ABSTRACT
The coronavirus disease 2019 (COVID-19) pandemic has led many clinics to move from clinician-collected to self-collected oropharyngeal swabs for the detection of sexually transmitted infections (STIs). Before this change, however, self-collection was used primarily for genital and anorectal infections, with only limited studies on the performance of self-collection of oropharyngeal swabs for oropharyngeal STI detection. The Melbourne Sexual Health Centre (MSHC) changed from clinician-collected to self-collected oropharyngeal swabs for oropharyngeal gonorrhea and chlamydia screening on 16 March 2020 in order to reduce health care worker risk during the COVID-19 pandemic. We compared the proportions of valid and positive samples for gonorrhea and chlamydia among men who have sex with men (MSM) in two time periods; the clinician collection period, between 20 January and 15 March 2020, and the self-collection period, between 16 March and 8 May 2020. A total of 4,097 oropharyngeal swabs were included. The proportion of oropharyngeal swabs with equivocal or invalid results for Neisseria gonorrhoeae was higher in the self-collection period (1.6% [24/1,497]) than in the clinician collection period (0.9% [23/2,600]) (P = 0.038), but the proportions did not differ for the detection of Chlamydia trachomatis. The positivity rates of oropharyngeal N. gonorrhoeae (adjusted prevalence ratio [PR], 1.07 [95% confidence interval {CI}, 0.85 to 1.34]) (P = 0.583) and oropharyngeal C. trachomatis (adjusted PR, 0.84 [95% CI, 0.51 to 1.39]) (P = 0.504) specimens did not differ between the two periods. Self-collected oropharyngeal swabs for the detection of N. gonorrhoeae and C. trachomatis have acceptable performance characteristics and, importantly, reduce health care worker exposure to respiratory infections.
INTRODUCTION
Self-collected genital and anorectal specimens for the screening of sexually transmitted infections (STIs) have been widely adopted by clinical services worldwide, since the sensitivity and specificity of self-collected samples are comparable to those of clinician-collected specimens (1–4). Self-collected genital and anorectal specimens not only provide greater privacy and minimize patient embarrassment but also are cost-effective and highly acceptable (3, 5–7). However, clinician-collected oropharyngeal swabs are still used for screening for oropharyngeal STIs because of the difficulties in self-swabbing the posterior pharyngeal wall and tonsils without touching the tongue and eliciting the gag reflex (8).
On 11 March 2020, the World Health Organization (WHO) classified coronavirus disease 2019 (COVID-19) as a pandemic. Given that the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can be transmitted via close contact and respiratory droplets, the Melbourne Sexual Health Centre (MSHC) changed its guidelines for STI screening on 16 March 2020, so that all oropharyngeal swabs were to be collected by patients themselves rather than by clinicians, in order to minimize the risk of health care worker exposure to SARS-CoV-2. This study aimed to evaluate the change from clinician-collected to self-collected oropharyngeal swabs among men who have sex with men (MSM) attending the MSHC by examining the performance of these swabs in the detection of oropharyngeal Neisseria gonorrhoeae and Chlamydia trachomatis infections.
MATERIALS AND METHODS
The MSHC is the largest sexual health clinic in Victoria, Australia, and provides free HIV/STI testing and management to patients. The present study was a retrospective data analysis of MSM attending the MSHC between 20 January and 8 May 2020. All MSM attending the MSHC are offered screening across three anatomical sites (i.e., the urethra, oropharynx, and anorectum) for N. gonorrhoeae and C. trachomatis. We restricted the analyses to MSM because oropharyngeal STI screening is not routinely performed for heterosexuals. Before 16 March 2020, first-void urine specimens were provided by the patients, oropharyngeal swabs were collected by clinicians, and anorectal swabs were collected either by the clinicians or by the patients, depending on preference and clinical indication for testing. However, the MSHC revised its guidelines and policy, changing from clinician-collected to self-collected oropharyngeal swabs for N. gonorrhoeae and C. trachomatis screening on 16 March 2020, in order to minimize the risk of exposure to SARS-CoV-2 among health care workers. Clinicians provided verbal instructions on how to collect an oropharyngeal swab to patients, and a laminated color poster was placed next to the mirror in each bathroom (see Fig. S1 in the supplemental material). Urine and anorectal swab specimen collection remained unchanged. All specimens were tested by a nucleic acid amplification test using the transcription-mediated amplification (TMA)-based Aptima Combo 2 assay (Hologic Panther system; Hologic, San Diego, CA, USA). All results (valid, invalid, or equivocal) were interpreted according to the manufacturer’s instructions.
All men aged ≥16 years who had ever had sex with another man were included in this analysis. The demographic characteristics, sexual practices, and lab results for N. gonorrhoeae and C. trachomatis screening of MSM attending the MSHC between 20 January and 8 May 2020 were extracted. The study period provided 8 weeks of data in the clinician collection period, between 20 January and 15 March 2020, and 8 weeks of data in the self-collection period, between 16 March and 8 May 2020. The short study period was chosen to minimize any seasonal variations in STI diagnoses (9, 10).
The positivity rate for oropharyngeal N. gonorrhoeae or C. trachomatis detection was defined as the number of specimens that tested positive divided by the number of specimens that tested with a valid result. A chi-square test was used to compare the positivity rates for oropharyngeal N. gonorrhoeae and C. trachomatis detection and patient characteristics in the clinician collection period with those in the self-collection period. The number and proportion of specimens with equivocal or invalid results were calculated and compared between the two periods. We used binomial log-linear regression models to calculate the prevalence ratios (PR) for oropharyngeal N. gonorrhoeae and C. trachomatis, and we adjusted for any characteristics that differed between the two periods with a P value of <0.10. All analyses were performed using Stata (version 14; StataCorp, College Station, TX, USA). Ethics approval was obtained from the Alfred Hospital Ethics Committee, Melbourne, Australia (project 246/20).
RESULTS
There were 6,647 consultations for MSM during the study period (3,955 in the clinician collection and 2,692 in the self-collection period). We excluded 2,550 (38.4%) consultations where oropharyngeal swabs were not taken; in the majority of these consultations, MSM were coming back for STI treatment or a review (n = 1,371 [53.8%]). The remaining 4,097 MSM (2,600 in the clinician collection period and 1,497 in the self-collection period) had oropharyngeal swabs taken for N. gonorrhoeae and C. trachomatis screening and were included in the analysis.
Table 1 shows that there were no significant differences in demographic characteristics (i.e., age, country of birth), reasons for presentation (i.e., known contacts with gonorrhea or chlamydia, presentation with symptoms), HIV status, or the number of male partners in the past 3 months between the clinician collection and self-collection periods. However, there were slightly more HIV-negative MSM taking pre-exposure prophylaxis (PrEP) in the self-collection period than in the clinician collection period (43.6% versus 35.8% [P < 0.001]). Furthermore, the proportion of MSM who had anal sex without a condom in the past 3 months was higher in the self-collection period than in the clinician collection period (82.0% [739/901] versus 76.4% [1,253/1,639] [P = 0.001]).
Comparison of patient characteristics and the positivity rates of N. gonorrhoeae and C. trachomatis between the clinician collection and self-collection periods for men who have sex with men
There were 47 (1.1%) oropharyngeal swabs with equivocal results for N. gonorrhoeae, and the proportion of swabs with equivocal results was higher in the self-collection period than in the clinician collection period (1.6% [24/1,497] versus 0.9% [23/2,600]) (P = 0.038). Of the remaining 4,050 oropharyngeal swabs with valid results, the overall positivity rate for N. gonorrhoeae was 7.2% (291/4,050), and the positivity rate did not differ between the two periods (7.6% [112/1,473] in self-collected versus 6.9% [179/2,577] in clinician-collected swabs) (P = 0.436), with a crude PR of 1.09 (95% confidence interval [CI], 0.87 to 1.37; P = 0.435). Additionally, there was no significant difference in the positivity rate of oropharyngeal N. gonorrhoeae swabs between the two periods after adjustment for PrEP use and condom use (adjusted PR, 1.07 [95% CI, 0.85 to 1.34]; P = 0.583).
Similarly, there were 4 (0.1%) oropharyngeal swabs with equivocal results for C. trachomatis, and the proportion did not differ between the two periods (P = 0.576). The overall positivity rate of oropharyngeal C. trachomatis swabs was 1.7% (69/4,093), and the positivity rate did not differ between the two periods (1.5% [23/1,495] in self-collected versus 1.8% [46/2,598] in clinician-collected swabs [P = 0.579]), with a crude PR of 0.87 (95% CI, 0.53 to 1.43; P = 0.579). Additionally, there was no significant difference in the positivity rate of oropharyngeal chlamydia swabs between the two periods after adjustment for age and PrEP use (adjusted PR, 0.84 [95% CI, 0.51 to 1.39]; P = 0.504).
There was one equivocal result each among urine specimens for N. gonorrhoeae and C. trachomatis. The positivity rates of urethral N. gonorrhoeae and C. trachomatis swabs did not change between the two periods (Table 1). A small number of anorectal swabs had equivocal or invalid results for N. gonorrhoeae (n = 34 [0.9%]) and for C. trachomatis (n = 34 [0.9%]); however, for both N. gonorrhoeae and C. trachomatis, the positivity rates of anorectal swabs did not change between the two periods (Table 1).
DISCUSSION
To minimize the risk of exposure to SARS-CoV-2 among clinicians, our clinic changed from clinician-collected to self-collected swabs for oropharyngeal gonorrhea and chlamydia screening in mid-March 2020. We found no difference in performance between self-collected and clinician-collected oropharyngeal swabs for C. trachomatis, and we found a small, significant increase in equivocal results for N. gonorrhoeae with self-collected oropharyngeal swabs. Importantly, when we compared the positivity rates of oropharyngeal gonorrhea and chlamydia swabs between the clinician collection and self-collection periods, we found no significant difference. Similarly, when we used the number of sexual partners, condom use, and the positivity rates of N. gonorrhoeae and C. trachomatis at other anatomical sites as proxies for sexual risk, the risk profiles of men in the two periods were relatively similar. Our study findings suggest that self-collected oropharyngeal swabs are a valid and safe method for N. gonorrhoeae and C. trachomatis screening of MSM in sexual health clinic settings.
Our study showed a higher proportion of oropharyngeal swabs with equivocal results in the self-collection period than in the clinician collection period for N. gonorrhoeae but not for C. trachomatis. This may suggest that a small proportion of men might have collected their oropharyngeal swabs less rigorously or thoroughly than most. Further, it is possible that equivocal test results are due to technical issues, including insufficient sample volume and pipetting error. We were unable to compare these proportions to those of other studies, since these numbers and proportions were not commonly reported previously when self-collected swabs were compared with clinician-collected swabs (4). Some individuals may experience difficulties in collecting oropharyngeal swabs; for instance, they may find it difficult to avoid touching the tongue, or they may be reluctant to swab the back of the oropharynx during a gag reflex (11). However, several studies have reported that self-collected oropharyngeal swabs for STI screening are highly acceptable (11–14).
Evaluations comparing the performance of self-collected swabs with that of clinician-collected swabs have been conducted for some pathogens, such as group A streptococcus (15), but there have been limited studies on oropharyngeal screening for N. gonorrhoeae and C. trachomatis. A systematic review published in 2015 has identified one study examining the sensitivity and specificity of self-collected versus clinician-collected swabs for oropharyngeal N. gonorrhoeae and C. trachomatis (4). The study, conducted among 480 MSM in the United States in a sexual health clinic setting, reported that sensitivity (91% for N. gonorrhoeae and 83% for C. trachomatis) and specificity (97% for N. gonorrhoeae and 100% for C. trachomatis) were comparable for self-collected and clinician-collected oropharyngeal swabs and were highly acceptable (12). Self-collected oropharyngeal swabs have become more common during the COVID-19 pandemic than previously, since they are used for testing for SARS-CoV-2 (16). Our results showed that the positivity rate of oropharyngeal STIs did not differ between the clinician collection and self-collection periods, suggesting that self-collected oropharyngeal swabs could also be an routine alternative option for patients in the future. It is important to provide detailed step-by-step illustrations together with verbal instructions to the patients in order to ensure that they take the swabs confidently and correctly (4).
There are several limitations to this study. First, this study was conducted at a single sexual health clinic, and the results may not be generalizable to other MSM in the community or to other populations, such as females and heterosexuals. Heterosexual females and males are not routinely screened for oropharyngeal STIs, with the exception of sex worker populations (17), and therefore, further studies may be required to understand acceptability and performance characteristics in these populations. Second, this was a before-and-after study, and we were unable to determine the sensitivity and specificity of self-collected swabs versus clinician-collected swabs. Third, this evaluation was conducted during the COVID-19 pandemic, when the level of sexual risk might have changed due to social distancing and nationwide lockdown (18). There were 1,100 fewer oropharyngeal swabs included in the self-collection period than in the clinician collection period, and this might be due to the reduction in the number of clients attending the clinic during the lockdown. However, we used a series of indications (e.g., the number of partners, the positivity rate for N. gonorrhoeae and C. trachomatis at other anatomical sites) to determine sexual risk, and we found no differences between the two periods. Fourth, we were unable to investigate the reasons for invalid samples, because the primary samples were not available for further testing at the time of this evaluation. Further studies, which would include a human housekeeping gene (e.g., beta-globin) as a marker of sample adequacy, would be useful for determining whether the invalid results are due to inadequate sampling from individuals or to technical errors. Fifth, we collected data only on anal sex practices as part of routine care and management. Past studies have shown that non-anal sex practices such as kissing, oral sex, and rimming are associated with oropharyngeal STIs (19–21). We were unable to determine whether there were any changes in these sexual practices between the two periods. Sixth, we did not standardize the verbal instructions, and thus, they might have differed across clinicians. However, all patients were advised to refer to the laminated color poster placed in the bathroom.
After the change from clinician-collected to self-collected oropharyngeal swabs, there were no changes in the positivity rates of oropharyngeal gonorrhea and chlamydia among MSM. Self-collected oropharyngeal swabs for STI screening among MSM may be an alternative option for patients in the future. However, review and evaluation of the instruction sheet and the procedures are required in order to ensure that patients understand the step-by-step self-collection. Further studies are required if self-collection of oropharyngeal swabs is to be used for other at-risk populations, such as sex workers.
ACKNOWLEDGMENTS
We thank Afrizal Afrizal at the Melbourne Sexual Health Centre for assistance with data extraction and Mark Chung for assistance in designing the illustrated instruction sheet for patients in the survey at the Melbourne Sexual Health Centre.
E.P.F.C. and D.A.W. are supported by Australian National Health and Medical Research Council (NHMRC) Emerging Leadership Investigator grants (GNT1172873 and GNT1174555, respectively). C.K.F. and C.S.B. are supported by Australian NHMRC Leadership Investigator grants (GNT1172900 and GNT1173361).
We have no conflicts of interest to declare.
E.P.F.C. and C.K.F. designed the study. E.P.F.C. performed data analysis and wrote the first draft of the manuscript. D.A.W. contributed to the interpretation of laboratory results. C.S.B. changed the clinic’s policy and guidelines in responding to the COVID-19 pandemic. E.P.F.C., C.S.B., D.A.W., S.H., M.Y.C., T.R.P., R.F., K.M., and C.K.F. were involved in data interpretation, revised the manuscript critically for important intellectual content, and approved the final version of the manuscript.
FOOTNOTES
- Received 21 May 2020.
- Returned for modification 14 June 2020.
- Accepted 23 June 2020.
- Accepted manuscript posted online 1 July 2020.
Supplemental material is available online only.
- Copyright © 2020 American Society for Microbiology.
