ORIGINAL RESEARCH ARTICLE
The value of testing multiple anatomic sites for gonorrhoea and chlamydia in sexually transmitted infection centres in the Netherlands, 2006–2010 F D H Koedijk MSc*, J E A M van Bergen MD PhD*†, N H T M Dukers-Muijrers PhD‡§, A P van Leeuwen MD PhD**, C J P A Hoebe MD PhD‡§, M A B van der Sande MD PhD*†† and on behalf of the Dutch STI centres *Centre for Infectious Disease Control, RIVM National Institute of Public Health and the Environment, PO Box 1, 3720 BA Bilthoven; †STI AIDS Netherlands, Amsterdam, Keizersgracht 392, 1016 GB Amsterdam; ‡Department of Infectious Diseases, Public Health Service South Limburg, PO Box 2022, 6160 HA Geleen; §Department of Medical Microbiology, School of Public Health and Primary Care (CAPHRI), Maastricht University Medical Center (MUMCþ), PO Box 5800, 6202 AZ Maastricht; **Department of Infectious Diseases, Municipal Health Service Amsterdam, PO Box 2200, 1000 CE Amsterdam; ††Academic Medical Centre Utrecht, University of Utrecht, Utrecht, Netherlands
Summary: National surveillance data from 2006 to 2010 of the Dutch sexually transmitted infection (STI) centres were used to analyse current practices on testing extragenital sites for chlamydia and gonorrhoea in men who have sex with men (MSM) and women. In MSM, 76.0% and 88.9% were tested at least at one extragenital site ( pharyngeal and/or anorectal) for chlamydia and gonorrhoea, respectively; for women this was 20.5% and 30.2%. Testing more than one anatomic site differed by STI centre, ranging from 2% to 100%. In MSM tested at multiple sites, 63.0% and 66.5% of chlamydia and gonorrhoea diagnoses, respectively, would have been missed if screened at the urogenital site only, mainly anorectal infections. For women tested at multiple sites, the proportions of missed chlamydia and gonorrhoea diagnoses would have been 12.9% and 30.0%, respectively. Testing extragenital sites appears warranted, due to the numerous infections that would have been missed. Adding anorectal screening to urogenital screening for all MSM visiting an STI centre should be recommended. Since actual testing practices differ by centre, there is a need for clearer guidelines. Routine gonorrhoea and chlamydia screening at multiple sites in STI centres should be investigated further as this might be a more effective approach to reduce transmission than current practice. Keywords: sexually transmitted infection, STI, screening, testing, chlamydia, gonorrhoea, multiple site, oral, pharyngeal, anorectal, MSM, women
INTRODUCTION Untreated infections with Neisseria gonorrhoeae and Chlamydia trachomatis, the causative agents of gonorrhoea and chlamydia in men and women, can result in epididymitis, cervicitis, urethritis and pelvic inflammatory disease (PID). PID may further lead to disseminated infections, ectopic pregnancy, infertility or abortion.1,2 Especially since chlamydia and gonorrhoea infections are often asymptomatic, rapid and appropriate diagnosis and treatment of chlamydia and gonorrhoea are the cornerstone of the public health approach, because it shortens the infectious period and limits transmission of the disease. An infection with chlamydia or gonorrhoea increases the Correspondence to: FDH Koedijk Email:
[email protected]
Dutch STI centres: A van Daal (East), AP van Leeuwen (North-Holland Flevoland), F de Groot (North), AM Niekamp (Limburg), M Langevoort (Utrecht), AM van Camerijk (South-Holland North), J van de Sande (Zeeland-Brabant), HM Go¨tz (South-Holland South)
risk of acquiring HIV infection3,4 and in HIV positives, timely diagnosis and treatment of gonorrhoea and chlamydia may reduce the risk that they will transmit HIV.5 The standard approach towards screening for gonorrhoea and chlamydia is often restricted to urogenital screening in many countries. However, both gonorrhoea and chlamydia can be transmitted through unprotected urogenital, anorectal or oral sex. Patient identification and thereby adequate treatment and interruption of the chain of transmission can be hampered when patients are positive at another anatomic site than that sampled for testing. It is unknown how large this potentially missed sexually transmitted infection (STI) burden in health care is. In the Netherlands, guidelines recommend testing anorectal sites for chlamydia and gonorrhoea if anal intercourse or symptoms were reported, and testing the oropharyngeal site for gonorrhoea when oral sex was reported. Testing for oropharyngeal chlamydia is included as optional.6 To evaluate current screening strategies for both chlamydia and gonorrhoea in the Netherlands, data on prevalence of chlamydia and gonorrhoea by anatomic site are needed. Here we
International Journal of STD & AIDS 2012; 23: 626 –631. DOI: 10.1258/ijsa.2012.011378
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analyse prevalence rates based on available surveillance data for gonorrhoea and chlamydia at different anatomic sites for women and for men having sex with men (MSM). We also estimate the proportion of diagnoses that would have been missed and not treated if the clients who were currently tested at multiple anatomic sites had been tested urogenital only.
proportion of missed anorectal and/or oropharyngeal diagnoses was calculated among the positive diagnoses at all combinations of anatomic sites tested. Analyses were carried out using the software SAS v9.2 (SAS Institute Inc, Cary, NC, USA).
RESULTS Study population
MATERIALS AND METHODS Since 2006, 27 specific STI centres, within the public health services, provide STI/HIV testing and care, free of charge, targeted at high-risk groups (MSM, commercial sex workers and their clients, people having multiple sexual partners, people from STI/HIV endemic countries, young people) and people who want to be tested anonymously.7 The system of testing and care was set up in addition to the regular national health services (mainly general practitioners), to reach people who might otherwise not seek timely STI care. All new consultations and corresponding diagnoses are reported to the National Centre for Infectious Disease Control (based within the National Institute of Public Health and the Environment [RIVM]) for surveillance purposes, facilitated by a web-based application. A ‘new STI consultation’ is defined as a consultation for new symptoms or one resulting from routine STI screening of asymptomatic cases, both involving laboratory testing and medical examination. At each new consultation, information on demographics, behaviour, diagnostics and clinical outcome is recorded. Data collection does not allow identification of repeated visits by the same individual. National guidelines are that patients should be screened routinely for at least chlamydia, gonorrhoea and syphilis, as well as HIV since 2010. Additional anorectal and oropharyngeal testing is undertaken according to reported symptoms and/or sexual risk behaviour, following the Dutch Society of Dermatology and Venereology (NVDV) Guidelines. Microbiological diagnostics are carried out locally at laboratories related to the STI centres in accordance with standard procedures established in an STI screening protocol, including quality control measures. For gonorrhoea, diagnostics were performed using nucleic acid amplification tests (NAATs), sometimes in combination with culture; for chlamydia only NAATs were used.6 Urogenital infections were defined here as infections diagnosed on urine, urethral, cervical or vaginal specimens. For men, guidelines recommend urine or a urethral swab; in women, vaginal and/or cervical or urethral swabs were recommended.
Data analyses Based on all new consultations with at least a urogenital chlamydia and/or gonorrhoea test, positivity rates were calculated per anatomic test site by dividing the number of diagnoses per anatomic test site by the total number of tests per site (100%). All analyses were done separately for women and MSM. Since heterosexual men were rarely tested at more than one anatomic site (3%), they were not included in this analysis. Based on new consultations in which at least one other anatomic site was tested in addition to the urogenital site, the proportion of missed diagnoses was assessed in the virtual scenario of only screening at the urogenital site. Therefore, the
Between 2006 and December 2010, 207,134 new STI consultations in women and 69,506 in MSM were registered. In more than 99%, at least the urogenital site was screened for chlamydia and gonorrhoea (Table 1). Characteristics of the study population are shown in Table 1.
Chlamydia In the period 2006–2010, 79.5% of female patients were screened urogenitally only; 17.6% were also tested on two anatomical sites (either pharyngeal or anorectal) and 2.9% were tested at all three sites (Figure 1). In MSM this was 24.0%, 69.5% and 21.3%, respectively. Testing more than one anatomical site for chlamydia differed by STI centre, ranging from 32% to 96% in MSM and from 2% to 76% in women. Overall positivity rate for chlamydia in women was 10.7% and for MSM this was 10.4% (Table 1). In women, the positivity rate for urogenital infections was 10.4% during 2006 –2010 (Table 1). In MSM this was 4.3%; the positivity rate for anorectal infections was higher with 10.1%. Also in women, the positivity rate for anorectal infections was high with 9.3%. In contrast, pharyngeal positivity rates for chlamydia were lower in both groups (less than 3%). If all MSM currently tested at more than one anatomic site would have been screened only urogenitally for chlamydia, 4189 anorectal and/or pharyngeal diagnoses (128 isolated pharyngeal infections, 3947 isolated
Table 1 Characteristics of the study population, national STI surveillance within STI centres in the Netherlands, 2006 –2010
Age (years) ,25 25 –35 .35 Dutch ethnicity Commercial sex worker STI in last two years Median no of partners in , six months Known HIV-positive Chlamydia test Chlamydia positivity rate Urogenital Anorectal Oral Gonorrhoea test Gonorrhoea positivity rate Urogenital Anorectal Oral
Women (%) (n 5 207,134)
MSM (%) (n 5 69,506)
55.0 29.7 15.3 83.2 9.2 11.7 2 (0– 1980)
13.9 27.6 58.5 82.0 1.9 24.7 4 (0 –1024)
0.1 99.8 10.7 10.4 9.3 2.7 99.7 1.2 1.0 1.2 1.2
14.1 99.4 10.4 4.3 10.1 1.7 99.4 8.6 3.4 5.5 3.9
STI ¼ sexually transmitted infection; MSM ¼ men who have sex with men Data available since 2008
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Figure 1 Distribution of anatomic sites tested for chlamydia and gonorrhoea for women and men who have sex with men (national STI surveillance within STI centres in the Netherlands, 2006– 2010). STI ¼ sexually transmitted infection
anorectal infections and 114 pharyngeal/anorectal dual infections) would have been missed (Table 2); 66.5% of the total number of chlamydia diagnoses in the MSM group were detected at multiple mucosal sites (Figure 2). If MSM who were currently tested anorectally in addition to urogenitally and/or pharyngeally, were tested anorectally only, 21% (n ¼ 1303; 1187 isolated urogenital infections, 85 isolated pharyngeal infections and 31 urogenital and pharyngeal infections) would have been missed. In women, 13% (n ¼ 624; 427 isolated anorectal infections, 194 isolated pharyngeal infections and 3 anorectal/pharyngeal dual infections) of the diagnoses of chlamydia would have been missed in the group currently tested at more than one mucosal site.
Gonorrhoea For gonorrhoea, 69.8% of women were tested urogenitally only; 16.7% were tested at a second anatomic site and 13.4% were tested at three sites (Figure 1). In MSM, 88.9% were tested at more than one anatomic site, with 72.8% tested at three sites. Testing more than one anatomical site for gonorrhoea differed by STI centre, ranging from 37% to 100% in MSM and from 2% to 76% in women. As shown in Table 1, overall positivity rate for gonorrhoea in women was 1.2% and for MSM this was 8.6%. The positivity rate for urogenital gonorrhoea infections in women was 1.0%, for anorectal and pharyngeal gonorrhoea the positivity rate was 1.2%. In MSM, positivity rates were higher; 3.4%, 5.5% and 3.9%, for urogenital, anorectal and pharyngeal, respectively. If the MSM currently tested at three sites for gonorrhoea had been tested urogenitally only, 63.0% (n ¼ 3594) would not have been diagnosed as infected; 1154 isolated pharyngeal infections, 1883 isolated anorectal infections and 557 pharyngeal/anorectal dual infections would have been missed (Table 2, Figure 2). If MSM who were currently tested anorectally in addition to urogenitally and/or pharyngeally, were tested anorectally only, 44% (n ¼ 2406; 1126 isolated urogenital infections, 1049 isolated pharyngeal infections and 231 urogenital/pharyngeal dual infections) would have been missed. In women tested at more than one mucosal site, 30.0% (n ¼ 418) of the infections in this group would have been missed by screening urogenitally only, including 275 isolated pharyngeal infections, 115 isolated anorectal infections and 28 pharyngeal/anorectal dual infections.
DISCUSSION Using a large set of routinely collected STI surveillance data, the current study demonstrates a considerable missed STI burden in women and MSM visiting STI centres, in the scenario of urogenital screening only. While current guidelines already recommend screening extragenital sites based on symptoms or reported risk behaviour, the range between STI centres in the proportion of MSM and women actually being tested at multiple mucosal sites is very wide. This could be partly due to the fact that different populations visit different centres, but also suggests lack of uniform interpretation or implementation of these guidelines. Although there are no data available as to what extent the current study population reported extragenital sexual activities or symptoms, nor to what extent those not tested at multiple sites were at risk of anorectal or oropharyngeal STIs, our results show that patients of STI centres may benefit from comprehensive screening strategies involving multiple site sampling to avoid missed diagnoses of chlamydia and gonorrhoea. In the current analysis two-thirds of both chlamydia and gonorrhoea diagnoses would have been missed if MSM had been screened urogenitally only, which is comparable with results from other studies.5,8 – 10 USA and UK guidelines therefore recommend screening MSM for anorectal chlamydia and gonorrhoea and for pharyngeal gonorrhoea in addition to urogenital screening based on reported exposure.11,12 Australian guidelines advise screening all MSM at all anatomic sites for gonorrhoea, and urogenital and anorectal for chlamydia, regardless of reported exposures.13 Since more than half of all chlamydia and gonorrhoea diagnoses in MSM were anorectal in this study, with many isolated anorectal infections, adding at least standard anorectal screening to urogenital screening for all MSM visiting an STI centre in the Netherlands may be warranted to enable more effective interruption of transmission. Although we do not have insight into the reasons for (not) testing MSM anorectally, our results are unlikely to be significantly biased, since the majority (.80%) of MSM were already tested anorectally. In women presenting at STI centres, the effectiveness of additional anorectal screening for all should be evaluated further; however in the 20% of women currently tested anorectally in addition to urogenitally, isolated anorectal infections were found frequently. It is very likely that the group of women was tested according to their reported exposure
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Table 2 Anatomic test sites and sites of infection for chlamydia and gonorrhoea per risk group, national STI surveillance within STI centres in the Netherlands, 2006 –2010 Site of infection
Test site Chlamydia Women Total no. of tests: 206,753
MSM Total no. of tests: 69,051
Gonorrhoea Women Total no. of tests: 206,525
MSM Total no. of tests: 69,077
No. of tests
Urogenital only
Oral only
154
Urogenital only Urogenital and oral Urogenital and anorectal Urogenital and anorectal and oral Urogenital only Urogenital and oral Urogenital and anorectal Urogenital and anorectal and oral
164,346 24,169
17,254 1971
12,257
293
5981
151
40
16,569 5415
890 171
43
32,357
832
14,710
355
85
Urogenital only Urogenital and oral Urogenital and anorectal Urogenital and anorectal and oral Urogenital only Urogenital and oral Urogenital and anorectal Urogenital and anorectal and oral
144,238 25119
1044 172
155
9442
128
27,726
162
120
7637 5996
260 78
105
5127
69
50,317
1057
Anorectal only
Urogenital and oral
Urogenital and anorectal
Oral and anorectal
Urogenital anorectal and oral
Total no. of infections ( positivity rate) 22,083 (10.7%)
512 321 106
909 13
270
3
86
7189 (10.4%) 15 2793 1154
458 31
189
114
59
2436 (1.2%) 143 36 79
90 70
116
28
93
5968 (8.6%) 71 228 1049
1655
55 231
362
557
191
STI ¼ sexually transmitted infection; MSM ¼ men who have sex with men
histories, i.e. anal intercourse, but no information is available on this, nor on the exposure risks of women not tested at multiple sites. A recent Dutch study from a single STI centre found that screening women based on reported site of sexual contact for chlamydia and gonorrhoea increased the prevalence by 10% and 31%, respectively, compared with urogenital testing alone, indicating that reported exposure correlates well with increased STI risk.14 Since national results from the current study showed that testing women at multiple sites differed widely between STI centres, ranging from 2% to 76%, it is very likely that anorectal diagnoses are missed in those not tested at multiple sites, resulting in ongoing transmission. These differences also imply there is probably a need for clearer guidelines on testing multiple anatomic sites, followed by uniform implementation. Adding pharyngeal gonorrhoea screening to standard screening may also be relevant, since isolated pharyngeal infections were frequently found. Pharyngeal gonorrhoea infections are more frequently asymptomatic than anorectal and urogenital infections,15 16 and may therefore be missed more easily. Although asymptomatic pharyngeal gonorrhoea may clear spontaneously, previous studies showed that pharyngeal gonorrhoea infections may be important in the transmission of gonorrhoea and that screening of the pharynx could play a
role in reducing the prevalence of anorectal and urogenital gonorrhoea infections.17 – 19 The fact that pharyngeal gonorrhoea infections are more difficult to cure than genital tract infections also points out the importance to evaluate the added benefit of a standard pharyngeal examination for gonorrhoea for specific risk groups to enable appropriate treatment, interrupt further transmission and limit the emergence of (multi-) drug resistant gonococci.20 – 24 On the other hand, pharyngeal testing for chlamydia was less common and the positivity rate for pharyngeal chlamydia was low compared with urogenital and anorectal positivity rates. The benefit of pharyngeal chlamydia screening has been a topic of discussion for several years. Since pharyngeal chlamydia infections, like pharyngeal gonorrhoea infections, are mostly asymptomatic and people therefore do not seek treatment, it is difficult to assess the contribution of pharyngeal infections on further spread of chlamydia in the absence of clear data. While some studies found that transmission of chlamydia from the pharynx to the urethra was prevalent in MSM and that pharyngeal infections may be important in the transmission or persistence of chlamydia infections,25 – 27 other studies could not confirm that pharyngeal chlamydia infections were a health risk.28,29 So far, the Dutch guidelines, similar to those issued by Centers for Disease Control and Prevention,
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Figure 2 Proportion of non-urogenital diagnoses that would have been missed for different testing practices, in the virtual scenario where these patients were screened urogenitally only (national STI surveillance within STI centres in the Netherlands, 2006– 2010). STI ¼ sexually transmitted infection
do not recommend standard pharyngeal screening for chlamydia.6,12 The potential value of standard additional pharyngeal screening for chlamydia in (specific) risk groups remains a point of discussion and more evidence is needed on the outcomes of systematic pharyngeal testing as well as on the effect of aborting pharyngeal infections on transmission dynamics. The strength of the current study is the data being collected nationwide, yielding large numbers. A limitation is that results are based on data from STI centres, whose patients belong to high-risk groups, so our findings may not be representative for the general population or patients in general practice. More importantly, results showed that extragenital testing is much more widely practiced in some STI centres than in others. Therefore, extrapolation to the whole patient population of positivity rates by anatomical site and number of infections that would have been missed if not tested could be biased, especially in women, but also albeit to lesser extent in MSM. Also the fact that patients with symptoms would have been tested anyway, may overestimate the number of missed infections, but no data on symptoms were available. Another limitation of our study is that our data do not allow identification of repeated visits by the same individual, so some patients may be contributing multiple visits and the consultations may therefore be not entirely independent.
Conclusion Anorectal and pharyngeal gonorrhoea and chlamydia infections remain a public health concern. Testing extragenital sites seems to be warranted, especially in MSM, since many gonorrhoea and chlamydia infections would have been missed, resulting in ongoing transmission. Also in women, infections will be missed by screening urogenital sites only. Since current testing practices differ according to STI centre, there is a need for clearer guidelines on testing high-risk populations at multiple locations. Ongoing studies with systematic screening at three anatomic sites regardless of reported exposure, linked with clinical and epidemiological risk factor data collected from all patients, should enable evaluation of the actual gain in STI diagnoses and may lead to more targeted guidelines for screening policies. This will support optimal use of scarce diagnostic resources in interrupting the ongoing
transmission of chlamydia and gonorrhoea and preventing long-term sequelae.
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