Surveillance of STIs at the European Centre for Disease Prevention and Control

Four bacterial STIs are under surveillance within the European Union/European Economic Area (EU/EEA): chlamydia, gonorrhoea, syphilis (including congenital syphilis) and lymphogranuloma venereum (LGV). Every year, data are uploaded by EU/EEA countries to the European Surveillance System hosted by the European Centre for Disease Prevention and Control (ECDC), in accordance with case definitions for confirmed cases established by the EU2–4 and available in the ECDC Surveillance Atlas of Infectious Diseases.5 In 2019, the number of reported STIs increased by 9% for chlamydia, 55% for gonorrhoea, 25% for syphilis and 75% for LGV relative to 2015 (figure 1; box 1).

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Figure 1

Reported cases of bacterial STIs in EU/EEA in 2015 (solid colour) vs 2019 (patterned colour).5 EEA, European Economic Area; EU, European Union; LGV, lymphogranuloma venereum.

Did the COVID-19 pandemic have an impact on STI notifications?

While the EU/EEA STI surveillance data for 2020 are under validation, initial information on trends can be gathered from national reports, surveys and peer-reviewed publications, including a series of articles hosted by the STI journal9–16 (table 1). A reduction in the number of STI diagnoses coinciding with pandemic-related restrictions on social interactions was reported from many settings, although some reported stable or even increasing numbers. The EuroTEST consortium recently conducted an online survey assessing the impact of the pandemic on testing for HIV, viral hepatitis and STIs during March–August 2020 in the 53 countries of the WHO European region.17 Most respondents reported decreased testing volumes, and many described severe disruptions to testing provision, particularly in March–May 2020 versus the same period in 2019, followed by some improvement in June–August 2020. Current research aims to understand how the pandemic is impacting STI epidemiology and provision of sexual health services, and its effects on sexual behaviour and healthcare-seeking behaviour.18 Data are also needed on the opportunities offered by innovative healthcare approaches, such as provision of e-health services and implementation of self-sampling services for STI testing using postal services.

Bidirectional interactions between STIs and HIV

STIs that cause inflammation and ulceration may enhance the infectiousness of people living with HIV and increase susceptibility to infection in their partners by directly promoting HIV replication, disrupting the mucosal barrier and attracting activated lymphocytes to sites of exposure.19 20 However, data indicate that antiretroviral treatment (ART) and pre-exposure prophylaxis (PrEP) effectively prevent HIV transmission despite the presence of STIs. HIV continues to modulate the impact of STIs, most notably with human papilloma virus (HPV), which remains an important cause of disease for people living with HIV (box 2).21–24

HIV PrEP and STIs

Much attention has been focused on the concept that the availability of HIV PrEP may modify behaviours and increase STI incidence among PrEP users. Data have been somewhat discordant, probably reflecting that PrEP studies tend to be biased by (1) the recruitment of participants who have more frequent STI diagnoses overall, and (2) the probability of more frequent STI screening of participants of PrEP studies than of non-PrEP users. In 2018, a systemic review showed a 24% increase in STI prevalence among PrEP users versus non-users (OR 1.24; 95% CI 0.99 to 1.54).25 In a PrEP trial in Australia in 2016–2018, overall STI incidence was 92 per 100 person-years among 2892 MSM.26 In a subset (n=1378) with pre-enrolment data, starting PrEP was associated with a small increase in STI incidence (adjusted incidence rate ratio 1.12). It has been highlighted that 76% of all STIs in the trial occurred in a fraction (25%) of the overall population19; the factors associated with STI acquisition were those related to sexual behaviour and young age.26 One important dataset comes from the PROUD Study that randomised MSM in the UK to receive PrEP either immediately or after a deferral period of 1 year: in the deferred arm, a history of syphilis or rectal chlamydia or gonorrhoea was associated with a high risk of HIV infection,27 highlighting how STI epidemiological trends can point to the need for PrEP in a population.

An online survey in Ireland aimed to determine the level of knowledge of STI and HIV transmission, testing and treatment in the MSM population.28 As many as 36% of respondents were classed as having lower levels of knowledge. Predictors of lower levels of knowledge were younger age, lack of disclosure of MSM behaviour to contacts and not having visited a national MSM-specific health promotion website. Other interesting observations emerged from an online survey of PrEP users in the UK; among over 1800 MSM, 9% reported taking self-sourced antibiotic prophylaxis for STIs, most commonly doxycycline, usually due to perceiving themselves as being at risk of exposure.29 Whereas there is evidence of the beneficial effect of doxycycline for post-exposure prophylaxis against chlamydia and syphilis,30 current guidance firmly recommends against antibiotic use for STI PrEP.31

ART and PrEP prevent HIV transmission despite STIs

The efficacy of suppressive ART in preventing HIV transmission despite the occurrence of STIs has been confirmed in several studies which recruited heterosexual or homosexual HIV-serodifferent couples, including HPTN 052 (heterosexual couples),32 PARTNER 1 (heterosexual and MSM couples),33 PARTNER 2 (MSM couples)34 and Opposites Attract (MSM couples).35 In PARTNER 2, of 782 gay couples reporting more than 76 000 episodes of condomless anal sex, 27% of 779 partners with HIV and 24% of 779 partners without HIV had an STI over a median follow-up of 2 years.34 Despite this, no episodes of within-couple HIV transmission were detected. Possible reasons include: (1) STI-induced HIV shedding during suppressive ART occurs at low copy numbers, (2) the shed virus is defective or (3) ART has direct prophylactic effects in the anogenital tract.19 In a meta-analysis of surveillance data from HIV-negative MSM attending sexual health clinics throughout England in the period predating HIV PrEP roll-out (2011–2018), HIV incidence rates decreased while rates of rectal gonorrhoea markedly increased.36 Investigators concluded that the effect likely resulted from expanded HIV testing, prompt ART initiation after diagnosis and high rates of virological suppression in people living with HIV. PrEP with tenofovir disoproxil plus emtricitabine is also efficacious in preventing HIV acquisition, despite the frequent occurrence of STIs among PrEP users.19 37 38 In the open-label observational phase of the IPERGAY Study of on-demand PrEP for example, 43% of 361 MSM had ≥1 STI (chlamydia, gonorrhoea or syphilis), yet PrEP led to a 97% relative reduction in HIV incidence over a median follow-up of 18.4 months.37

From infection control towards disease control for chlamydia?

Starting from the 1970s, successive breakthroughs in diagnostics helped identify Chlamydia trachomatis as an STI. Subsequent work established that most infections are mild or asymptomatic, although in a small proportion of cases they can lead to pelvic inflammatory disease (PID) and infertility.39 The potential for significant disease and sequelae led some countries to implement extensive screening programmes as part of a ‘test and treat’ approach. Recently, the cost-effectiveness of asymptomatic screening for chlamydia has been called into question,40 reflecting several considerations: (1) PID-related hospital admissions have been declining both in countries with extensive screening programmes, such as the UK and the Netherlands, and in countries that have not adopted such programmes, such as Ireland and Belgium, causing uncertainty about the true population attributable fraction of PID that may be related to chlamydia41; (2) ‘test and treat’ does not seem to translate into reduced chlamydia transmission at the population level; (3) antibiotic treatment of asymptomatic infections may contribute to the spread of antimicrobial resistance; (4) among men, and especially among MSM, chlamydia infection of extragenital and probably genital sites causes low or even negligible morbidity; and (5) at the individual level, the potential benefits of asymptomatic testing need balancing against a potentially negative psychosocial impact, for example, on relationships (box 3).

How is LGV spreading among MSM?

C. trachomatis genovar L – the cause of LGV – is an invasive organism that can cross the mucosal layer and spread to loco-regional lymph nodes, causing severe inflammation. About 75% of infections are symptomatic, presenting with anal and rectal symptoms.42 43 Before 2000, LGV was seen in Europe mainly in heterosexual contacts of people from countries in the equator. Outbreaks affecting MSM in large urban centres followed, initially among people living with HIV but now increasingly among HIV-negative MSM.7 8 Using stored samples, the first evidence of transmission among MSM was traced to the early 1980s in San Francisco. Genome analyses show that the strains causing LGV among MSM in Europe (UK, Netherlands, Spain) are highly similar to those found in major cities in Australia and North America, pointing to a clonal origin of the epidemic.44

When to screen for Mycoplasma genitalium?

Mycoplasma genitalium is sexually transmitted and is associated with urethritis in men. An association with other urogenital manifestations, including cervicitis and PID in women, is proposed, but understanding of the natural history of the infection is incomplete.45 Most people are asymptomatic and widespread asymptomatic screening is not recommended.46 In addition, M. genitalium is highly prone to antimicrobial resistance, limiting therapeutic options for symptomatic infections and raising concerns about the emergence of untreatable strains. Diagnosis requires access to molecular assays and a characterisation of resistance. IUSTI is developing guidelines indicating that testing should be primarily directed to people with specific syndromes.46

How can anal cancer be prevented in MSM?

In a meta-analysis of data from 29 900 men, prevalence of anal HPV16 and other high-risk HPV types was highest in MSM living with HIV, lower in heterosexual men living with HIV and in HIV-negative MSM, and lowest in HIV-negative heterosexual men.22 HIV infection and HIV-related immunosuppression were also significant predictors of anal high-grade squamous intraepithelial lesions (HSILs). These data are consistent with a previous meta-analysis showing a strikingly increased risk of anal cancer among MSM, which was associated with HIV infection as well as older age.23 MSM living with HIV have nearly 100-fold higher risk of anal cancer relative to HIV-negative MSM, and the risk is increased with low nadir CD4 cell count, alcohol use and smoking, whereas virologically suppressive ART has a partially protective effect.24 Results were recently announced from the phase 3 ANCHOR Study, which randomised just over 4000 people living with HIV who had anal HSIL to either immediate treatment of the lesions or observation.47 The study was terminated early due to the observation that immediate treatment significantly reduced the incidence of anal cancer. The data indicate a role for screening (by high-resolution anoscopy) MSM living with HIV as a key strategy to prevent anal cancer.

A survey of standards of STI care indicates considerable variation and room for improvement

When managing STIs within HIV services, it is important that practitioners are familiar with practice guidelines. However, familiarity with practice guidelines is not sufficient for situations in which individuals are unable to access a service or appropriate diagnostic test. These matters pertain to service standards, which consider areas such as overall service quality, values, governance and rights (figure 2). Standards for STI services began to be defined in the UK by the mid-2000s, first in Scotland in 2008 followed by England in 2010 and have undergone revision in the intervening years.48 Our survey gathered the opinions of country representatives of IUSTI Europe and country leads from the ECEE network1 on standards of STI services for people living with HIV across the European region. Responses were collected via an email link to a survey form. Twenty-two representatives from 21 countries responded (figure 3). Participants were first asked to give a single overall score, between 1 (poor) and 5 (excellent), to represent their opinion of the quality of STI care in their country’s HIV services. The median score was 3 with a range of 1–5, suggesting considerable variation (Box 4). The reported concerns could be grouped into four main areas:

1. Strong professional demarcations along traditional specialty lines that were not always helpful to patient care. The specific expertise required to treat some STIs was not always accessed, although there were good examples of collaborative working in other areas.

2. Problems accessing modern testing technology both for symptomatic diagnostics and for asymptomatic screening.

3. Commissioning of HIV services was often carried out without co-commissioning STI treatment and prevention and reproductive health services, leading to complex referral pathways rather than integration within HIV services. A further reported problem was a separate focus on specific STIs or some blood-borne viruses, which were sometimes described as separately funded through third-sector or non-governmental agencies, leading to pathway fragmentation. Some countries reported comprehensive expert and high-quality STI care within HIV services, indicating this can be achieved.

4. Ongoing challenges of stigma and broader concerns around values and legal systems in some countries. Some respondents described barriers to the implementation of self-sampling, self-testing, postal submission of tests or sending of medication, preventing remote management. Other countries clearly exploited the capabilities of digital transformation to mitigate the impact of the COVID-19 pandemic.17 The recently published findings of the INTEGRATE work programme in the EU highlighted the legal challenges surrounding partner notification,49 with under 30% of jurisdictions responding having guidelines for partner notifications for a range of STIs including HIV.

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Figure 2

Examples of statements about standards for the management of STIs.48

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Figure 3

Survey on standards of STI care for people living with HIV. (A) Country representatives that responded to the survey (represented in dark)^a; (B) a driver diagram to improve STI care in HIV services developed from the survey. ^a The designations employed and the presentation of the map do not imply the expression of any opinion whatsoever on the part of the WHO Secretariat concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers and boundaries.

What does good look like?

The findings from the survey leave us with much to think about. Respondents felt that standards of STI care in HIV clinics in Europe should be developed along clear priorities, indicating two broad aims: recognising the need for an STI service and establishing the provision of the right STI service (figure 3), finding ways to integrate STI care into routine HIV care. Funders in some areas may need convincing that there is a problem requiring public health capacity, and need, at the bare minimum, awareness of the epidemiology and mechanisms to plan and commission services. There are opportunities to harness the impact of the third sector (non-governmental organisations, charities, etc), which has been so influential in campaigns for ART provision and more recently HIV PrEP. There may be significant legal and stigma barriers in some jurisdictions but there is also a good track record in HIV of success in overcoming these barriers. The second main aim is to focus on improving the quality of the services that are on offer. Professionals need to find ways to reduce the demarcation between them. Leadership and cooperation are needed to drive service transformation, embed modern diagnostics, and make sure that guidelines for STI care are adopted and the workforce is appropriately trained. From a patient perspective, a set of rights should apply to anyone living with HIV in Europe, including being able to talk about STI concerns with HIV care providers, getting access to accurate tests for STIs, having free screening for cervical and anal cancer, and having treatment for STIs free of charge with minimal inconvenience.