher K. PHD*†; Hocking, Jane PHD†; Bradshaw, Catriona S. PHD†‡; Chen, Marcus Y. PHD*†
From the *Melbourne School of Population Health, University of Melbourne, Australia; †Melbourne Sexual Health Centre, Alfred Hospital, Australia; and ‡Department of Epidemiology and Preventive Medicine, Monash University, Australia
The authors thank Afrizal and Jun Kit Sze for their assistance in data extraction, all the clinicians from Melbourne Sexual Health Centre who kindly completed surveys for this study, and staff at the Microbiologic Diagnostic Unit.
M.C. and C.F. came up with the concept for this study. All authors contributed to the design of the study. J.H. and M.R. performed the statistical analyses. All authors contributed to the writing and checking of the manuscript.
Correspondence: Marcus Y. Chen, PhD, Melbourne Sexual Health Centre, 580 Swanston St, Carlton, Victoria 3053, Australia. E-mail: email@example.com.
Received for publication October 6, 2009, and accepted February 2, 2010.
In a study of 6721 pharyngeal gonorrhoea culture results taken by 43 clinicians, there was a significant difference in the detection rate by individual clinician (0%–10%, median: 1.3%, P = 0.05). The detection rate was associated with the frequency with which clinicians reported inducing a gag reflex when taking pharyngeal swabs (P < 0.05).
In many countries men who have sex with men (MSM) are at high risk for bacterial sexually transmitted infections (STI) including gonorrhoea. Among MSM, gonorrhoea can infect the pharynx, urethra, and rectum and has been associated with an increased risk for HIV transmission.1 Pharyngeal gonorrhoea is common among MSM and is usually asymptomatic.2–4
Regular screening of MSM for bacterial STI such as gonorrhoea and chlamydia has been advocated as a key strategy for the control of these infections.5 Testing methods for the detection of gonorrhoea at the pharynx have included culture as well as nucleic acid amplification tests (NAATs). Studies suggest that NAATs are sensitive at detecting pharyngeal gonorrhoea than culture.6,7 However, because of concerns about the specificity of NAATs for the detection of gonorrhoea at nongenital sites,8 many sexual health services continue to use culture.
There are no published studies examining whether the technique of specimen collection from the pharynx affects the sensitivity of gonorrhoea detection. The aim of this study was to determine whether collection technique from the pharynx was associated with the detection rate for gonorrhoea at this site using culture.
This was a retrospective study of computer records of patients attending the Melbourne Sexual Health Centre, the main public sexual health service in Victoria, Australia. The centre operates a walk-in, triage clinic where MSM are managed as a priority population. Asymptomatic MSM were offered screening for chlamydia and gonorrhoea using culture for gonorrhoea from the pharynx and rectum and testing for chlamydia from first void urine, and a rectal swab using strand displacement assay (ProbeTec, Becton Dickinson, NJ). Pharyngeal specimens were collected using cotton swabs and plated at the time of collection onto modified Thayer Martin medium.
Routine epidemiologic data were collected at each client visit and entered onto a computer database by clinicians. We examined epidemiologic and testing data for all visits by MSM who attended the centre between January 2006 and November 2008. Victorian legislation requires individuals tested for HIV to return for results in person and retesting for gonorrhoea and chlamydia would not occur at this visit. Using these data, we calculated the detection rates for pharyngeal gonorrhoea for each clinician who worked at Melbourne Sexual Health Centre over the entire study period. The χ2 test was used to determine whether there was a difference in the detection rates for pharyngeal gonorrhoea between individual clinicians. Furthermore, clinicians were grouped into high and low detecting clinicians based on whether their individual detection rates were above or below the median detection rate for the group as a whole. We then compared the epidemiologic risk profile of MSM seen by these 2 groups of clinicians.
To ascertain how the clinicians obtained swabs for pharyngeal gonorrhoea, we conducted a questionnaire in January 2009 that sought to describe the technique used by clinicians during the study period. A diagram of the pharynx was provided with questions including the distance the pharynx was swabbed, the anatomical sites (for instance, tonsils vs. oropharynx) swabbed, and the frequency with which clinicians reported inducing a gag reflex when taking a pharyngeal specimen. Partial correlations between numeric variables obtained via the survey and detection rates for gonorrhoea controlling for the number of tests performed by each clinician were performed using SPSS. Ethical approval was obtained from the Alfred Hospital Research Ethics Committee.
In the 3-year period, there were 14,888 clinic visits by MSM who were seen by the 43 nurses and doctors who practiced at the centre throughout the whole study period. Pharyngeal specimens were collected for gonorrhoea at 6721 of these visits. The number of pharyngeal swabs taken by each clinician ranged from 9 to 560 (Table 1). The overall yield from testing by all clinicians was 1.6% (110 cultures positive). The detection rates by clinician are shown in Table 1. There was a significant difference in the detection rates between clinicians ranging from 0% to 10%, with the median being 1.3% (P = 0.05).
There was a significant correlation between the detection rate for pharyngeal gonorrhoea and the frequency with which clinicians reported inducing a gag reflex when collecting pharyngeal specimens (P = 0.009). There was no correlation between the detection rate for pharyngeal gonorrhoea and other variables such as the distance or anatomical site swabbed.
The epidemiologic profiles and STI diagnoses for MSM seen by high and low detecting clinicians are compared in Table 2. There was no significant difference in the age or the number of male sex partners reported by MSM seen by clinicians in the 2 groups. There was a higher prevalence of urethral chlamydia (3.5% vs. 2.5%, P = 0.019) and rectal gonorrhoea (3.7% vs. 2.1%, P = 0.001) among the MSM seen by high detecting clinicians compared with low detecting clinicians, respectively. When the prevalence for urethral chlamydia and frequency of reported gag reflex were entered into a logistic regression model, only the frequency of reported gag was significantly associated with the detection rate for pharyngeal gonorrhoea. When the prevalence of rectal gonorrhoea and the frequency of reported gag reflex were entered into a logistic regression model, both remained independently associated with the detection rate for pharyngeal gonorrhoea (Table 3).
To our knowledge, this is the first published study to examine whether sampling technique for pharyngeal gonorrhoea tested using culture affects its rate of detection. We found that the detection rate for pharyngeal gonorrhoea was associated with the frequency with which clinicians reported inducing a gag reflex when taking pharyngeal specimens. The findings suggest that the technique for collecting swabs for pharyngeal gonorrhoea may be important in optimizing detection of gonorrhoea from the pharynx when culture is used.
One of the strengths of this study was the large number of MSM who had pharyngeal swabs collected included in the sample. There are, however, a number of important limitations. Our questionnaires asked clinicians about how they collected pharyngeal specimens historically, that is, how they generally collected samples over a 3-year period. The responses were, therefore, prone to recall bias. Furthermore, clinicians provided only one overall summary figure for multiple episodes of specimen collection when the technique used is likely to have varied to some degree between consultations. We did not have data on the technique used during individual consultations.
It is possible that high detecting clinicians may have been seeing higher risk men, and therefore, detecting more pharyngeal gonorrhoea as a result. Although there was no difference in the average number of recent sexual partners reported by clients to low and high diagnosing clinicians, clinicians with a higher detection rate for pharyngeal gonorrhoea also detected more urethral chlamydia and rectal gonorrhoea. Adjusted analyses were performed to determine if differing gonorrhoea prevalence in the clients seen by high and low diagnosing clinicians was the basis for the increased detection of pharyngeal gonorrhoea, rather than the method of collection. These analyses showed that both the frequency of gag reflex reported during pharyngeal swabbing, and the prevalence of rectal gonorrhoea remained independently associated with the detection of pharyngeal gonorrhoea. Although it is possible that gonorrhoea may have been more prevalent in the clients seen by clinicians who diagnosed more pharyngeal gonorrhoea, the method of collection still appeared to be a significant factor in the detection of pharyngeal infection.
We hypothesize that those clinicians who induced gag reflexes more frequently were taking more thorough or extensive pharyngeal swabs, which induced more frequent gag reflexes but which also captured more material for culture. A prospective study that assessed different sampling techniques and detection rates for gonorrhoea in the pharynx would be required to provide definitive evidence as to whether technique determines the yield from swabbing at this site, although clearly such a study would need to be large and expensive.
It was clear in this study that there was wide variation not only in the detection rates for gonorrhoea but also techniques for specimen collection used by individual clinicians. If clinics are using culture for pharyngeal gonorrhoea, clinicians should be made aware of the importance of collecting an adequate sample with instructions on how a swab should be taken.
Concerns have been raised over the positive predictive value of NAATs for gonorrhoea at nongenital sites because of potential cross reactivity with other Neisseria species and false-positive results.8 However, studies suggest that NAATs are more sensitive at detecting pharyngeal and rectal gonorrhoea than culture.6,7 Several recent studies have shown self-collected rectal specimens for gonorrhoea using NAATs to be as sensitive as clinician collected specimens in detecting rectal infection in MSM, which point to the sensitivity of NAATs in the detection of gonorrhoea at nongenital sites.9–11 The results of this study suggest that the sensitivity of culture may be further undermined by inadequate collection technique.
1. Jin F, Prestage G, Imrie J, et al. Anal sexually transmitted infections and risk of HIV infection in homosexual men. JAIDS 2010; 53:144–149.
2. Lister NA, Smith A, Tabrizi S, et al. Screening for Neisseria gonorrhoeae and Chlamydia trachomatis in men who have sex with men at male-only saunas. Sex Transm Infect 2003; 30:886–889.
3. Morris SR, Klausner JD, Buchbinder SP, et al. Prevalence and incidence of pharyngeal gonorrhea in a longitudinal sample of men who have sex with men: The EXPLORE study. CID 2006; 43:1284–1289.
4. Ota Kaede V, Fisman David N, Tamari Itamar E, et al. Incidence and treatment outcomes of pharyngeal Neisseria gonorrhoeae and Chlamydia trachomatis infections in men who have sex with men: A 13-year retrospective cohort study. CID 2009; 48:1237–1243.
5. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2006. MMWR Recomm Rep 2006; 55(RR-11):1–49.
6. Schachter J, Moncada J, Liska S, et al. Nucleic acid amplification tests in the diagnosis of chlamydial and gonococcal infections of the oropharynx and rectum in men who have sex with men. Sex Transm Dis 2008; 35:637–642.
7. Page-Shafer K, Graves A, Kent C, et al. Increased sensitivity of DNA amplification testing for the detection of pharyngeal gonorrhea in men who have sex with men. CID 2002; 34:173–176.
8. McNally LP, Templeton DJ, Jin F, et al. Low positive predictive value of a nucleic acid amplification test for nongenital Neisseria gonorrhoeae infection in homosexual men. CID 2008; 47:e25–e27.
9. Alexander S, Ison C, Parry J, et al. Self-taken pharyngeal and rectal swabs are appropriate for the detection of Chlamydia trachomatis and Neisseria gonorrhoeae in asymptomatic men who have sex with men. Sex Transm Infect 2008; 84:488–492.
10. van der Helm JJ, Hoebe CJ, van Rooijen MS, et al. High performance of acceptability of self-collected rectal swabs for diagnosis of Chlamydia trachomatis and Neisseria gonorrhoeae in men who have sex with men and women. Sex Transm Dis 2009; 36:493–497.
11. Moncada J, Schachter J, Liska S, et al. Evaluation of self-collected glans and rectal swabs from men who have sex with men for detection of Chlamydia trachomatis and Neisseria gonorrhoeae by use of nucleic acid amplification tests. J Clin Microbiol 2009; 47:1657–1662.