2014 STI Testing Guidelines for MSM
2014 STI Testing Guidelines for MSM
David J. Templeton A,B,C,H, Phillip Read B,D, Rajesh Varma E and Christopher BourneF,G
A
RPA Sexual Health, Royal Prince Alfred Hospital, Camperdown, NSW 2050, Australia.
B
The Kirby Institute for Infection and Immunity in Society, The University of New South Wales, Kensington,
NSW 2052, Australia.
C
Central Clinical School, The University of Sydney, Sydney, NSW 2006, Australia.
D
Kirketon Road Centre, PO Box 22, Kings Cross, Sydney, NSW 1340, Australia.
E
Western Sydney Sexual Health Centre, Jeffery House, Level 1, 162 Marsden Street, Parramatta,
NSW 2150, Australia.
F
Sydney Sexual Health Centre, Sydney Hospital, PO Box 1614 Sydney, NSW 2001, Australia.
G
School of Public Health and Community Medicine, The University of New South Wales, Kensington,
NSW 2052, Australia.
H
Corresponding author. Email: dtempleton@[Link]
Abstract. Men who have sex with men (MSM) in Australia and overseas are disproportionately affected by sexually
transmissible infections (STIs), including HIV. Many STIs are asymptomatic, so regular testing and management of
asymptomatic MSM remains an important component of effective control. We reviewed articles from January 2009–May
2013 to inform the 2014 update of the 2010 Australian testing guidelines for asymptomatic MSM. Key changes include: a
recommendation for pharyngeal chlamydia (Chlamydia trachomatis) testing, use of nucleic acid amplification tests alone
for gonorrhoea (Neisseria gonorrhoeae) testing (without gonococcal culture), more frequent (up to four times a year)
gonorrhoea and chlamydia testing in sexually active HIV-positive MSM, time required since last void for chlamydia
first-void urine collection specified at 20 min, urethral meatal swab as an alternative to first-void urine for urethral
chlamydia testing, and the use of electronic reminders to increase STI and HIV retesting rates among MSM.
Additional keywords: chlamydia, first-void urine, gonorrhoea, nucleic acid amplification test, reminders, swabs.
Received 3 January 2014, accepted 9 February 2014, published online 2 April 2014
Table 1. Australian sexually transmitted infection (STI) and HIV testing guidelines for asymptomatic men who have sex with men (MSM), 2014
EIA, enzyme immunoassay; FVU, first-void urine (initial part of the urine stream, not the first urine of the day and not mid-stream urine; specimen collected at
least 20 min after last passing urine); HAV, hepatitis A virus; HBV, hepatitis B virus; HCV, hepatitis C virus; IgG, immunoglobulin G; NAAT, nucleic acid
amplification test
* HIV-positiveA,B
outlined below. For STIs not previously considered in the Chlamydia and gonorrhoea
guidelines (Mycoplasma genitalium and Trichomonas Chlamydia and gonorrhoea are among the most common STIs
vaginalis), all available articles, irrespective of publication affecting Australian MSM.10,11 Testing at nongenital as well
date, were considered. All potentially relevant abstracts were as urethral sites is an important component of chlamydia and
reviewed and the reference lists of reviewed full-text articles gonorrhoea control.10–14 However, such ‘comprehensive’ STI
checked. For each STI, the number of articles retrieved, testing is occurring in less than half of Australian MSM.15
abstracts reviewed and full-text articles reviewed were as Recommendations for chlamydia and gonorrhoea testing
follows: gonorrhoea (Neisseria gonorrhoeae) and chlamydia among MSM in the 2010 STIGMA guidelines were largely
(Chlamydia trachomatis): 758, 216, 84; lymphogranuloma based on the community-based Health in Men (HIM) cohort,
venereum (LGV): 168, 74, 32; M. genitalium: 17, 12, 9; which identified a variety of receptive nonpenile intercourse
T. vaginalis:19, 7, 5; hepatitis A virus (HAV): 17, 17, 4; practices that were risk factors for anal chlamydia and
hepatitis B virus (HBV): 57, 57, 17; hepatitis C virus: 236, gonorrhoea infections, including fingering, fisting, toys and
22, 22; syphilis: 288, 43, 28; HIV: 534, 86, 16; HIV coinfected: rimming.10 In contrast to syphilis and HIV infection, there
454, 76, 15; herpes simplex virus (HSV): 55, 29, 19; human have been no published mathematical models assessing the
papillomavirus (HPV): 142, 45, 26. References from the 2010 likely impact of more frequent chlamydia and gonorrhoea
guidelines, relevant national surveillance and public health testing in Australian MSM.
reports, and international STI or HIV testing guidelines for For pharyngeal infections, there was no association of either
MSM were also accessed. chlamydia or gonorrhoea with sore throat symptoms in the HIM
Questions addressed by the review panel were: cohort,11,16 while all pharyngeal chlamydia or gonorrhoea
identified in a recent Dutch clinic-based study was
*
Should we be testing asymptomatic MSM for each specific asymptomatic.17 Most pharyngeal chlamydia or gonorrhoea
STI? infections are isolated to the pharynx11,16–18 and there is
*
If so, should we be testing all MSM or a particular subgroup strong epidemiological evidence that supports transmission of
of MSM? chlamydia and gonorrhoea between pharyngeal and anogenital
*
Which anatomical sites should be tested (if relevant)? sites among MSM. The HIM study found an independent
*
Overall frequency of testing and indications for more frequent association of both urethral and anal chlamydia with
testing receptive oral sexual practices among MSM, while the
*
What tests or technology should be used for diagnostic univariate association of anogenital gonorrhoea with oral sex
testing? was no longer significant after adjustment for demographic and
*
Should testing recommendations differ depending on HIV behavioural risk factors.10 Likewise, independent associations
status? were identified in the HIM study between pharyngeal chlamydia
MSM testing guidelines 2014: literature review Sexual Health 219
and receptive penile–oral sex,16 and between pharyngeal perform equally well as clinician-collected swabs and are
gonorrhoea and insertive rimming.11 Overseas, the prevalence acceptable to MSM.14,33–37 In addition, self-collected samples
of both urethral chlamydia and gonorrhoea infections was found remove the need for routine examination among asymptomatic
to be over 4% among MSM whose only recent exposure was HIV-negative MSM,38 with self-collected penile meatal swabs
receptive penile–oral sex, and this was similar to urethral also performing well if adequate sampling of the urethral meatus
chlamydia and gonorrhoea prevalence among MSM who occurs.39,40 If first-void urine (FVU) is to be used, studies from
reported recent unprotected insertive anal intercourse.19 For Australia41 and overseas42 have suggested the sensitivity for
pharyngeal chlamydia, a high prevalence-to-incidence ratio16 chlamydia detection in the male urethra is similar if urine
suggests that chlamydia infection may be long-lasting in the specimens are collected 20 min after the last void, compared
pharynx, in contrast to gonorrhoea, where a high incidence-to- with 1 h after the last void.
prevalence ratio11 supports frequent spontaneous resolution.20,21 Anal chlamydia and gonorrhoea infections have been
More recently, a pharyngeal chlamydia prevalence of up to 2.3% identified as important risk factors for HIV acquisition
has been reported among MSM overseas14,18,22 and these studies among MSM in Australia43 and overseas.44–46 Irrespective of
have identified a higher prevalence of pharyngeal chlamydia antiretroviral therapy, urethral chlamydia or gonorrhoea can
among MSM than previously reported. Thus chlamydia as well increase seminal HIV viral load and thus infectiousness
as gonorrhoea testing is now recommended in the pharynx of among HIV-positive MSM.47 Therefore, regular STI testing
MSM. among HIV-positive MSM is likely to have public as well as
There is strong evidence in Australian MSM that nucleic acid individual health benefits.
amplification testing (NAAT) for gonorrhoea in those without Given that higher rates of gonorrhoea48 and chlamydia24,49
urethral symptoms yields very few positive results. In a large have been reported in Australia and overseas among HIV-
Sydney clinical cohort, the prevalence was only 0.04% among positive MSM compared with HIV-negative MSM, more
almost 4500 asymptomatic MSM,23 and prevalence (0.33%) and frequent chlamydia and gonorrhoea testing should be
incidence (0.26 per 100 person-years (PY)) were both low in the considered among sexually active HIV-positive MSM.
predominantly asymptomatic community-based HIM study.10
Thus, the previous recommendation not to test asymptomatic
MSM for urethral gonorrhoea remains. Lymphogranuloma venereum
Commercially available NAAT is substantially more sensitive Lymphogranuloma venereum (LGV) appears to have been
for anal and pharyngeal chlamydia and gonorrhoea detection endemic among MSM in the United States (US) since the
among MSM than culture.24–27 NAAT is now recommended early 1980s50 but, in the last decade, it has re-established
as the preferred method of chlamydia and gonorrhoea testing itself as an important STI affecting MSM worldwide.51 The
at all sites, provided that supplementary laboratory testing for majority of LGV identified among MSM has been anorectal and
nongenital gonorrhoea occurs28,29 and that gonococcal culture for symptomatic, and has predominantly affected highly sexually
antibiotic resistance surveillance is performed before treatment.29 active and sexually adventurous core groups of HIV-positive
Among MSM, gonococcal NAAT is particularly more sensitive MSM.52–54
than culture at extragenital sites and also among those with A recent systematic review and meta-analysis55 found a
asymptomatic infections.30–32 significant association of LGV with HIV infection in
Self-collected anorectal and pharyngeal swabs for chlamydia MSM. LGV has also been described in association with
and gonorrhoea detection using commercially available assays incident HCV infections among MSM.52 However, it remains
220 Sexual Health D. J. Templeton et al.
unclear if such associations are due to behavioural factors, M. genitalium prevalence (4–6%) has been reported among
biological factors or a combination of both. sexual health clinic attendees overseas.70,76 Urethral-to-anal
Previous investigations in North America56,57 and the United transmission has been reported in MSM,77 although no
Kingdom (UK)58 have failed to identify a substantial reservoir of significant association of M. genitalium with anorectal
asymptomatic LGV infection among MSM. This contrasts with symptoms or clinical proctitis has been described.68,70,76
other European data, where a large proportion of asymptomatic Multiple studies report an association between M. genitalium
anorectal chlamydia has been identified as LGV.59,60 Anorectal and HIV infection. M. genitalium prevalence appears to be
LGV has been identified among Australian MSM in both significantly higher at both anal and genital sites among HIV-
clinic61,62 and community-based63,64 settings. In common positive MSM compared with HIV-negative MSM in UK and
with most overseas reports, Australian cases predominantly US clinical settings.70,76 A 2009 systematic review and meta-
affect HIV-positive MSM, with symptoms of proctitis. analysis78 reported a statistically significant association of
LGV was rarely identified on systematic typing of positive M. genitalium and HIV in 12 of 19 included studies,
pharyngeal and anogenital chlamydia samples in Australian although only two included MSM. Most importantly, very
clinic- and community-based studies.61,63,65 Although LGV few included studies were of prospective design and the
has been identified in the pharynx of MSM overseas,60,66 a critical question of temporal relationship remains unanswered.
single Australian study failed to identify any cases.63 Longitudinal studies are required to address whether
Urethral LGV was recently identified in over 2% of MSM M. genitalium is a risk factor for HIV in MSM.
with anorectal LGV and almost 7% of their contacts at an Before advocating routine M. genitalium testing, further
Amsterdam clinic,67 with around half of these infections studies to understand the contribution of M. genitalium to
being asymptomatic. This report, from a relatively high-LGV anogenital disease and its impact on HIV acquisition among
prevalence setting contrasts sharply with other European58,60 MSM are required.
and Australian63 data, where no reservoir of urethral LGV has
been found among unselected MSM populations, irrespective Trichomonas vaginalis
of symptoms. There are few data on T. vaginalis among MSM and none have
LGV remains comparatively rare among MSM in Australia. reported its association with site-specific symptoms or clinical
Given the low prevalence of LGV, especially in asymptomatic syndromes. To date, no studies have been performed among
Australian MSM, routine LGV typing of chlamydia infections Australian MSM.
in asymptomatic MSM is not currently justified. A T. vaginalis prevalence of 1.1% was found on urine NAAT
testing of over 600 community-based MSM in El Salvador.79
However, over one-third of these MSM reported sex with a
Mycoplasma genitalium female partner in the past year.79 In contrast, a prospective
Anogenital M. genitalium appears to be uncommon in primary care-based US study involving over 350 HIV-positive
community-based Australian MSM. Prevalence at urethral MSM failed to identify any prevalent or incident genital
and anorectal sites was <1% and <2%, respectively, in a T. vaginalis infections.80 In a longitudinal US study
cross-sectional study of over 500 Melbourne attendees at sex- comparing STI and HIV incidence between 600 Black and
on-premises venues (SOPV).68 There were no demographic or White MSM, no baseline genital T. vaginalis infections were
behavioural correlates of infection and site-specific symptoms identified.81 These studies, importantly, suggest that the notable
were rare. The overall prevalence of anogenital M. genitalium racial disparities in T. vaginalis prevalence between Black and
was substantially lower than chlamydia or gonorrhoea, a pattern White heterosexual Americans are not present among MSM.
consistent with the prevalence of rectal infections among MSM In two US studies involving a total of 725 MSM clinic
clinic attendees in the US.69 This contrasts with findings from attendees reporting recent receptive anal sex, only three
a UK clinic-based study,70 where the overall prevalence of all NAAT-detected anal T. vaginalis infections were identified,
three infections was similar (5–8%), but among a subgroup of with a prevalence of 0.9%82 and 0.2%.76 Anal T. vaginalis
HIV-positive men, the prevalence of M. genitalium was prevalence among MSM was almost tenfold lower than among
substantially higher (21%) than that of either gonorrhoea women reporting anal sex82 and was substantially lower than the
(8%) or chlamydia (13%). prevalence of all other anal STIs in MSM.82
There is strong and consistent epidemiological and clinical Pharyngeal T. vaginalis has been identified among
evidence that M. genitalium can cause both acute and chronic predominantly asymptomatic STI clinic attendees in the US,
nongonococcal urethritis (NGU).69 Findings from clinic-based although most (>90%) infections were identified among
studies suggest that M. genitalium is detected significantly more heterosexual men.83
often in men with NGU than in asymptomatic patients.70–73 Taken together, these studies suggest that T. vaginalis
Nonetheless, M. genitalium-related NGU appears to be rarely colonises the pharynx or anogenital mucosa of MSM,
significantly less common among MSM compared with even in settings where the heterosexual community prevalence
heterosexual men.72,74 Evidence for a role of M. genitalium of T. vaginalis is substantial. Testing for T. vaginalis among
in ascending male genital infections is lacking75 and there is asymptomatic Australian MSM is therefore not recommended.
currently no evidence that M. genitalium colonises or infects the
pharynx of MSM.68 Hepatitis A virus
Although anorectal M. genitalium was identified in under Several sexually transmissible HAV outbreaks among MSM
2% of Australian SOPV attendees,68 a higher anorectal have been reported worldwide.84 These outbreaks are usually
MSM testing guidelines 2014: literature review Sexual Health 221
populations with varying HSV-2 prevalence.90,120 Some experts HIV risk factors identified in Australia and overseas may
have advocated HSV-2 serology testing among those at high risk indicate the need for more frequent testing in MSM and include:
of acquiring HIV.119 However, the benefits of HSV-2 receptive unprotected anal intercourse, higher numbers of
serological testing remain unclear. Further evaluation of male sexual partners, IDU and noninjecting drug use during
testing asymptomatic MSM in terms of reducing HSV sex (including the use of amphetamines with oral erectile
and HIV transmission, impact on sexual behaviour and dysfunction medications), engaging in group sex, other
psychological effects are required before any recommendations (especially anal) STIs, sex with HIV-positive partners and
can be made for Australian MSM. high viral load in those partners.133,143–145 However, although
identifying risk factors for HIV is important for targeted testing,
one in eight HIV diagnoses in Australia may be missed by
Human papillomavirus offering risk-based HIV testing only.146
The majority of adult MSM are infected with HPV often with Annual HIV testing is recommended for MSM by the US
multiple HPV types.121 HPV-related disease such as anogenital Centers for Disease Control,90 although only 60% of US MSM
warts and malignancies cause substantial morbidity and report being tested for HIV in the previous 12 months.147 British
mortality in these men,121–123 although the national guidelines also recommend yearly HIV testing for MSM and
introduction of a school-age male HPV vaccination program more frequent testing if there are symptoms suggestive of
last year can be expected to have a major impact on HPV-related seroconversion or ongoing high-risk exposures.148 In the US,
disease among future generations of Australian MSM.124 HIV testing of MSM every 3 months when combined with
The majority of research on HPV-related disease in MSM high engagement in care, immediate initiation of antiretroviral
has involved DNA detection of prevalent anal HPV infection. therapy and inexpensive self-testing has recently been shown
There are fewer prospective data on the frequency of acquisition to be cost-effective compared with annual testing.149 However,
and duration of anal HPV infection in MSM,125,126 and studies differences in US health care systems and the availability of
of penile and pharyngeal HPV infection in MSM are rare.123,127 HIV testing means these modelling data are unlikely to be
A small number of studies have assessed HPV seroprevalence in generalisable to Australian MSM populations.
MSM125 but this is unlikely to be a useful clinical diagnostic Australian researchers have assessed the impact and
tool due to the low sensitivity of HPV serology as a marker of acceptability of increased coverage and frequency of HIV
HPV infection.125 testing on the number of HIV infections averted in MSM.150
Estimated anal HPV prevalence in a recent large meta- Modelling indicated the single most effective scenario (increasing
analysis of 31 studies was 64% and 93% among HIV- the frequency of testing among the 70–80% of MSM who already
negative and HIV-positive MSM, respectively, whereas the test annually to four times per year) resulted in a relatively modest
prevalence of high-risk (oncogenic) anal HPV types was 37% 14% reduction in HIV incidence over 10 years, provided that
and 74%, respectively.128 Although the natural history of other factors such as sexual behaviour and antiretroviral treatment
anogenital HPV in MSM has not been clearly defined, MSM initiation at a CD4 count of 350 cells mL–1 remain unchanged. If
appear to be at risk of both frequent reinfection and persistent annual HIV testing coverage was increased to 100% of MSM,
infection, which, for high-risk anal HPV types, may explain the there would be a similar (11%) reduction in HIV infections over
substantially elevated risk of anal cancer in this population.121 10 years. Only one-third of Australian MSM in an online
Studies that include assessing the utility of anal HPV testing to survey150 reported being ‘very likely’ to increase their testing
predict the risk of anal precancerous lesions are ongoing and frequency from current levels, although men reporting recent
are expected to guide future recommendations.129 unprotected anal intercourse and who were thus at the highest
There are few data regarding the impact of HPV infection and risk of HIV, were more willing to increase HIV testing frequency.
HIV acquisition.130 In a recent meta-analysis of the association Current inflexible and inconvenient clinic-based testing was
of HIV acquisition with HPV infection at a variety of anogenital cited as a barrier to achieving this goal. The availability of
sites, a significant association was identified.131 Anal HPV clinic-, community- or home-based rapid HIV testing may
infection was independently associated with HIV acquisition address some of these concerns, although there are few
in the single included study that assessed anal infection among controlled studies on the impact of such strategies on the
MSM.132 coverage or frequency of HIV testing.151
Considerable uncertainty surrounds the natural history of HPV Given that a large proportion of Australian MSM are not
infection and clinical utility of testing among MSM at present. willing to test more frequently150 and that many do not even have
Thus regular testing for HPV in MSM is not recommended. annual HIV testing,142 testing for HIV at least once per year is
recommended for all MSM. This recommendation is largely
based on models suggesting little difference in the proportion
HIV of HIV infections averted between annual HIV testing among
Globally, HIV incidence, prevalence and the number of all MSM and current HIV testers being tested more often.150
undiagnosed infections among MSM remain high.133–138 In However, those at highest HIV risk, including those reporting
Australia, an estimated 12–33% of HIV among MSM unprotected anal intercourse, more partners, drug use during
remains undiagnosed.139,140 Despite around two-thirds of gay- sex or group sex (Table 1), should be targeted for more
community-attached MSM consistently reporting testing,141 frequent HIV testing. This subgroup of the men at highest risk
less than 40% of high-risk MSM return for HIV testing also appear to be the most willing to increase their frequency of
within 1 year of a previous test.142 HIV testing.150
MSM testing guidelines 2014: literature review Sexual Health 223
Syphilis Conclusion
The rate of new syphilis infections continue to rise among MSM Efforts to improve the rates of comprehensive STI and HIV
overseas,152–156 whereas rates have plateaued in Australia since testing for MSM should focus on STI education, promotion of
2010.4 Syphilis is frequently diagnosed concurrently with new regular testing and building the sexual health capacity of general
HIV infection.114 Globally, ~50% of infectious syphilis is practice.178,179 To improve access to STI and HIV testing for
diagnosed in HIV-positive MSM.157 Australian MSM, strategies such as rapid HIV testing,
Identified risk factors for syphilis in MSM with HIV are information technology and the use of social media180–182
fisting, rimming, the use of anal sex toys, unprotected oral sex, should be fully utilised. The testing guidelines outlined in
multiple sexual partners and group sex.158–160 Mathematical Table 1 aim to guide clinicians in their STI and HIV testing
modelling in Australia indicates testing high-risk MSM who practice for MSM and provide an additional clinical tool to
report more than 10 partners per year and/or group sex (or both) assist in reducing the community prevalence of STIs and HIV
every 3 months will substantially reduce the incidence and, among Australian MSM.
subsequently, the prevalence of syphilis; in fact, more so than
increasing the coverage of annual syphilis testing.160,161 MSM Conflicts of interest
at are high risk of reinfection following a syphilis diagnosis.162 None declared.
However, such men, as well as those having regular
asymptomatic syphilis testing, are being tested less frequently Acknowledgements
than recommended,142,163 which is likely to jeopardise syphilis
control efforts. We thank Dr Shi-Chi Kao for his assistance with the review process,
Dr Mary Poynten for her review of the HPV section, A/Prof Catriona
Bradshaw for her review of the M. genitalium section and A/Prof
STI testing among HIV-positive MSM
Rebecca Guy for her advice on the HIV section.
The prevalence and incidence of STIs in MSM with HIV infection
remains high in Australia164 and elsewhere in the References
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