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Proctitis in gay and bisexual men. Are microscopy and proctoscopy worthwhile?
  1. Gwamaka Eliudi Mwasakifwa1,2,
  2. Colleen Nugent2,
  3. Rick Varma1,2
  1. 1The Kirby Institute, University of New South Wales, Sydney, NSW, Australia
  2. 2Sydney Sexual Health Centre, Sydney, NSW, Australia
  1. Correspondence to Dr Gwamaka Eliudi Mwasakifwa, The Kirby Institute, High Street, UNSW Australia, Kensington NSW 2052, Australia; gmwasakifwa{at}kirby.unsw.edu.au

Abstract

Objectives We explored the association between nucleic acid amplification testing (NAAT) and rectal microscopy/proctoscopy findings and correlates of rectal STIs among 150 gay and bisexual men (GBM) diagnosed with proctitis at the Sydney Sexual Health Centre from March 2016 to October 2017.

Methods From case files, we analysed risk behaviours, microscopy, proctoscopy and NAAT results for rectal STIs (Chlamydia trachomatis, Neisseria gonorrhoeae, Mycoplasma genitalium, herpes simplex virus type 1/2, lymphogranuloma venereum and syphilis). χ2 test assessed the association between microscopy/proctoscopy findings and NAAT results. Linear regression assessed the association between NAAT positivity and correlates of rectal STIs.

Results The mean age was 32.5 (9.8) years, 43% (65/150) were taking pre-exposure prophylaxis, 17% (26/150) were HIV positive and 24% (36/147) had multiple rectal STIs.

Among GBM with documented proctoscopy findings (n=113), 58% (65/113) had discharge, 36% (41/113) had anorectal erythema and 25% (28/113) had bleeding. A quarter of GBM (28/113) had negative proctoscopy findings.

Discharge found on proctoscopy (p=0.001), positive HIV status (p=0.030) and time since last receptive anal intercourse (p=0.028) were independently associated with NAAT positivity for any rectal STI. Discharge had a positive likelihood ratio of 1.6 (95% CI 1.0 to 2.4).

Among those with documented microscopy findings (n=69), 59% (41/69) and 41% (28/69) were NAAT positive and negative, respectively. Among NAAT-positive GBM, 27 (66%) had polymorphonuclear cells (PMNs) (mean number of PMNs, 10 (SD 9) cells per oil immersion field), 1 (2%) had Gram-negative intracellular diplococci and 11 (27%) had negative findings. There was no significant association between microscopy findings and NAAT results (p=0.651) or the number of rectal STI (p=0.279).

Conclusion Microscopy does not reliably provide information necessary to tailor the management of GBM diagnosed with proctitis. Discharge found during proctoscopy may identify GBM with rectal STI. Services should consider recommendations to perform these investigations.

  • anogenital conditions
  • microbiology
  • gay men
  • PCR
  • Neisseria gonorrhoeae

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Introduction

Proctitis is an important inflammatory syndrome of the anorectal mucosa. Among gay and bisexual men (GBM), STIs are the leading cause of infectious proctitis, increasing the risk of HIV acquisition. 12 Inflammation from the anal verge to the pectinate line, which is lined by stratified cuboidal epithelium with an abundant supply of sensory nerve endings, results in anorectal pain, tenesmus, mucopurulent exudates, haematochezia and occasionally with lymphadenopathy and fever.3 The region above the pectinate line is lined by columnar epithelium, and STI involvement in this region is typically painless.

Among the STIs, Neisseria gonorrhoeae (NG) is the most common bacterium in proctitis with a positivity approximately 25%, followed by non-lymphogranuloma venereum (LGV) Chlamydia trachomatis (CT),4Mycoplasma genitalium (MG) at 12%, while herpes simplex virus (HSV) type 1 and HSV type 2 have been reported as 6.2% and 15.1%, respectively.5

Proctitis is frequently polymicrobial, and nucleic acid amplification testing (NAAT) positivity for any rectal STIs has ranged from 55% to 82%.4

Increasing rates of condomless anal sex and bacterial rectal STIs among GBM in the era of pre-exposure prophylaxis (PrEP)6 suggest that proctitis is going to contribute significantly to clinical workload.

Clinical presentation of proctitis correlates poorly with specific pathogens.7 Rectal microscopy and proctoscopy are recommended for the assessment of proctitis. However, the evidence supporting these recommendations is grounded in historically small studies, predating the NAAT era. Additionally, sensitivity of microscopy relative to rectal NAAT NG positivity is largely unknown.

Despite poor sensitivity, in earlier studies, rectal microscopy was shown to increase the proportion of GBM with culture-positive rectal NG treated on the same day.8

In this study, we sought to explore the association between rectal microscopy, proctoscopy and NAAT results and identify predictors of rectal NAAT positivity among GBM diagnosed with proctitis at the Sydney Sexual Health Centre (SSHC).

Methods

SSHC is an urban publicly funded HIV and STI service. The diagnosis of proctitis is based on the in-house clinical guideline for proctitis diagnosis and management. Microscopy and proctoscopy were performed according to in-house procedures by experienced sexual health physicians and sexual health registrars accredited for microscopy. All patients receive empirical treatment for NG and CT prior to NAAT results. LGV typing is requested by clinicians on all CT-NAAT-positive rectal samples, while MG and HSV NAAT are based on the severity of the presentation.

We reviewed files for all patients diagnosed with proctitis from 1 March 2016 (when HIV PrEP became available) until 31 October 2017.

NAAT positivity was defined as a positive NAAT for either one or multiple rectal STIs (CT, NG, MG, HSV1//HSV2, LGV and syphilis). For microscopy and proctoscopy, the analysis was limited to those with documented and interpretable findings.

Continuous variables were summarised as mean and SD. Student’s t-test compared continuous variables, and Pearson’s χ2 test compared categorical variables. McNemar test compared proctoscopy findings (dichotomised into presence or absence) and NAAT positivity (positive vs negative). Linear regression analysed the association between predictors and NAAT positivity. Covariates assessed for the association with NAAT positivity are described in the online supplementary appendix 1. The multivariable model was built by using backward stepwise regression. Predictors with a p value <0.1 in univariate analysis were assessed for inclusion in the multivariable model. All tests were two sided and considered significant at p<0.05. Statistical analysis was performed using STATA V.14.2, StataCorp, Texas.

Results

Patient characteristics are shown in the online supplementary table 1. Two transgender women and 150 GBM were diagnosed with proctitis. Mean (SD) age was 32.5 (9.8) years, 43% (65/150) were currently taking PrEP and 26/150 were HIV seropositive. Over half of GBM reported rectal pain, 13% had tenesmus and 64% had rectal discharge on presentation.

The proportion of NAAT testing for individual rectal STIs is provided in the online supplementary table 1. About 65.8% (98/149) had NAAT positive versus negative in 34.2% (51/149). Among those with NAAT positive, 76.5% (73/98) and 25.5% (25/98) had single and multiple rectal pathogens, respectively. The distribution of rectal pathogens is shown in the online supplementary figure 2.

Among GBM with documented proctoscopy findings (n=113), mucopurulent discharge was observed in 58% (65/113) of patients, anorectal erythema in 36% (41/113); and bleeding in 25% (28/113). A quarter of patients (28/113) had negative proctoscopy findings. We recorded a significant association between NAAT findings and the presence or absence of mucopurulent discharge, p=0.02. No significant association was recorded between NAAT findings and presence or absence of erythema (p=0.69) or bleeding (p=0.67). The discharge observed during proctoscopy had a positive likelihood ratio of 1.6, 95% CI 1.0 to 2.4, for any rectal STI (online supplementary table 2).

Among GBM with interpretable microscopic findings (n=69), 59% (41/69) and 41% (28/69) were NAAT positive and negative, respectively. Among NAAT-positive GBM, 27 (66%) had PMNs (mean number of PMNs, 10 (SD 9) cells per oil immersion field), 1 (2%) had gram-negative intracellular diplococci (GNID) and 11 (27%) had negative findings. For NAAT-negative GBM, 79% had PMNs (mean (SD), 8±5.1). No significant association was observed between rectal microscopy findings and NAAT results for any rectal STIs (p=0.651) or the number of rectal pathogens (p=0.279).

Figure 1 shows the results of the univariable and multivariable analysis of the predictors of NAAT positivity for any rectal STI. In multivariable analysis, presence of mucopurulent discharge observed on proctoscopy (adjusted OR 6.1, 95% CI 2 to 18.7; p=0.001), positive HIV serostatus (OR 5.4, 95% CI 1.2 to 25.1; p=0.03) and time since the last receptive anal intercourse (OR 1.0, 95% CI 1.1 to 1.2; p=0.028) were independently associated with NAAT positivity for any rectal STI.

Figure 1

Univariable and multivariable analysis of the predictors of the rectal nucleic acid amplification testing (NAAT) positivity for any STI (Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT), Mycoplasma genitalium (MG), lymphogranuloma venereum (LGV), herpes simplex virus 1 and 2 (HSV1/2) and syphilis) among gay and bisexual men diagnosed with proctitis at the Sydney Sexual Health Centre (SSHC). PrEP, pre-exposure prophylaxis; RAI, Receptive anal intercourse. Note: * indicate reference category; ** indicate significant result.

Discussion

In this group of GBM diagnosed with proctitis, the presence of PMNs or GNID viewed on microscopy was not associated with any rectal STIs. Additionally, multiple STIs were found in a quarter of GBM. Discharge observed during proctoscopy was significantly associated with NAAT positivity for any rectal STIs.

Traditionally, proctoscopy has enabled clinicians to examine the rectal mucosa and collect samples without contamination. In an analysis of GBM with anorectal LGV in Amsterdam, Van der Bij et al showed that proctoscopy findings independently predicted rectal LGV infection.9 In our study, two-thirds of GBM with NAAT confirmed rectal LGV had proctoscopic evidence of discharge. Taken together, these findings underscore the significance of discharge observed during proctoscopy in identifying GBM at a high risk of rectal pathogens. Well-designed prospective studies are needed to corroborate and validate these findings in other settings.

Consistent with previous studies,3 4 NG was the most common aetiological cause of proctitis among GBM in our study. However, among GBM with NAAT-confirmed rectal NG, no GNID was observed on microscopy, and the number of PMNs was comparable between GBM, who had positive versus negative rectal NAAT for any STIs.

Our study implies that among GBM diagnosed with proctitis, microscopy does not sufficiently support clinicians to tailor antibiotic use to the most common rectal STI or identify those with multiple STIs. Although the time taken for performing microscopy was not documented in our study, in other centres, the average time required for processing microscopy was between 10 and 15 min.10

Although rectal STIs cause proctitis, clinicians need to consider proctitis with negative rectal pathogens among men who have sex with men clinically diagnosed with proctitis.4 In our study, 34% of all GBM clinically diagnosed with proctitis had no rectal pathogens on NAAT, which may also reflect a testing bias within our patients or incorrect diagnosis by the clinician.

Our findings support polymicrobial therapeutic coverage among GBM diagnosed with proctitis, however, the observed limitation of microscopy, which fails to identify NG or suggest CT, MG or HSV, questions the rationale for performing this investigation. On the other hand, proctoscopy, when performed, does have value in predicting rectal STI in these patients when discharge was observed.

Our study has several limitations. There were a significant number of cases where microscopy and proctoscopy data were not documented or performed, limiting the capacity to reach robust findings. In some cases, proctoscopy was contraindicated due to pain or declined. Culture for enteric pathogens was not a standard test, limiting our diagnostic assessment for proctocolitis. MG and HSV NAAT were not requested in all patients, which may have underestimated the number of clients with ‘NAAT negative’ results. Caution should be exercised when extrapolating our findings to the management of proctitis in other settings with different protocols for STI testing.

Conclusion

To our knowledge, this is the first study to provide contemporary data on the utility of microscopy and proctoscopy in the management of proctitis among high-risk GBM in an urban sexual health service. Microscopy did not reliably provide information necessary to tailor the antimicrobial management of GBM in whom the clinician had diagnosed proctitis. However, discharge observed during proctoscopic examination, positive HIV serostatus and time since last receptive anal intercourse (RAI) predicted the presence of a rectal STI. Services should consider recommendations to perform these investigations in patients diagnosed with proctitis.

Acknowledgments

We acknowledge Melissa Arnott and Heng Lu for their contribution in data collection. We thank Tristian O’Dowd and Tracy Purvis, for their logistical and administrative support. We thank all the staff and patients at the Sydney Sexual Health Centre for their support.

References

Footnotes

  • Handling editor Tristan J Barber

  • Twitter @SydneySHC, @@RickVarma

  • Contributors GEM and RV designed the study concept. GEM and CN oversaw the study conduct and data collection. GEM designed the analysis plan, conducted the data analysis and drafted the manuscript. GEM, CN and RV reviewed the analysis plan, reviewed the article and approved the final manuscript.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • Competing interests None declared.

  • Patient consent for publication Not required.

  • Ethics approval Data are available upon request.

  • Provenance and peer review Not commissioned; externally peer reviewed.