Optimizing care and control

of sexually transmitted
infections in risk groups

Karlijn Kampman
Optimizing care and control of
sexually transmitted infections
in risk groups

Karlijn Kampman
Colofon

Cover Design and Layout: © evelienjagtman.com

Printing: Gildeprint – Enschede

ISBN: 978-94-6419-542-2

The work presented in this thesis was carried out within the Radboud Institute for
Health Sciences.

Financial support for printing of this thesis was kindly provided by the department of
Primary and Community care, Radboud Institute for Health Sciences, Radboudumc
and the Lide Jannink Stichting.

© 2022 Carolina (Karlijn) J.G. Kampman

All rights reserved. No parts of this publication may be reproduced, stored in a retrieval system
of any nature in any form or any means, electronic, mechanical, photocopying, recording or
otherwise, without prior written permission of the publisher.
Optimizing care and control of
sexually transmitted infections
in risk groups

Proefschrift

ter verkrijging van de graad van doctor

aan de Radboud Universiteit Nijmegen
op gezag van de rector magnificus prof. dr. J.H.J.M. van Krieken,
volgens besluit van het college voor promoties
in het openbaar te verdedigen op

woensdag 14 december 2022

om 14:30 uur precies

door

Carolina (Karlijn) Johanna Gertruda Kampman

geboren op 19 augustus 1980
te Almelo
Promotoren
Prof. dr. J. van der Velden
Prof. dr. C.J.P.A. Hoebe (Maastricht University)

Copromotor
Dr. J.L.A. Hautvast

Manuscriptcommissie
Prof. dr. M. de Bruin
Prof. dr. A.J.A.M. van der Ven
Dr. ir. E.L.M. Op de Coul (RIVM)

Paranimfen
Femke Koedijk
Nelleke Kistemaker-Koedijk
 “Sometimes all you hear about is the hate,
but there is more love in this world than you could possibly imagine”

The boy, the mole, the fox and the horse - Charlie Mackesy
Table of contents

Chapter 1 General introduction 11

Chapter 2 Retesting young STI clinic visitors with urogenital Chlamydia 35
trachomatis infection in the Netherlands; response to a text
message reminder and reinfection rates: a prospective study
with historical controls
CJG Kampman, FDH Koedijk, HCM Driessen-Hulshof, JLA
Hautvast, IVF van den Broek
Sexually Transmitted Infections, 2015
Chapter 3 Determinants of frequent and infrequent STI testing and STI 53
diagnosis related to test frequency among men who have
sex with men in the eastern part of the Netherlands: a 6-year
retrospective study
CJG Kampman, JCM Heijne, PHM Kistemaker-Koedijk, FDH
Koedijk, M Visser, JLA Hautvast
British Medical Journal Open, 2018
Chapter 4 Consultation rate and chlamydia positivity among ethnic 69
minority clients at STI clinics in the Netherlands
SB Ostendorf, CJG Kampman, CJPA Hoebe, J van der Velden, JLA
Hautvast, CHM van Jaarsveld
PLoS One, 2021
Chapter 5 Sexual risk and STI testing behaviour among Dutch female 85
and male self-employed sex workers; a cross-sectional study
using an Internet based survey
CJG Kampman, CMM Peters, FDH Koedijk, TS Berkenbosch, JLA
Hautvast, CJPA Hoebe
BMC Public Health, 2022
Chapter 6 Sexually transmitted infections in male heterosexual Dutch 105
clients who visited German cross-border female sex workers;
a 3 year retrospective study
CJG Kampman, CJPA Hoebe, R Koene, L Kamp, K Jansen, FDH
Koedijk, A Tostmann, JLA Hautvast
BMC Public Health, 2020
Chapter 7 Sexual behaviour and STI testing among Dutch swingers: A 121
cross-sectional internet based survey performed in 2011 and
2018
CJG Kampman, JLA Hautvast, FDH Koedijk, MEM Bijen, CJPA
Hoebe
PLoS One, 2020
Chapter 8 General discussion 143

Appendices 169
Summary 171
Samenvatting 177
Dankwoord 183
About the author 187
List of publications 189
Research Data Management 193
PhD portfolio 197
Chapter 1
General introduction
Background
1
Sexually transmitted infections (STI) are infections characteristically transmitted by
sexual contact, such as vaginal, anal and oral sex. There are more than 30 pathogens that
can spread through sexual contact, of which 8 are predominant. The 4 most common
bacterial infections, with each year an estimated 376 million new infections globally,
are syphilis, gonorrhoea, chlamydia and trichomoniasis, of which trichomonas (156
million) and chlamydia (127 million) are the most prevalent [1-3]. Globally, the 4 most
common viral STI are caused by the hepatitis B virus (around 240 million people are
living with chronic hepatitis B globally), the herpes simplex virus (more than 500
million people), the human immunodeficiency virus (HIV) (37.7 million people living
with HIV) and the human papillomavirus (HPV) (around 300 million women) [3-6].
The World Health Organization (WHO) estimates that worldwide every day more
than 1 million persons acquire an STI [3]. In general, trichomoniasis is the most prevalent
STI across all six WHO regions. The highest estimated prevalence and incidence rates of
chlamydia and trichomoniasis occur in the Americas. The highest rates of gonorrhoea
and syphilis occur in Sub Saharan Africa. Chlamydia is most prevalent STI in Europe
(and the Western Pacific) [7,8].
Being infected with an STI can result in a substantial burden of disease [9]. Though
the main bacterial STI caused by Chlamydia trachomatis, Neisseria gonorrhoeae, treponema
pallidum (syphilis or lues) and Trichomonas vaginalis, are curable and usually not fatal,
reported complications include pelvic inflammatory disease, ectopic pregnancy,
infertility, chronic pelvic pain, arthropathy and neurological and cardiovascular
disease [10,11]. Viral STI are mostly incurable and can cause a range of complications,
such as cervical cancer caused by HPV, cirrhosis and hepatocellular carcinoma
caused by hepatitis B and immunological abnormalities leading to an increased risk
of oncological complications, cardiovascular disease, bone disease, renal and hepatic
dysfunction and several other common morbidities caused by HIV [12,13] .
In the battle against STI, counselling and behavioural interventions that promote
primary prevention against STI, such as STI prevention education and counselling,
safer sex and risk reduction counselling are imperative and will strongly influence the
course of the STI epidemic [14-16]. Secondary prevention methods, such as STI testing,
treatment and partner notification, specifically targeting key populations, such as men
who have sex with men (MSM), and sex workers can further reduce the spread of STI
[16].
In the Netherlands, the STI healthcare is mainly provided by the STI clinics
(formally known as sexual health centres, providing a range of activities in promoting
sexual health, in conjunction with STI testing) and the general practitioners (GPs).
A small portion is provided by specialized care such as hospitals and commercial

13
providers. Of these providers, GPs perform most of the STI-related consultations in the
Netherlands, with roughly half to two-thirds of all clients or patients visiting the GP for
an STI consultation [17-19]. Most of the STI clinics are based within the regional Public
Health Services, which are commissioned by the municipalities. A total of 25 regional
Public Health Services organized into 8 regions provide an STI public healthcare
network covering the whole of the Netherlands. Besides STI care, the Public Health
Services also offer other services like youth health care, infectious disease control,
environmental health, inspection of childcare facilities, health promotion activities
and epidemiological surveillance [20].
The STI clinics of the Public Health Services are government funded, thus free
of public charge services, and are anonymous for clients. They aim to provide low-
threshold care to groups at risk of an STI. Internationally, these groups are referred to
as “key populations” as opposed to “STI risk groups”, as this latter label is considered
generally stigmatizing in view of the fact that the STI risk does not always apply to all
members of the group [14]. However, in the Netherlands they are referred to as STI risk
groups. These risk groups can contribute disproportionately to the transmission of STI
and sometimes these STI are transmitted to the general population through bridging
between populations [21,22]. The criteria for the Dutch STI risk groups eligible for STI
clinic care, are determined based on their STI prevalence or incidence rates and focuses
specifically on people who are hard to reach and/or are vulnerable, have a high risk of
being infected with an STI and who might otherwise not seek timely STI care [23]. The
current inclusion criteria to receive a free and anonymous STI test at an STI clinic are
listed below [24].

Current inclusion criteria to receive a free and anonymous STI test at an STI clinic:
• reporting STI related symptoms
• being notified for an STI exposure
• being a man who has sex with men (MSM)
• originating from an HIV/STI endemic area
• reporting a partner from an HIV/STI endemic area or MSM
• being aged under 25
• being a sex worker regardless of gender
• being a victim of sexual violence

14
As a result of these inclusion criteria, the STI clinics are attended by clients at high
risk of acquiring an STI, while referring clients with a low risk to the GP for an STI
1
consultation. Since the introduction of the STI clinics in the Netherlands, there has been
a strong growth in the total annual number of consultations, with a little over 100.000
consultations in 2010, and more than 150.000 consultations in 2019 nationally [24].
This increase in consultations can be explained by the design of the Dutch healthcare
system, in which STI testing at the GP requires a financial contribution from the patient
for laboratory costs (while the consultation at the GP is free of charge for the patient).
This thesis focuses on groups at risk of an STI: groups who do not test routinely,
groups who test with a suboptimal frequency and groups who are hard to reach by the
STI clinics; young people, MSM, ethnic minority clients and self-employed sex workers.
Furthermore, this thesis debates whether clients of female sex workers and swingers
(heterosexuals who, as couples, practice mate swapping or group sex with other couples
or heterosexual singles) should be reconsidered as an STI risk group, as they have been
excluded as a risk group since 2015.

STI risk groups

The corona virus disease pandemic has led to a breach in consultation- and STI
positivity rates among groups at the STI clinics in 2020. Therefore, in this introduction
the consultation- and STI positivity rates of 2019 are used [24].
The two most prevalent groups who visit the STI clinics are heterosexual young
people (around 57.000 consultations yearly) and MSM (around 55.000 consultations
yearly) [24]. Almost 30.000 ethnic minority clients visited an STI clinic in 2019, and a
little over 4500 female sex workers visited an STI clinic (and around 5600 including
MSM sex workers and heterosexual male sex workers) [24]. Since clients of sex workers
and swingers were no longer eligible for an STI test at the STI clinics, they are only
registered when they disclose themselves as being a client of a sex worker or a swinger
when they attend an STI clinic based on another eligibility criterium, thus yielding a
gross under registration of these two groups.
In line with these consultation rates, young people and MSM are described first,
then ethnic minority clients and female sex workers are covered, and lastly clients of
a female sex worker and swingers are discussed. In each group below, the reasons why
each group is or was considered an STI risk group are described, followed by their STI
testing behaviour and their STI positivity rate.

15
Young heterosexual people
Young people (adolescents or sexually active teens, and generally people who are
younger than 25 years) are at risk of STI due to behavioural, cognitive and biological
reasons [25]. From a behavioural perspective, studies have shown that adolescents
engage in high risk sexual behaviour, such as having multiple partners, and condomless
sex [26,27]. In addition, the increasing use of dating apps among young people can lead
to a false sense of security of sexual health when they share "common connections"
with potential partners (the “common connections” feature on Tinder, for example,
displays mutual Facebook friends between users, and might serve as an unintentional
validation of a user’s character) [28,29]. Furthermore, young people who are at risk
of STI tend to become sexually active at an early age, often have multiple partners,
and use/abuse substances or participate in sexualized drug use [30]. Adolescents are
also less likely than adults to access and utilize health services [26]. Barriers to health
services and concerns about confidentiality often prevent adolescents from performing
an STI test [25].
The cognitive factor refers to the prefrontal cortex of the brain (responsible for
executive function), which is still developing in young people [31]. As a consequence,
young adolescents are more likely to be concrete thinkers, with an underdeveloped
capacity for good judgment and decision making, resulting in an inability to plan ahead
[32]. As some STI may have adverse effects that may only display after a long period
of time (such as HIV or chlamydia), young people may not take the immediate actions
needed to avoid such future consequences [32]. Furthermore, young people may have
difficulty implementing complex tasks, such as condom use, which involves a series
of steps to be effective [32].
Biologically, adolescent females are more susceptible to an STI infection because
of lower production of cervical mucous, an increased cervical ectopy, decreased local
immunity, a smaller introitus and lack of lubrication that can lead to vaginal lesions
during sex [31,33,34]. In males, uncircumcised males are at increased risk of being
infected with an STI, regardless of age [34].

STI testing among young heterosexual people

The Dutch STI clinics offer young people under the age of 25 years, free of charge
and anonymous STI testing since the opening of the STI clinics in 2006. Of all clients
visiting an STI clinic in 2019, young clients were represented in 51% of all consultations
and 38% of all consultations were attended by young heterosexual clients [24]. At the
GPs, a sample of 404 practices (in 2019) and their total number of STI-related episodes
is extrapolated to the Dutch population, showing an increase per 1,000 population
over time for STI related episodes among people aged below 25 years (from 16.9 per
1,000 population in 2017, to 18.3 per 1,000 population in 2018 and to 20.8 per 1,000

16
population in 2019) [24,35]. A Scottish study performed in 2016 among a little under
1300 university students showed that students held a generally favorable attitude
1
towards STI testing and 52% reported ever having had an STI test [36]. Another UK
study shows that an internet-accessed STI testing and results service for young people
almost doubled uptake of STI testing among ‘never testers’ [37]. A Dutch study shows
that home collection is the preferred method for most young, low-risk, heterosexual
clients, who seek STI care [38].

STI positivity among young heterosexual clients

The STI positivity rate among young clients visiting an STI clinic in the Netherlands was
23%, compared to a 19% STI positivity rate among all clients who visited an STI clinic in
2019 [24]. Clients who were aged 19 years or younger, had the highest STI positivity rates
compared to all age groups; 26% among women aged younger than 19 years, 27% among
heterosexual men aged younger than 19 years and 24% among MSM aged younger than
19 years [24]. In general practice, the annual reporting rate of chlamydia among women
was higher among women aged under 25 years (4.7 per 1,000) than it was among women
aged 25 years and older (2.1 per 1,000). Similarly, the annual reporting rate of chlamydia
among men aged under 25 years of (2.5 per 1,000) was higher compared with men aged
25 years and older (2.0 per 1,000) [24].
According to Dutch guidelines, clients who were diagnosed with an STI in the
previous year are advised to perform a retest [23]. This policy is based on a number
of studies that determined high reinfection rates upon retesting [39-42]. A Dutch
study performed among different providers of STI care who retested chlamydia
positive individuals, calculated reinfection rates of 19% at the STI clinics, 15% at the
gynecologists and 17% at the GPs [41]. Another Dutch study specifically targeting
heterosexual STI clinic clients, also established that retesting produced a positive test
result in 20% of young heterosexuals (aged 25 years or younger) and heterosexuals of
any age with a chlamydia infection at initial consultation [42]. According to 2019 STI
clinic-data, the number of retests among young heterosexual people is low: only 10%
had a second consultation and a little over 1% had a third consultation, regardless of
being STI positive at first consultation [24].

Men who have sex with men

Sexually active gay, bisexual, and other men who have sex with men are
disproportionately at risk for STI, including HIV [43]. There are many reason behind
this increased risk, one being that higher rates of infections among the MSM
community increases the likelihood of a person coming into contact with a person
who is infected with an STI [44]. In parallel to this epidemiological explanation, STI
transmission among MSM is higher compared with other populations due to the higher

17
transmission probabilities during anal sex, which is the riskiest sexual behaviour for
exposure to HIV [44]. To illustrate this, the estimated per-act probability of acquiring
HIV is 138 per 10,000 exposures for condomless receptive anal sex compared to 8
per 10,000 exposures for condomless receptive vaginal sex [45]. Therefore, MSM are
also at risk of more severe STI like HIV, syphilis and hepatitis B and C. Furthermore,
chlamydia serovar L1, L2 or L3, which can cause lymphogranuloma venereum (LGV),
is more prevalent among MSM, than in other groups. LGV is considered a more
severe form of chlamydia, causing genital ulceration, painful inguinal adenopathy
or “buboes” and, if left untreated, can progress to a systemic spread, leading to a
number of extra-genital manifestations [46].
Furthermore, STI positivity rates are higher among MSM who report sexual risk
behaviour, such as performing unprotected anal sex, having a higher number of sex
partners, performing in group sex, and chemsex (using substances to enhance sexual
experience) [47-49]. Subsequently, chemsex has been associated with: multiple sexual
partners, group sex, condomless anal intercourse, fisting, sharing of sex toys, injecting drug
use and higher alcohol consumption [50-52]. Furthermore, the high number of overlapping
sexual relationships (concurrent partnerships) among MSM, accelerates the spread of
STI [53,54]. These concurrent partnerships are possibly fueled by the use of dating apps,
which are used by more than 60% of MSM, and in turn could lead to increased STI risk
behaviour [55,56]. Finally, the criminalization of, stigma attached to, and the discrimination
and violence against MSM (to varying extents in different countries), has created an
environment in which MSM are less likely to access health services [43].

STI testing among MSM

As applies to all STI risk groups, offering STI testing for MSM reduces the health risk of
men who are infected and decreases the risk of transmission to their partners [21]. A
large European internet survey study, performed among MSM in European countries
in 2017, determined that 58% of participating Dutch MSM (n=786) reported being
tested for STI [57]. Though testing only once for STI can be of major value, retesting
MSM can yield an even greater merit in early detection and halting further spread of
STI [39,58,59]. In the Netherlands, guidelines advise MSM to test at least twice a year;
and high-risk MSM (e.g. HIV-positive MSM, MSM who are commercial sex workers
and MSM who take pre-exposure prophylaxis to reduce risks of HIV infection), four
times a year [23]. In 2019, around 30,000 MSM tested for STI at one of the STI clinics in
the Netherlands; 35% had a second consultation, 13% had a third consultation, and
5% had a fourth consultation at an STI clinic [24]. Another Dutch study calculated
that the proportion of consistent 6-monthly testers among MSM visiting an STI clinic,
was low with 19%, and an association between risk behaviour and test behaviour was
established in this study [60].

18
STI positivity among MSM
The STI positivity rates among MSM are high, compared with other groups, see table
1
1 below. The percentage of chlamydia positivity among MSM visiting an STI clinic
has remained stable at 10%, for many years [24]. Of all chlamydia diagnoses in 2019
in the Netherlands, MSM accounted for 23% [24]. Among HIV-negative MSM, the LGV
positivity rate was low over the full period, but slowly increased from 0.2% in 2010 to
0.5% in 2019 [24]. The percentage of gonorrhoea infections among MSM visiting an STI
clinic also remained stable in recent years (11%), with MSM accounting for 77% of all
gonorrhoea diagnoses [24]. The percentage of positive test results of infectious syphilis
among MSM remained relatively stable (from 2.9% in 2016, to 2.4% in 2018, and to 2.5%
in 2019), with 96% of these infections being diagnosed in MSM [24]. Regarding HIV, the
positivity rate among MSM has been decreasing for years (from 2.0% in 2010, to 0.3%
in 2019) [24].

Table 1. Number of STI diagnoses and percentage of positive tests among clients visiting a
Dutch STI clinic, by gender and type of sexual contact, 2019 [24]

Diagnosis Women Heterosexual men MSM

n (% positive) n (% positive) n (% positive)

Chlamydia 9,977 (15.3) 5,374 (18.4) 5,783 (10.6)

Gonorrhoea 1,262 (1.9) 658 (2.2) 6,266 (11.5)

Syphilis, infectious 17 (0.1) 35 (0.3) 1,378 (2.5)

HIV 8 (0.0) 4 (0.0) 152 (0.3)

Hepatitis B, infectious 13 (0.2) 22 (0.6) 32 (0.3)

Ethnic minority clients

Around 280 million people around the world are thought to be international migrants
[61,62]. The number of people who live in a country other than that of their birth has
more than doubled since a generation ago [62,63]. Once living in another country than
the country of birth, these migrants are considered an ethnic minority. An ethnic
minority is a group of people who differ in race or colour, or in national, religious,
or cultural origin from the dominant group (often the majority population), of the
country in which they live [64]. Even when healthcare is available to ethnic minority
populations, fear and distrust of healthcare institutions may lead to barriers in seeking
healthcare [65]. Social and cultural discrimination, language barriers, provider bias (or
the perception that these may exist), likely discourage some ethnic minority people
from seeking care [66,67]. Moreover, the quality of care can differ substantially for
ethnic minority patients compared with native patients [63].

19
STI testing among ethnic minority clients
In the Netherlands, 31% of all STI clinic attendees in 2019 were of non-Dutch origin.
Most non-Dutch consultations were attended by European clients (6% of total
clients, Eastern European clients excluded (3%)), followed by Asian clients (5%),
and Surinamese clients (4%) [24]. In the Eastern part of the Netherlands, only 18%
of STI clinic clients were registered as an ethnic minority client in 2019, and only
15% in 2018 [68]. A Dutch study conducted in four large Dutch cities, found higher
consultation rates among most ethnic minority clients, than among native Dutch
clients. The highest consultation rate was found among Latin American clients with
82.3 per 1,000 person years, compared with a consultation rate of 40.3 per 1,000
person years among native Dutch clients [69]. However, ethnic minority clients
from Turkey (9.6 per 1,000 person years), North Africa (15.5 per 1,000 person years),
Asia (24.0 per 1,000 person years) and Western countries (33.5 per 1,000 person
years), in this study, had lower consultation rates than native Dutch clients [69]. In
a Dutch survey study performed in 2011, a little over 8,000 participants showed that
Surinamese and Antilleans were found to test more often for STI, and Turkish and
Moroccans less often, than the Dutch, which was in line with another Dutch study
conducted in 2011-2014 in Amsterdam [70,71].

Figure 1. Percentage of positive STI tests among clients visiting a Dutch STI clinic, by
ethnicity, gender and sexual preference, 2019 [24]

STI positivity among ethnic minority clients

In a Dutch 2019 surveillance report, STI positivity was 19% in native Dutch clients
visiting an STI clinic compared with a 22% STI positivity rate among Eastern European

20
clients, a 20% STI positivity rate in African clients, and a high STI positivity rate of 25%
among Antillean or Aruban clients. The highest STI positivity rate was found among
1
Latin American MSM clients (28%), see figure 1 below [24].
A Dutch study conducted in 2003-2005 assessed whether older heterosexual men
of Surinamese and Antillean origin, might form a bridge population for STI, by having
unprotected sex in both the Netherlands, and their country of origin [72]. Another Dutch
study determined that 41% of the migrants were sexually active with other ethnicities
than their own, including the Dutch population, which is called disassortative mixing
[73]. This disassortative mixing may lead to an increased level of HIV and other STI,
not only within migrant groups, but also between migrant groups and in the Dutch
population [73,74]. Furthermore, in communities where the STI prevalence is high,
members of minority groups face a greater chance of encountering an STI infected
partner, than those in lower prevalence settings [75].

Sex workers
Sex workers are defined as female, male (having sex with men and/or women) and
transgender individuals, who receive income, employment, survival (e.g., food or
shelter), and/or drugs in exchange for sexual services (either regularly or occasionally)
[76]. Sex workers are at an increased risk of STI including HIV, due to biological reasons
(e.g., infection with another STI), behavioural reasons (e.g., number of sex partners
and/or inconsistent condom use), and stigma and discrimination (e.g., unsafe working
conditions, criminalization, lack of protection of human rights, and barriers to adequate
health services) [61]. The stigma placed upon sex workers by society, forces sex workers
to remain mostly anonymous about the fact that they perform sex work, out of fear of
anticipated governmental consequences, rejection by institutions (such as insurance
companies, banks or health care institutions), and out of fear of aggression, judgement,
and being shut out by friends, neighbors or institutions [76-80].
Often, sex workers lead a double life, which places a heavy burden on them, and
increases their feelings of being unsafe when they are visiting a client, as they cannot share
their work location with anyone [77,79]. In many countries sex work is not legally protected,
see figure 2 below [6]. Dutch legislation on sex work is aimed at reducing human trafficking
and only legalizes sex work with permits, forcing sex workers to disclose themselves as a
sex worker and needing to report themselves to a governmental institution to obtain such
permits, which many sex workers will not do [77,79-81]. For self-employed sex workers
especially, there are limited work-options without a permit leading them to work in illegal
circuits, which increases the risk of exploitation and unsafe working conditions [77,79].
Self-employed sex workers are defined as men, women or transgender men or
women, who have sex in exchange for money or goods, independent of a third party,
such as a manager, a pimp or a company [76,77,82,83]. These self-employed sex workers

21
are harder to reach for healthcare workers, since they are not organized or centralized
like sex workers who work in a formal indoor or outdoor setting [77]. Moreover, because
of trust issues with governmental institutions such as an STI clinic, and consequent
non-disclosure about sex work to healthcare workers, this group remains largely
hidden [77,78,84,85].

Figure 2. Percentage of countries with legal protection for sex workers, 2020 [6]

STI testing among sex workers

Data on sex workers in the Netherlands is limited to registries from the STI clinics,
where a rather small group of attendees in 2019, reported doing sex work in the past
6 months: 4,550 female sex workers (8% of all women), 154 male sex workers having
sex with women (0.6% of all heterosexual men) and 893 male sex workers having sex
with men (2% of all MSM) [24]. Dutch studies showed that sex workers with STI related
issues in less urbanized regions visit their GP more often than the STI clinic, while the
opposite is the case in urbanized regions [86,87].
Dutch guidelines advises STI testing twice a year for female sex workers and four
times a year for male sex workers having sex with men, and transgender sex workers
[23]. According to STI clinic data in 2019, the retest rate of female sex workers was 30%
for a second consultation and 9% for a third consultation. For male sex workers who
have sex with men, the retest rates were higher; 39% for a second consultation and 17%
for a third consultations [24].

STI positivity among sex workers

Of the sex workers who attended an STI clinic for an STI consultation in 2019, 9%
of female sex workers tested STI positive, 16% of male sex workers having sex with
women tested STI positive and 27% of male sex workers having sex with men tested
STI positive. A Dutch study (2009-2012) comparing STI positivity rates among female
sex workers, male sex workers having sex with men and MSM who did not get paid

22
for sex, found that male sex workers having sex with men, tested positive for STI in
40% of their consultations, and a new HIV infection being diagnosed in 8% of their
1
consultations, compared with a lower STI positivity rate of 14% among MSM, who did
not get paid for sex, and 9% among female sex workers [88]. This study also showed that
male sex workers who have sex with men are at higher risk of one or more new STI than
female sex workers, even after correction for age, ethnicity, known HIV positivity and
behavioural variables [88]. Another Dutch study conducted in 2014-2015 established
that the bacterial STI positivity was 29% in male sex workers having sex with men, 27%
in transgender sex workers, and 13% in male sex workers having sex with women [89].
Furthermore, 20% of male sex workers having sex with men and 20% of transgender
sex workers, in this study, were known HIV positive, compared with none of male sex
workers having sex with women [89].

Clients of sex workers

Clients of sex workers can serve as a bridging population between sex workers and the
general population when they become infected with an STI by a sex worker [90-93]. One
study determined that clients of female sex workers were 10 times more likely to have
an STI than men who did not report having sex with a female sex worker, while being
equally likely to use condoms inconsistently with their private partners [91]. The most
common reason for clients of sex workers to become infected with an STI is the high
demand for sex without a condom, and the offering of more money for unsafe sex,
which is, in turn, mostly accepted by the sex worker [94-97]. This demand for unsafe
sex by clients of sex workers, places the responsibility for condom use not only with
the sex worker, but equally with their clients, and underlines the need for preventative
efforts aimed towards them [94].

STI testing among clients of sex workers

As of 2015, clients of sex workers are no longer considered a high risk group of STI in the
Dutch STI clinic eligibility criteria, and although the registration of clients being a client
of sex workers has remained in place, the question of being a client of sex workers, upon
consultation, is not mandatory, thus resulting in a gross under-registration. To illustrate
this, 4,952 clients of female sex workers were registered in 2014 at the STI clinics in the
Netherlands, compared with 1,487 clients of female sex workers in 2019 [24,98].

STI positivity among clients of sex workers

Twelve percent of male clients having sex with a female sex worker tested STI positive
at an STI clinic in 2019, while the STI positivity rate among female sex workers was 9%
in the same year [24]. A possible explanation for the discrepancy in these STI positivity
rates among clients of female sex workers and female sex workers, is that clients of

23
female sex workers could have become STI positive by a casual non-paid sex partner.
Another possible explanation is that clients of sex workers visit sex workers abroad,
because of more unsafe sex being offered there. Anecdotal reports from clients of
female sex workers visiting STI clinics bordering Germany, confirm that clients visit
Germany for this unsafe sex offering. There are studies on cross-border commercial sex,
but as they are mostly concentrated on Vietnam, Mexico and Africa, they are difficult
to compare to the European situation, due to differences in cultural, economic, and
legislative contexts [99-102]. However, a British study determined that men who paid
for sex were more likely to report 10 or more sexual partners in the previous 5 years
(commercial and non-commercial sexual partners), were more likely to meet partners
abroad, and were more likely to report previous STI [103]. Another British study found
that unprotected vaginal sex was more common in men who had paid for sex abroad,
and 20% of these men, reported having had an STI [104].

Swingers
Swingers are defined as heterosexual couples who have sex with others and singles
who have sex with these couples [105,106]. Swingers are at risk of STI, as they engage in
risky sexual behaviour, such as unprotected sex with multiple sexual partners, group
sex and substance abuse [105,107,108]. One Dutch study using data from a convenience
sample of 289 swingers who visited an STI clinic between 2009 and 2012, determined
that 57% of swingers did not use a condom with vaginal sex, while at the same time,
77% of swingers reported that condom use is the norm in the swinger community
[109]. Another Dutch study established that condomless vaginal (46%), and condomless
anal sex (22%), was higher in drug-using swingers (vs 34% and 13% in non-drug-using
swingers) [106]. A Swedish study calculated much lower condom use rates among 235
participating swingers; 47% women and 39% men always used a condom during vaginal
sex [110].

STI testing among swingers

Up until 2015, swingers in the Netherlands could receive free of charge, and anonymous
STI testing at the STI clinics, mainly because of having had "3 or more partners in the
last 6 months", which was considered to be an eligibility criterium for STI clinic care
at that time. Consequently, STI testing and STI positivity rates among swingers are
difficult to assess from 2015 onwards. Two Dutch studies reported that STI testing is the
social norm among swingers [105,109]. However, in 2018, consultation rates of swingers
decreased from 4.8% in 2011, to 3.3% in 2018, of all consultations [111,112]. The number
of consultations among swingers in 2018 have mostly decreased for heterosexual
men and women but the number of consultations have increased for MSM-swingers,
suggesting a link between swingers and the MSM-network [111,112].

24
STI positivity among swingers
The STI positivity rates among swingers increased from 10% in 2011 to 18% in 2018,
1
compared to an overall STI positivity rate of 14% in 2011 and 18% in 2018 among
all clients visiting an STI clinic in the Netherlands [111,112]. Another Dutch study
performed between 2006-2013 determined that 3-4% of swingers visiting an STI clinic,
tested positive for gonorrhoea, and 6-8% did so for chlamydia [113]. A second Dutch
study found that the prevalence of chlamydia and/or gonorrhoea among swingers
visiting an STI clinic in 2009-2012 was 13% (no other STI were found) [107].

Aim and outline of this thesis

As described above, STI risk groups are at increased risk of STI, mainly through specific
risk factors, such as behavioural, cognitive, biological and social factors. Furthermore,
certain STI risk groups might perceive barriers towards health care, which may lead
them to not seek timely STI care. In the Netherlands, the STI clinics (in addition to
STI care provided by GPs and second line care) aim to provide low threshold STI care
for STI risk groups, by ensuring client’s anonymity and not charging for STI testing,
while referring people that are not considered a high risk group to the GP. These STI
risk groups are determined by a high STI prevalence and incidence rates, and focus
specifically on people who are hard to reach and/or are vulnerable, who have a high
risk of being infected with an STI, and who might otherwise not seek timely STI care.
One might question whether the STI clinics provide optimal STI care for these groups
at risk of an STI, or whether there is room for improvement?
This thesis aims to contribute to optimal STI care, STI control, and STI policy from
an STI clinic point of view, by studying (1) the STI care of two current STI risk groups,
and ways to optimize this care, (2) the reach of the STI clinic, and the STI risk and test
behaviour of two presumably underrepresented risk groups, and (3) the STI risk and
test behaviour of two groups, who are no longer eligible for free and anonymous STI
clinic-care. The outcomes of this thesis can be used to inform and guide policy makers
and STI clinic professionals, in developing and selecting targeted interventions towards
groups with high STI risk and/or a low STI test frequency, thereby optimizing overall
STI care and control.

The research questions and the outline of this thesis are;

1. Optimizing STI care in current STI risk groups: is there a retest necessity for
young chlamydia positive clients, and what is the optimal test frequency for
MSM based on STI positivity?

25
• Chapter 2: Young heterosexual clients
This chapter assesses the retest behaviour of young clients with a chlamydia-
infection and investigates the effect of a test message reminder to encourage
retesting, thereby evaluating the implementation of a retest advise.
• Chapter 3: Men who have sex with men
This chapter determines which MSM have a low test frequency and a high STI
positivity, urging this group to test more often.

2. Reaching underrepresented STI risk groups: what is the sexual risk behaviour
of ethnic minority clients and self-employed sex workers and do they attend the
STI clinic?
• Chapter 4: Ethnic minority clients
Chapter 4 describes consultation rates and chlamydia positivity rates among ethnic
minority clients, compared to native Dutch clients, and concludes whether ethnic
minority clients are indeed underrepresented at the STI clinics.
• Chapter 5: Self-employed sex workers
This chapter assesses sexual risk behaviour, STI test behaviour and STI positivity
among self-employed sex workers and gains more insight in this possibly hidden
STI risk group.

3. Considering non-eligible STI risk groups: what is the sexual risk behaviour and
STI test behaviour of clients of female sex workers and swingers?
• Chapter 6: Clients of female sex workers
This chapter assesses whether clients who visit a female sex worker abroad,
especially a female sex worker in cross-border Germany, are at risk of STI
compared to clients who visit a Dutch sex worker, aiming to conclude whether
this subpopulation should be reconsidered as an STI risk group.
• Chapter 7: Swingers
Chapter 7 determines sexual risk behaviour, STI risk perception, STI test behaviour
(as well as attitudes, social norms, self-efficacy and barriers regarding STI testing),
and STI positivity among swingers, evaluating whether they should be reconsidered
as an STI risk group.

26
References
1
1. Rowley J, Vander Hoorn S, Korenromp E, Low N, Unemo M, Abu-Raddad LJ, et al. Global and
Regional Estimates of the Prevalence and Incidence of Four Curable Sexually Transmitted
Infections in 2016. WHO Bulletin. June 2019. Retrieved from: https://www.who.int/bulletin/
volumes/97/8/18-228486.pdf
2. World Health Organization. Report on global sexually transmitted infection surveillance, 2018.
Geneva: WHO; 2018. Retrieved from: https://www.who.int/reproductivehealth/publications/
stis-surveillance-2018/en/
3. World Health Organization. Sexually transmitted infections. WHO 2019. Retrieved from:
https://www.who.int/news-room/fact-sheets/detail/sexually-transmitted-infections-(stis)
4. Looker KJ, Magaret AS, Turner KM, Vickerman P, Gottlieb SL , Newman LM. Global
estimates of prevalent and incident herpes simplex virus type 2 infections in 2012. PLoS One
2015;10:e114989
5. De Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, et al. Worldwide prevalence
and genotype distribution of cervical human papillomavirus DNA in women with normal
cytology: a meta-analysis. Lancet Infect Dis 2007 Jul;7:453-9
6. UNAIDS. Global HIV & AIDS statistics — Fact sheet. UNAIDS 2021. Retrieved from: https://
www.unaids.org/sites/default/files/media_asset/UNAIDS_FactSheet_en.pdf
7. European Centre for Disease Prevention and Control. Presentation: annual epidemiological
report for 2017: Sexually Transmitted Diseases. Stockholm: ECDC; 2017. Retrieved from:
https://www.ecdc.europa.eu/en/publications-data/presentation-annual-epidemiological-
report-2017-sexually-transmitted-diseases
8. Chesson HW, Mayaud P, Aral SO, Holmes KK, Bertozzi S, Bloom RB, et al. Sexually transmitted
infections: impact and cost-effectiveness of prevention. Major Infectious Diseases. 3rd edition.
Washington (DC): The International Bank for Reconstruction and Development / The World
Bank; 2017 Nov 3. Chapter 10
9. GBD 2015 Disease and Injury Incidence and Prevalence Collaborators. Global, regional,
and national incidence, prevalence, and years lived with disability for 310 diseases and
injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet
2016;388:1545–602
10. Holmes KK, Sparling PF, Stamm WE, et al. Sexually transmitted diseases. New York: McGraw-
Hill, 2008
11. Unemo M, Bradshaw CS, Hocking JS, de Vries HJC, Francis SC, Mabey M, et al. Sexually
transmitted infections: challenges ahead. Lance Infect Dis 2017;17:e235-e279
12. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018:
GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.
CA Cancer J Clin. 2018 Nov;68(6):394-424
13. Deeks SG, Overbaugh J, Phillips A, Buchbinder S. HIV infection. Nat Rev Dis Primers
2015;1:15035
14. World Health Organization. Consolidated guidelines on HIV prevention, diagnosis, treatment
and care for key populations. WHO 2016, retrieved from: http://apps.who.int/iris/bitstream/
handle/10665/246200/9789241511124-eng.pdf?sequence=8

27
15. World Health Organization. Global Health Sector Strategy on Sexually Transmitted Infections,
2016–2021. WHO 2016. Retrieved from: https://www.who.int/reproductivehealth/publications/
rtis/ghss-stis/en/
16. World Health Organization. Global HIV, hepatitis and STI programmes. WHO 2021. Retrieved
from: https://www.who.int/teams/global-hiv-hepatitis-and-stis-programmes/populations/sex-
workers
17. Slurink IAL, K. Groen K, Arguedas Flores CM, Kroone M, Hogewoning A, Ott A, Niessen W,
Dukers-Muijers NHTM, Hoebe CJPA, Gotz HM, Meima A, Koedijk FDH, Kampman CJG,  Bergen
van JEAM. GPs and sexual health centres contribution to STI consultations in five Dutch
regions using laboratory data of Chlamydia trachomatis testing. Int J STD AIDS 2020;31:517-
525
18. Van den Broek IV, Verheij RA, van Dijk CE, Koedijk FD, van der Sande MA, van Bergen JE.
Trends in sexually transmitted infections in the Netherlands, combining surveillance data
from general practices and sexually transmitted infection centers. BMC Fam Pract 2010;11:39
19. Den Heijer CD, van Liere GA, Hoebe CJ, van Bergen JE, Cals JW, Stals FS, Dukers-Muijrers NH.
Who tests whom? A comprehensive overview of Chlamydia trachomatis test practices in a
Dutch region among different STI care providers for urogenital, anorectal and oropharyngeal
sites in young people: a cross-sectional study. Sex Transm Infect 2016;92:211-7
20. GGD GHOR Nederland. Wat doet een GGD? GGD GHOR Nederland 2021. Retrieved from:
https://ggdghor.nl/home/wat-doet-een-ggd/
21. Wasserheit JN , Aral SO . The dynamic topology of sexually transmitted disease epidemics:
implications for prevention strategies. J Infect Dis 1996;174:S201–13
22. Low N, Broutet N, Adu-Sarkodie Y, Barton P, Hossain M, Hawkes S. Global control of sexually
transmitted infections. Lancet 2006;368: 2001–16
23. Rijksinstituut voor Volksgezondheid en Milieu. Het consult seksuele gezondheid. RIVM 2018.
Retrieved from: https://lci.rivm.nl/draaiboeken/consult-seksuele-gezondheid
24. Staritsky LE, van Aar F, Visser M, Op de Coul ELM, Heijne JCM, Götz HM, et al. Sexually
transmitted infections in the Netherlands in 2019. RIVM 2020
25. Shannon CL, Klausner JD. The growing epidemic of sexually transmitted infections in
adolescents: a neglected population. Curr Opin Pediatr 2018;30:137-143
26. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance 2016.
CDC; 2017
27. Carmine L, Castillo M, Fisher M. Testing and treatment for sexually transmitted infections
in adolescents--what’s new? J Pediatr Adolesc Gynecol 2014;27:50-60
28. Green SM, Turner D, Logan RG. Exploring the Effect of Sharing Common Facebook Friends
on the Sexual Risk Behaviors of Tinder Users. Cyberpsychol Behav Soc Netw 2018;21:457-462
29. Shapiro GK, Tatar O, Sutton A, Fisher W, Naz A, Perez S, Rosberger Z. Green. Cyberpsychol
Behav Soc Netw 2017;20:727-734
30. Kaestle CE, Halpern CT, Miller WC, et al. Young age at first sexual intercourse and sexually
transmitted infections in adolescents and young adults. Am J Epidemiol 2005;161:774-80
31. Steinberg L. Cognitive and affective development in adolescence. Trends Cogn Sci 2005; 9:69–
74
32. Holmes, KK, Sparling PF, Stamm WE, Berman SM, Hein K. Chapter 11: Adolescents and STDs,
including HIV infection. Sexually Transmitted Diseases (4th ed.), McGraw-Hill, New York
2007, pp. 165-186

28
33. Burchell AN, Winer RL, de Sanjose´ S, Franco EL. Chapter 6: epidemiology and transmission
dynamics of genital HPV infection. Vaccine 2006;24:S3/52–S3/61 1
34. Peipert JF. Clinical practice. Genital chlamydial infections. N Engl J Med 2003;18:2424-30
35. Staritsky LE, Visser M, van Aar F, Op de Coul ELM, Heijne JCM, van Wees DA, et al. Sexually
transmitted infections in the Netherlands in 2020. RIVM 2021
36. Martin-Smith HA, Okpo EA, Bull ER. Exploring psychosocial predictors of STI testing in University
students. BMC Public Health 2018;18:664
37. Wilson E, Leyrat C, Baraitser P, Free C. Does internet-accessed STI (e-STI) testing increase testing
uptake for chlamydia and other STIs among a young population who have never tested? Secondary
analyses of data from a randomised controlled trial. Sex Transm Infect 2019;95:569-574
38. Van Rooijen MS, Koekenbier RH, Hendriks A, de Vries HJ, van Leeuwen P, van Veen MG. Young
Low-Risk Heterosexual Clients Prefer a Chlamydia Home Collection Test to a Sexually Transmitted
Infection Clinic Visit in Amsterdam, the Netherlands, A Cross-Sectional Study. Sex Transm Dis
2016;43:710-716
39. Rose SB, Garrett SM, Stanley J, Pullon SRH. Retesting and repeat positivity following diagnosis of
Chlamydia trachomatis and Neisseria gonorrhoea in New Zealand: a retrospective cohort study.
BMC Infect Dis 2017;17:526
40. Kollars K, Plegue M, Riley M. Testing for Chlamydia Reinfection Among Adolescent Patients in
Different Clinical Settings: How Are We Doing? PRiMER. 2017;1:16
41. Dukers-Muijrers NH, Van Liere GA, Hoebe CJ. Re-screening chlamydia trachomatis positive
subjects; a comparison of practices between an STI clinic, general practitioners and gynaecologists.
Sex Transm Infect 2013;89:25-27
42. Visser M, van Aar F, Koedijk FDH, Kampman CJG, Heijne JCM. Repeat Chlamydia trachomatis
testing among heterosexual STI outpatient clinic visitors in the Netherlands: a longitudinal study.
BMC Infect Dis 2017;17:782
43. World Health Organization. Prevention and treatment of HIV and other sexually transmitted
infections among men who have sex with men and transgender people: recommendations for
a public health approach 2011. Retrieved from: https://www.who.int/hiv/pub/guidelines/msm_
guidelines2011/en/
44. Hess KL, Crepaz N, Rose C, Purcell D, Paz-Baily G. Trends in Sexual Behavior Among Men Who
have Sex with Men (MSM) in High-Income Countries, 1990-2013: A Systematic Review. AIDS Behav
2017;21:2811-2834
45. Patel P, Borkowf CB, Brooks JT, Lasry A, Lansky A, Mermin J. Estimating per-act HIV transmission
risk: a systematic review. AIDS. 2014;28:1509–19
46. Sheinman MD, Vinod J. Lymphogranuloma Venereum Proctocolitis. In StatPearls [Internet].
Treasure Island (FL): StatPearls Publishing; 2021
47. Slurink IAL, van Benthem BHB, van Rooijen MS, Achterbergh RCA, van Aar F. Latent classes of
sexual risk and corresponding STI and HIV positivity among MSM attending centres for sexual
health in the Netherlands. Sex Transm Infect 2020;96:33-39
48. Desai S, Burns F, Schembri G, Williams D, Sullivan A, McOwan A, et al. Sexual behaviours and
sexually transmitted infection outcomes in a cohort of HIV-negative men who have sex with men
attending sexual health clinics in England. Int J STD AIDS 2018;29:1407-1416
49. Werner RN, Gaskins M, Nast A, Dressler C. Incidence of sexually transmitted infections in men
who have sex with men and who are at substantial risk of HIV infection - A meta-analysis of data
from trials and observational studies of HIV pre-exposure prophylaxis. PLoS ONE 2018;13:e0208107

29
50. Bourne A, et al . The Chemsex study: drug use in sexual settings among gay and bisexual men
in Lambeth, Southwark and Lewisham. London School of Hygiene and Tropical Medicine,
2014
51. Hegazi A, Lee MJ, Whittaker W, et al . Chemsex and the city: sexualised substance use in gay
bisexual and other men who have sex with men attending sexual health clinics. Int J STD
AIDS 2017;28:362–6
52. Glynn RW, Byrne N, O’Dea S, et al . Chemsex, risk behaviours and sexually transmitted
infections among men who have sex with men in Dublin, Ireland. International Journal of
Drug Policy 2018;52:9–15
53. Tieu HV, Nandi V, Frye V, Stewart K, Oquendo H, Bush B, et al. Concurrent partnerships and
HIV risk among men who have sex with men in New York City. Sex Transm Dis 2014;41:200-8
54. Rosenberg ES, Khosropour CM, Sullivan PS. High prevalence of sexual concurrency and
concurrent unprotected anal intercourse across racial/ethnic groups among a national, Web-
based study of men who have sex with men in the United States. Sex Transm Dis 2012;39:741-6
55. Hoenigl M, Little SJ, Grelotti D, Skaathun B, Wagner GA, Weibel N, Stockman JK, Smith DM.
Grindr Users Take More Risks, but Are More Open to Human Immunodeficiency Virus (HIV)
Pre-exposure Prophylaxis: Could This Dating App Provide a Platform for HIV Prevention
Outreach? Clin Infect Dis 2020;71:e135-e140
56. Winetrobe H, Rice E, Bauermeister J, Petering R, Holloway IW. Associations of unprotected
anal intercourse with Grindr-met partners among Grindr-using young men who have sex
with men in Los Angeles. AIDS Care 2014;26:1303–8
57. Doran J, Weatherburn P, Hickson F, Marcus U, Reid D, Schmidt AJ. An update on the
performance of STI services for gay and bisexual men across European cities: results from
the 2017 European MSM Internet Survey. Sex Transm Infect 2021;97:201-208
58. Hsu KK, Molotnikov LE, Roosevelt KA, Elder HR, Klevens RM, DeMaria Jr A, et al.
Characteristics of Cases With Repeated Sexually Transmitted Infections, Massachusetts, 2014-
2016 . Clin Infect Dis 2018;67:99-104
59. Fung M, Scott KC, Kent CK, Klausner JD. Chlamydial and gonococcal reinfection among men:
a systematic review of data to evaluate the need for retesting. Sex Transm Infect 2007;83:304-9
60. Visser M, Heijne JCM, Hogewoning AA, van Aar F. Frequency and determinants of consistent
STI/HIV testing among men who have sex with men testing at STI outpatient clinics in the
Netherlands: a longitudinal study. Sex Transm Infect 2017;93:396-403
61. European Centre for Disease Prevention and Control. Mapping of HIV/STI behavioural
surveillance in Europe. Stockholm: ECDC; 2009. Retrieved from: https://www.ecdc.europa.
eu/sites/default/files/media/en/publications/Publications/0909_TER_Mapping_of_HIV_STI_
Behavioural_Surveillance_in_Europe.pdf
62. United Nations Department of Economic and Social Affairs, Population Division (2020).
International Migration 2020 Highlights (ST/ESA/SER.A/452). Retrieved from: https://www.
un.org/development/desa/pd/sites/www.un.org.development.desa.pd/files/undesa_pd_2020_
international_migration_highlights.pdf
63. International Organization for Migration. World Migration 2008: managing labour mobility
in the evolving global economy. Geneva: IOM; 2008
64. Healey JF, Stepnick A, O’Brien E. Race, ethnicity, gender, & class : the sociology of group
conflict and change. Thousand Oaks, California 2018.
65. Centers for Disease Control and Prevention. National Center for HIV/AIDS Hepatitis Viral STD
and TB Prevention: 2006 Disease Profile. 2008, 30-35

30
66. Berk ML, Schur CL. The effect of fear on access to care among undocumented Latino
immigrants. J Immigr Health 2001;3:151–156 1
67. Pérez-Escamilla R. Health care access among Latinos: Implications for social and health care
reform. J Hispanic High Educ 2010;9:43–60
68. Thermometer Seksuele Gezondheid Oost Nederland. Retrieved from: https://
seksuelegezondheidoostnederland.nl/wp-content/uploads/2019/07/Thermometer-seksuele-
gezondheid-Oost-NL-2018-DEF.pdf
69. Van Oeffelen AA, Van den Broek IV, Doesburg M, et al. Ethnic and regional differences in STI
clinic use: a Dutch epidemiological study using aggregated STI clinic data combined with
population numbers. Sex Transm Infect 2017;93:46-51
70. Goenee M, Kedde H, Picavet C. Condoomgebruik en testgedrag in Nederland. Tijdschrift voor
Seksuologie 2012;36:12
71. Hulstein SH, Matser A, Alberts CJ, et al. Differences in Chlamydia trachomatis seroprevalence
between ethnic groups cannot be fully explained by socioeconomic status, sexual healthcare
seeking behavior or sexual risk behavior: a cross-sectional analysis in the Healthy Life in an
Urban setting (HELIUS) study. BMC Infectious Diseases 2018;18:612
72. Kramer MA, Van Veen MG, Op de Coul ELM, Geskus RB, Coutinho RA, Van de Laar MJW, et
al. Migrants travelling to their country of origin: a bridge population for HIV transmission?
Sex Transm Infect 2008;84:554-5
73. Van Veen MG, Kramer MA, Op de Coul ELM, Van Leeuwen AP, De Zwart O, Van de Laar MJW,
et al. Disassortative sexual mixing among migrant populations in The Netherlands: a potential
for HIV/STI transmission? AIDS Care 2009;21:683-91
74. Van Veen MG, Schaalma H, Van Leeuwen AP, Prins M, De Zwart O, Van de Laar MJW, et
al. Concurrent partnerships and sexual risk taking among African and Caribbean migrant
populations in the Netherlands. Int J STD AIDS 2011;22:245-50
75. Hogben, Matthew & Leichliter, Jami. Social Determinants and Sexually Transmitted Disease
Disparities. Sexually Transmitted Diseases 2008;35:S13–8
76. European Centre for Disease Prevention and Control. Expert consultation meeting: sexually
transmitted infections among sex workers 21 - 22 October 2014, Stockholm, Sweden.
Stockholm: ECDC; 2015. Retrieved from: https://www.nswp.org/sites/nswp.org/files/Sex%20
Work%20Expert%20Consultation%20Meeting%20Report_brief_v4.pdf
77. Kloek M, Dijkstra M. Sekswerk en geweld in Nederland. Aidsfonds 2018
78. Dourado I, Guimarães MDC, Damacena GN, Magno L, de Souza Júnior PRB, Szwarcwald CL;
Brazilian FSW Group. Sex work stigma and non-disclosure to health care providers: data from
a large RDS study among FSW in Brazil. BMC Int Health Hum Rights 2019;19:8
79. Campbell R, Sanders T, Scoular J, Pitcher J, Cunningham S. Risking safety and rights: online
sex work, crimes and ‘blended safety repertoires’. Br J Sociol 2019;70:1539-1560
80. Elmes J, Stuart R, Grenfell P, Walker K, Hill J, Hernandez P, et al. Effect of police enforcement
and extreme social inequalities on violence and mental health among women who sell sex:
findings from a cohort study in London, UK. Sexually Transmitted Infections Published
Online First: 26 October 2021
81. Albright E, D’Adamo K. Decreasing Human Trafficking through Sex Work Decriminalization.
AMA J Ethics 2017;19:122-126
82. Van Veen MG, Götz HM, van Leeuwen PA, et al. HIV and sexual risk behavior among
commercial sex workers in the Netherlands. Arch Sex Behav. 2010;39:714-23

31
83. Reeves A, Steele S, Stuckler D, et al. National sex work policy and HIV prevalence among
sex workers: an ecological regression analysis of 27 European countries. Lancet HIV
2017;4:e134-e140
84. Lasater ME, Grosso A, Ketende S, Lyons C, Pitche VP, Tchalla J, et al. Characterising the
relationship between migration and stigma affecting healthcare engagement among female
sex workers in Lomé, Togo. Glob Public Health 2019;14:1428-1441
85. Nyblade L, Reddy A, Mbote D, Kraemer J, Stockton M, Kemunto C, et al. The relationship
between health worker stigma and uptake of HIV counseling and testing and utilization of
non-HIV health services: the experience of male and female sex workers in Kenya. AIDS Care
2017;29:1364-1372
86. Woestenberg PJ, van Oeffelen AA, Stirbu-Wagener I, van Benthem BH, van Bergen JE, van den
Broek IV. Comparison of STI-related consultations among ethnic groups in the Netherlands:
an epidemiologic study using electronic records from general practices. BMC Fam Pract
2015;16:70
87. Trienekens SC, van den Broek IV, Donker GA, van Bergen JE, van der Sande MA. Consultations
for sexually transmitted infections in the general practice in the Netherlands: an opportunity
to improve STI/HIV testing. BMJ Open 2013;3:e003687
88. Verhaegh-Haasnoot A, Dukers-Muijrers NH, Hoebe CJ. High burden of STI and HIV in male
sex workers working as internet escorts for men in an observational study: a hidden key
population compared with female sex workers and other men who have sex with men. BMC
Infect Dis 2015;15:291
89. Drückler S, van Rooijen MS, de Vries HJC. Substance Use and Sexual Risk Behavior Among
Male and Transgender Women Sex Workers at the Prostitution Outreach Center in Amsterdam,
the Netherlands. Sex Transm Dis 2020;47:114-121
90. Mulberry N, Rutherford AR, Wittenberg RW, Williams BG. HIV control strategies for sex
worker-client contact networks. J R Soc Interface 2019;16:20190497
91. Huang ZJ, Wang W, Martin MC, Nehl EJ, Smith BD, Wong FY. “Bridge population”: sex workers
or their clients? STI prevalence and risk behaviors of clients of female sex workers in China.
AIDS Care 2011;23:45-53
92. Chen Y, Abraham Bussell S, Shen Z, Tang Z, Lan G, Zhu Q, et al. Declining Inconsistent
Condom Use but Increasing HIV and Syphilis Prevalence Among Older Male Clients of Female
Sex Workers: Analysis From Sentinel Surveillance Sites (2010-2015), Guangxi, China. Medicine
(Baltimore) 2016;95:e3726
93. Shah NS, Shiraishi RW, Subhachaturas W, Anand A, Whitehead SJ, Tanpradech S, et al.
Bridging populations-sexual risk behaviors and HIV prevalence in clients and partners of
female sex workers, Bangkok, Thailand 2007. J Urban Health 2011;88:533-44
94. Deering KN, Lyons T, Feng CX, Nosyk B, Strathdee SA, Montaner JS, Shannon K. Client
demands for unsafe sex: the socioeconomic risk environment for HIV among street and off-
street sex workers. J Acquir Immune Defic Syndr 2013;63:522-3
95. Johnston CL, Callon C, Li K, Wood E, Kerr T. Offer of financial incentives for unprotected sex
in the context of sex work. Drug Alcohol Rev 2010;29:144–149
96. Choi SYP, Holroyd E. The influence of power, poverty and agency in the negotiation of condom
use for female sex workers in mainland China. Cult Health Sex 2007;9:489–503
97. Patterson TL, Volkmann T, Gallardo M, Goldenberg S, Lozada R, Semple SJ, et al. Identifying
the HIV Transmission Bridge: Which Men Are Having Unsafe Sex With Female Sex Workers
and With Their Own Wives or Steady Partners? JAIDS 2012;60:414–420

32
98. Van Oeffelen AAM, van Aar F, van den Broek IVF, Op de Coul ELM, Woestenberg PJ, Heijne
JCM, et al. Sexually transmitted infections, including HIV, in the Netherlands in 2014. RIVM 1
2015
99. Zhang Y, Liang B, Liu D, Wei G, Mo S, Nong A, et al. Migrant female sex workers working at the
Sino-Vietnamese border for a short time have a higher risk of HIV transmission: a consecutive
cross-sectional study. AIDS Res Ther 2020;17:4
100. Yu J, Nehl EJ, Dinh VP, Liang B, Son NV, Meng D, et al. Vietnamese female sex workers in
rural cross-border areas of Guangxi, China: migration and HIV/STI risk behaviors. AIDS Care
2020;32:1515-1523
101. Gezie LK, Taye BW, Ayele. Time to unsafe sexual practice among cross-border female sex
workers in Metemma Yohannes, North West Ethiopia. BMC Public Health 2015 Jul 28;15:710
102. Robertson AM, Syvertsen JL, Ulibarri MD, Rangel MG, Martinez G, Strathdee SA. Prevalence
and correlates of HIV and sexually transmitted infections among female sex workers and their
non-commercial male partners in two Mexico-USA border cities. J Urban Health 2014;91:752-
67
103. Ward H, Mercer CH, Wellings K, Fenton K, Erens B, Copas A, et al. Who pays for sex? An
analysis of the increasing prevalence of female commercial sex contacts among men in
Britain. Sex Transm Infect 2005;81:467-71
104. Groom TM, Nandwani R. Characteristics of men who pay for sex: a UK sexual health clinic
survey. Sex Transm Infect 2006;82:364-7
105. Niekamp AM, Mercken AG, Hoebe CJPA, et al. A sexual affiliation network of swingers,
heterosexuals practicing risk behaviours that potentiate the spread of sexually transmitted
infections: a two-mode approach. Social Networks 2013;35:223–36
106. Evers YJ, Dukers-Muijrers NHTM, Kampman CJG, van Liere GAFS, Hautvast JLA, Koedijk FDH,
et al. Prevalence of drug use during sex among swingers and perceived benefits and risks - a
cross-sectional internet survey in the Netherlands. Sex Transm Infect 2020;96:40-46
107. Spauwen LW, Niekamp AM, Hoebe CJPA, et al. Drug use, sexual risk behaviour and sexually
transmitted infections among swingers: a cross-sectional study in The Netherlands. Sex
Transm Infect 2015;9:31-6
108. Dukers-Muijrers NH, Niekamp AM, Brouwers EE, et al. Older and swinging; need to identify
hidden and emerging risk groups at STI clinics. Sex Transm Infect 2010;86:315–17
109. Spauwen LWL, Niekamp AM, Hoebe CJPA, Dukers-Muijrers NHTM. Do swingers self-identify
as swingers when attending STI services for testing? A cross-sectional study. Sex Transm Infect
2018;94:559-561
110. Andersson N, Ejnestrand J, Lidgren Y, Allard A, Boman J, Nylander E. Are Swedish swingers
a risk group for sexually transmitted infections? Int J STD AIDS 2021;32:427-434
111. Trienekens SCM, Koedijk FDH, Van den Broek IVF, Vriend HJ, Op de Coul ELM, Van Veen MG,
et al. Sexually transmitted infections, including HIV, in the Netherlands in 2011. RIVM 2012
112. Slurink IAL, van Aar F, Op de Coul ELM, Heijne JCM, van Wees DA, Hoenderboom BM, et al.
Sexually transmitted infections in the Netherlands in 2018. RIVM 2019
113. Dukers-Muijrers NHTM, van Rooijen MS, Hogewoning A, et al. Incidence of repeat testing and
diagnoses of Chlamydia trachomatis and Neisseria gonorrhoea in swingers, homosexual and
heterosexual men and women at two large Dutch STI clinics, 2006-2013. Sex Transm Infect
2017;93:383-389

33
Chapter 2
Retesting young STI clinic visitors with
urogenital Chlamydia trachomatis
infection in the Netherlands;
response to a text message reminder and
reinfection rates: a prospective study with
historical controls

Carolina (Karlijn) J.G. Kampman

Femke D.H. Koedijk
Hélène C.M. Driessen-Hulshof
Jeannine L.A. Hautvast
Ingrid V.F. van den Broek

Published as a research article in Sexually Transmitted Infections, 2016 Mar;92(2):124-9

Abstract

Objectives
The objective of this study is to assess the effect of reminder text messages six
months after the initial treatment on retest- and chlamydia reinfection rates in young
heterosexuals as compared to a historical control group, and to assess factors associated
with both outcomes.

Methods
Heterosexual people (aged 16-23), testing positive for urogenital chlamydia, were
offered a retest after 6 months. Participants received a text message reminder at 6
months after the initial chlamydia diagnosis. Rates of retest uptake and result of the
retest were analysed using Cox regression. Prevalence ratios (PR’s) were calculated
to identify factors associated with these outcomes. Furthermore, the retest rate was
compared with the retest rate of a historical control group.

Results
30.6% of the study group returned within 5 to 8 months as compared to 9.2% in the
historical control group. Women and persons who were not notified for an STI at
inclusion were more likely to return for a retest. 20.3% participants had a chlamydia
reinfection upon retesting. Reinfection was higher in participants reporting STI related
symptoms (PR:3.2, 95%CI:1.8-5.6) and in participants who were notified for an STI at
retest (PR:5.3, 95%CI:2.4-11.5).

Conclusions
A text message reminder appeared to have a clear, positive impact on the resulting
retest rate. These results also indicate that retesting is necessary to identify chlamydia
reinfections.
Introduction

In the Netherlands, a significant part of sexually transmitted infection (STI) care is

provided by the freely accessible, low threshold STI clinics, where one can have an STI 2
test free of charge and anonymously. Most of these clinics are based within the public
health services, providing STI care additional to first line care by general practitioners.
The STI clinics are government funded aiming to reach high-risk groups including
young people (aged below 25 years) and men having sex with men, who might otherwise
not seek timely STI care [1].
Of all the heterosexual individuals who visited a municipal STI clinic, 12.8% of
young (aged 15-24) were diagnosed with chlamydia in 2012 [2]. Therefore, chlamydia
remains the most commonly diagnosed bacterial STI. The majority of chlamydia
infections are found amongst young people, below the age of 25 [2]. There are a
number of international studies that conclude that young people with chlamydia
are at risk for reinfection and should, therefore, be retested [3-5]. Retesting is crucial
because chlamydia infections, especially repeated episodes, are associated with pelvic
inflammatory disease (PID) and other reproductive sequelae [6]. In a database study
performed in the US among women aged 15-25 years with a chlamydia infection
between 2002 and 2006, the estimated majority of reinfections occurred between 2
and 5 months after treatment of the initial chlamydia infection [7].
Dutch dermatological guidelines already recommend retesting patients with
chlamydia infections, 6 months after the initial treatment [8]. Dutch research provides
evidence for high chlamydia reinfection rates at retest: a retrospective study in South
Limburg, in which retesting was performed based on a clients’ own initiative, found a
chlamydia reinfection rate of 19.0% in the period 3-12 months after the initial chlamydia
diagnosis [9]. Other evidence for high chlamydia reinfection rates at retest was provided
by a Dutch prospective study, in which clients received a home based test or a retest
at a clinic without the need for an appointment. The reinfection rate in this study
was 17.3% [10]. Until now, no prospective study in the Netherlands has evaluated the
efficacy of sending a simple mobile phone text message, to invite chlamydia positive
young individuals for a retest.
The aim of this study is to assess the effect of reminder text messages six months after
the initial treatment on retest- and chlamydia reinfection rates in young heterosexuals
as compared with a historical control group and to assess factors associated with both
outcomes.

37
Methods

Study setting, study design and population

We performed a prospective follow-up study, utilising 10 of the 25 STI clinics in the
Netherlands (see figure 1). The selected clinics were mainly situated in rural areas.
People are free to go to any STI clinic in the Netherlands, but clients who participated
in this study, could only go to one of the selected STI clinics for a retest. All clients aged
between 16 and 23, with a positive laboratory test for urogenital chlamydia, diagnosed
at one of the study STI clinics between May 2012 and May 2013, and whom were treated
with Azithromycin 1000 mg, were asked to participate in the study. We excluded clients
aged 24 years and older at T0, since they might have turned 25 years at retest (T1) and
they are therefore not eligible for a free STI test at the STI clinic. We excluded MSM as
well, as this target group already receives retest advice according to national guidelines.
However, bisexual women were included in this study, since they are not offered this
advice. For brevity, bisexual women are regarded as ‘heterosexual’ in this study.
As a control group, we retrospectively selected clients, satisfying the same inclusion
criteria, from the period January 2011 to January 2012. The control group was analysed to
determine how many clients had undergone a repeat test, based on their own initiative;
the control group did not receive a text message reminder for retesting. The retest rate
of the study group is compared with this control group. The reinfection rates and factors
associated with response to the retest offer and positivity at retest were also analysed.

Figure 1. Counties covered by STI clinics participating in current study (in dark grey), the
Netherlands, 2012-2013

38
Data collection
For the sample size calculation, we used data of our historical control group, in
which 9% came back on their own initiative for a retest between 5 and 8 months.
We expected that after sending a text message, 20% of the participants in our study 2
group would come back for a retest between 5 and 8 months. With an error of 5%
(alpha) and a power of 90% we would have to include a total of 211 participants in
both our study group and historical control group. The historical control group
was already reviewed before the start of the study and consisted of 547 persons, so
ample for meaningful comparison.
Clients meeting the inclusion criteria were asked to participate in the study
upon receipt of a positive chlamydia test outcome (T0). They received a letter
detailing the study and were asked to complete a consent form. Five-and-a-half
months after being treated for the chlamydia infection, participants received a
mobile phone text message, asking them to schedule an appointment for a retest.
Two weeks later, a second text message was sent as a reminder. The study allocated
a 2-month period in which a retest counted as a retest in the study data (T1), starting
after the second text message. Due to the fact that the inclusion period covered
12 months and the maximum follow-up period spanned 8 months, the total study
period was 20 months.
In the event that clients visited the STI clinic before receiving the first retest
reminder, that is, as a result of STI symptoms or notification, and the test provided
a chlamydia-positive outcome, then the test was considered a retest. If the test
results were found to be chlamydia negative, then the client still received the text
messages 5.5 and 6 months after T0. Participants could only participate once; when
participants tested positive in a retest, they could not enter the study for the second
time.
All participating STI clinics used an online patient registration system. The
following variables were used in the analyses at T0 and T1: gender, age, ethnicity
(when the participant or one of his/her parents was born outside the Netherlands,
the participant was regarded as having a non-Dutch ethnicity), notification by a
partner, STI symptoms, living in a city or a rural area, number of sexual partners
in the last 6 months and condom use during the last sexual contact.

Data analysis
The χ2 test was used for testing differences in proportions between participants and
non-participants. A p value of <0.05 was considered to be statistically significant.
Since our main outcomes (participation in retesting and chlamydia positivity at
retest) were common (prevalence >10%), Cox regression analyses were performed
to identify factors associated with the resulting outcomes. Factors associated with

39
a p value of <0.20 in univariate analyses were further analysed by multivariate Cox
regression, using the Enter method, in which we manually selected the factors to
be used in the multivariate regression analyses. In the multivariate model, factors
with a p<0.05 were considered to be statistically significant. Prevalence ratios (PRs)
and 95% CIs were calculated to compare the proportions of the factors associated
with retesting (table 1) or reinfection (table 2) between both groups. Analyses were
carried out using the IBM SPSS software V.22.

40
Results

Study population
A total number of 2,108 young people were eligible to participate in the study, of which 2
828 (39.3%) gave consent to participate. Participants differed from non-participants with
respect to: gender (72.9% of participants were women vs 61.7% of the non-participants),
STI-symptoms (32.4% vs 37.5%, respectively) and being notified for an STI (29.1% vs
34.5%, respectively, all p<0.05).

Response to the retest offer

Within 8 months after the initial test, 33.2% (275/828) of the participants returned for
a retest. Eight percent (22/275) requested a retest based on their own initiative (before
receiving a text message reminder), tested chlamydia positive and were, therefore,
considered ‘retesters’. The actual response after receiving the reminder text message
was 30.6% (253/828).
As shown in table 1, the retest rate was significantly higher for women (36.5%
versus 24.6%), for Dutch participants (34.9% vs 23.4%) and for participants who were
not notified (at T0) (36.9% vs 22.9%), all p<0.05. In multivariate analyses, being women
(PR:1.4, 95%CI:1.0 to 1.9) and not being notified by a partner at T0 (PR:0.6, 95%CI:0.5
to 0.9) were significantly associated with retesting.

41
 Table 1. Factors associated with retesting and retest rate with regard to chlamydia retesting in 10
participating sexually transmitted infection (STI) clinics in the Netherlands, May 2012 - May 2013

Factors n invited n Retest rate % Univariate Cox Multivariate

(measured (%) response (95%CI) regression Cox regression
at T0) PR(95%CI) PR(95%CI)**

Total 828 275 33.2

Gender

Male 228 (27.5) 56 24.6(18.9-30.2) 1.0 1.0

Female 600(72.5) 219 36.5(32.6-40.4) 1.5(1.1-2.0) 1.4 (1.0-1.9)

Age (years)

16-19 290 (35.0) 97 33.4(28.0-38.9) 1.0(0.8-1.3) nt

20-23 538 (65.0) 178 33.1(29.1-37.1) 1.0

Ethnicity

Dutch 704 (85.0) 246 34.9(31.4-38.5) 1.5(1.0-2.2) 1.4(1.0-2.1)

Non-Dutch 124 (15.0) 29 23.4(15.8-30.9) 1.0 1.0

Notified by partner

Yes 218 (26.3) 50 22.9(17.3-28.6) 0.6(0.5-0.8) 0.6(0.5-0.9)

No 610 (73.7) 225 36.9(33.0-40.7) 1.0 1.0

STI related symptoms*

Yes 265 (32.0) 86 32.5(26.8-38.1) 1.0(0.8-1.3) nt

No 552 (66.9) 184 33.2(29.3-37.1) 1.0

Residence*

City 434 (52.4) 157 36.2(31.6-40.7) 1.2(1.0-1.6) 1.2(0.9-1.5)

Rural 368 (44.4) 109 29.6(24.9-34.3) 1.0 1.0

No of partners < 6 months

0-2 505 (61.0) 161 35.3(30.1-40.5) 1.0 nt

≥3 323 (39.0) 114 31.9(27.8-36.0) 1.1(0.9-1.4)

Condom use last sexual contact*

Yes 143 (17.3) 48 33.6(25.7-41.4) 1.0(0.7-1.4) nt

No 683 (82.5) 226 33.1(29.6-36.6) 1.0

nt, not tested in multivariate model, since p>0.20 in univariate analysis

In bold: significant (p<0.05); due to rounding to one decimal place, 1.0 is not always significant
* Determinant contains missings
** Adjusted for gender, ethnicity, notified by partner and urbanisation
PR, prevalence ratio

42
Reinfection rates
We found a total number of 56 chlamydia reinfections among those who came back for
a retest before or after the text message reminder, indicating a positivity rate of 20.4%
(56/275). This is higher than the overall chlamydia positivity rate among all eligible 2
visitors of the STI clinic, during the study period of 20 months (15.9%). Table 2 shows
that reinfections were found significantly more often in clients who were notified by a
partner (90.0% vs 17.1%), in clients who reported STI related symptoms (53.7% versus
14.3%) and in clients who had three or more partners in the last 6 months (40.4% vs
15.7%) (at T1). In multivariate analyses, STI related symptoms (PR: 3.2, 95%CI:1.8 to
5.6) and being notified by a partner (PR: 5.3, 95%CI:2.4 to 11.5) were characteristics at
T1 associated with chlamydia reinfection.
We also analysed whether factors at T0 were predictive for having a reinfection at
retest. No significant associations were found.

43
 Table 2: Characteristics and chlamydia positivity rates of participants who came for retest in one
of the 10 participating sexually transmitted infection (STI) clinics in the Netherlands, 2012-2013

Factors n n positive Positivity rate Univariate Cox Multivariate

(measured response for % (95%CI) regression Cox regression
at T1) (%) chlamydia PR(95%CI) PR(95%CI)**

Total 275 56 20.4

Gender

Male 56 (20.4) 15 26.8(14.8-38.3) 1.0 nt

Female 219(79.6) 41 18.7(13.5-23.9) 0.7(0.4-1.3)

Age (years)

16-19 81 (29.5) 19 23.5(14.0-32.9) 0.8(0.5-1.4) nt

20-23 194 (70.5) 37 19.1(13.5-24.6) 1.0

Ethnicity

Dutch 246 (89.5) 48 19.5(14.5-24.5) 0.7(0.3-1.5) nt

Non-Dutch 29 (10.5) 8 27.6(10.3-44.8) 1.0

Notified by partner

Yes 10 (3.6) 9 90.0(67.4-112.6) 5.1(2.5-10.4) 5.3(2.4-11.5)

No 265 (96.4) 47 17.7(13.1-22.4) 1.0

STI related symptoms*

Yes 41 (15.1) 22 53.7(37.7-69.6) 3.8(2.2-6.4) 3.2(1.8-5.6)

No 231 (84.9) 33 14.3(9.7-18.8) 1.0 1.0

Residence*

City 157 (59.0) 38 24.2(17.4-31.0) 1.6(0.9-2.7) 1.6(0.9-2.9)

Rural 109 (41.0) 17 15.6(8.7-22.5) 1.0 1.0

No of partners <6 months

0-2 223 (81.1) 35 15.7(10.9-20.5) 1.0 1.0

≥3 52 (18.9) 21 40.4(26.6-54.2) 2.6(1.5-4.4) 1.5(0.9-2.8)

Condom use during the last sexual contact*

Yes 61 (22.6) 19 31.1(19.2-43.1) 1.8(1.0-3.2) 1.7(0.9-3.1)

No 209 (77.4) 36 17.2(12.1-22.4) 1.0 1.0

nt, not tested in multivariate model, since p>0.20 in univariate analysis

In bold: significant (p<0.05); due to rounding into 1 decimal 1.0 is not always significant
* Characteristic contains missings
** Adjusted for notified by partner, STI symptoms, urbanisation, number of partners <6 months
and condom use during the last sex contact
PR, prevalence ratio

44
Comparison of the study group and the historical control group
The historical control group consisted of 1530 young heterosexual people, diagnosed
with urogenital chlamydia in 2011, at the STI clinics participating in our study. The
study group was compared with the historical group in age, gender and number of 2
partners in the last 6 months. Gender differed significantly between the groups (39.1%
men in the control group vs 27.5% in the study group, p<0.05), no differences were found
on age and number of partners between the groups. Within a period of 20 months,
547 of the 1530 infected (35.7%) returned for a retest, without receiving a text message
reminder. When including all retests of our study group (not only the retests that met
the definition of a retest in our study), a total of 404 participants out of 828 (48.4%)
returned for a retest within 20 months.
Figure 2 identifies a peak in the retest rate of the study group, within 2 months after
the text message (5.5 months after the initial positive chlamydia test). Retesting in the
study group was concentrated in 5-8 month period, when 253 of 828 (30.6%) participants
returned. This contrasts with 140 of the 1,530 (9.2%) clients in the control group who
returned on their own initiative within the same time frame.

Figure 2. Comparison of the monthly proportions of initial chlamydia positive young clients
who returned for a retest within the study group (2012-2013) and the control group (2011) in
10 participating sexually transmitted infection (STI) clinics in the Netherlands

45
Discussion

In this study, we found that 30.6% of the participants responded to the text message
reminder by requesting a retest within the period of 5-8 months after initial positive
testing. Only 9.2% of the historical control group returned for a retest, on their own
initiative, between 5 and 8 months after initially testing positive.
Among the participants, 20.4% were found to be chlamydia positive after retest,
while the overall chlamydia positivity among all eligible visitors of the STI clinic,
during the study period of 20 months was 15.9%. Participants displaying STI-related
symptoms at retest were more likely to have a chlamydia infection when retested, as
were participants who were notified by a partner.

Strengths and limitations

This is the first study in the Netherlands to use a text message reminder system
to trigger participants to request a retest. One recent Dutch study on retesting was
performed in a more urban setting, and made use of a home-based test or a walk-in
retest drop off to stimulate retesting [10]. However, this is the first multi-centre study
which incorporates the predominant rural areas, and uses a text message reminder
to stimulate retesting.
The reasons for non-participation in the study were not recorded. It cannot be
excluded that some of the chlamydia-positive clients were not offered the chance to
participate in the study, due to time constraints during the STI consultation, direct
treatment before diagnosis or because the client was not a local resident or (small
minority) had no mobile phone. The number of clients participating in the study might
have been higher if there was no time constraint during the consultation or if no direct
treatment was given.
Although we had T0 data for participants who did not return for a retest, we do not
have further details regarding their decision not to return for a retest. This information
may provide valuable insight to explain over-representation or under-representation of
a certain group in the retest population. Also, we do not have data on changed mobile
phone numbers as a reason for not receiving the text message and re-attending. It
may have also been informative to ask additional questions at retest, that is: ‘Has your
steady partner been tested and treated for chlamydia?’ or ‘Have you visited a general
practitioner, in the mean time?’. Questions like these could have clarified reasoning for
participation in retesting and for testing positive again upon retest.
There is evidence that there is a frequent intermittent positive pattern of chlamydia
test results over time after Azithromycin treatment. This positive pattern was more
frequent in anorectal samples. In our study we excluded clients with an (concurrent)
anorectal chlamydia. Follow-up in these studies was performed up to only 8 weeks after

46
treatment, while the current study retested participants after 6 months. Also it remains
unclear whether these intermittent positive patterns of chlamydia after treatment are
a risk for transmission [11,12]. Therefore, treatment failure is unlikely to have played
a major role in the current study. 2

Comparison with other studies

Our results show that a text message, sent at 5.5 and 6 months after the initial
consultation, increases participation in retesting from 9.2% in our historical control
group, to 30.6% in our study group. These findings confirm results of previous studies
[13-15]. However, a study in the UK concluded that sending a text message did not
increase the retest rate after 4 months [16]. This was justified by the fact that there
already was a high retest rate in the control group, who did not receive a text message
(35%, n=92/226), compared with the study group, who did receive a text message (32%,
n=89/274). The retest rate of our historical control group isn’t already high like the UK
study; therefore, we cannot compare our study with the UK study.
The result indicating that young women are more likely to participate in retesting
than men, is also in line with other studies [9,10]. It is worrisome that, at retest, men
were more often reinfected with chlamydia than females, indicating that reinfection
in men may be missed. We, therefore, recommend extra effort to motivate the male
population to participate in retesting.
We do not have a clear explanation for the finding that participants who were not
notified for an STI during the first consultation were more likely to return for a retest,
compared with those who were notified. It may be the case that these participants do
not feel that there is a need for retesting since they were not notified before retest. Also,
persons who were notified at T0 could be more eager to join the study, because they are
worried after being notified. It is imperative to highlight the importance of retesting in
chlamydia-positive young people, even if they are not notified.
At inclusion, participants were informed that, even when they did not engage in
sex between the testing moments, they should still return for a retest after 6 months.
In our study, nine participants reported not having had sex in the last 6 months before
retest, and none of them were reinfected with chlamydia. Though sexual history
may not always be reliable, our study concludes that we must focus our attention on
individuals displaying STI symptoms and/or those notified by a partner. Having STI-
related symptoms and being notified were clear factors associated with reinfection in
the current study. This finding concurs with other studies [3,5,10,17,18].
In our study group, 22 participants reported to having STI-related symptoms. A
majority of these participants (n=13) returned before receiving a text message (data not
shown), probably as a result of the symptoms. The other nine participants responded to
the text message and did not attend for a retest on their own initiative. This shows that

47
despite own initiative retesting, text reminders are necessary and can improve retest
rates. Therefore, young people who previously tested positive for chlamydia infection
should receive specific instructions that they are at risk for reinfection and should
reattend for testing, particularly if they notice symptoms.

Interpretation
Despite the limitations, this study and other studies conclude that young people
with chlamydia are at risk for reinfection and that it is important to retest them and
preferably remind them of the retest [3,5,10,17,18]. This study has been performed
within a standard care environment, complying with the criteria for access to free STI
care at STI clinics in the Netherlands, simplifying potential future implementation. If
we were to implement sending a text message as a reminder of a retest as a standardised
method of triggering chlamydia-positive young people, this would require little time
investment and direct treatment at first consultation would not be an issue.
Higher retest participation can also be accomplished by other means; a recent
Dutch study showed that by offering a home-based test or a retest at the STI clinic
without making an appointment, recipients were more likely to respond to a retest offer
(46% and 23% respectively) [10]. However, the costs and efforts required for home-based
testing are higher than simply sending a text message and the retest rate for the group
that could retest without making an appointment is lower than in the current study.
The way the clients prefer to be reminded of a retest may vary and depends on
the resources of the STI clinic if it is possible to offer different methods of reminders.
While sending reminders is an important method for increasing retest attendance
and subsequently track and treat clients with a chlamydia reinfection, it is at least
as important to put a lot of effort into motivating clients to use a condom to prevent
reinfection. Sexual health education and motivational interviewing during first
consultation can be effective methods in achieving future condom use [19,20].

48
Conclusions

Reinfections of previously chlamydia-positive young people are common; therefore,

retesting is recommended. Despite the fact that these young people retest on their own 2
initiative, this study shows that sending text message reminders can improve retest
rates. The text message reminders should especially be targeted at those at highest risk
for reinfection; individuals experiencing STI-related symptoms and/or individuals who
are notified for an STI by a partner. When we retest individuals at risk for reinfection
timely, it may substantially reduce further spreading of chlamydia due to early case
finding. Sending a text message is a small effort and feasible manner to remind people
of taking a retest rather than relying on people’s own initiative to retest.

Acknowledgments

We would like to thank Joyce de Goede, epidemiologist of GGD Hart van Brabant, for
giving the study a kick-start and drafting the research proposal. We would also like to
thank the research group “SOROZ”, especially Hanna Bos, who helped setting up the
research and solving practical problems. Our thanks go out to all the medical staff of
the 10 participating STI clinics for their efforts in motivating all potential participants.
Last we would like to thank Linda Howson for revising this article, adjusting the English
language.

49
References

1. Van den Broek IVF, Verheij RA, Van Dijk CE, et al. Trends in sexually transmitted infections in
the Netherlands, combining surveillance data from general practices and sexually transmitted
infection centers. BMC Family Practice 2010;11:39
2. Soetens LC, Koedijk FDH, Vriend HJ, et al. Sexually transmitted diseases, including HIV, in
the Netherlands in 2012. Infectieziekten Bulletin 2013;24:291-3
3. Lamontagne DS, Baster K, Emmett L, et al. Incidence and reinfection rates of genital
chlamydial infection among woman aged 16-24 years attending general practice, family
planning and genitourinary medicine clinics in England: a prospective cohort study by the
chlamydia Recall Advisory Group. Sex Transm Infect 2007;83:292-303
4. Walker J, Tabrizi SN, Fairley CK, et al. Chlamydia trachomatis incidence and reinfection
among young woman – behavioural and microbiological characteristics. PlosOne 2012;7:1-9
5. Woodhall SC, Atkins JL, Soldan K, et al. Repeat genital chlamydia trachomatis testing rates
in young adults in England, 2010. Sex Transm Infect 2013;89:51-56
6. Haggerty CL, Gottlieb SL, Taylor BT, et al. Risk of sequelae after chlamydia trachomatis genital
infection in woman. J Infect Dis 2010;201:s134-S155
7. Heijne JC, Herzog SA, Althaus CL. Insights into the timing of repeated testing after treatment
for chlamydia trachomatis: data and modelling study. Sex Transm Infect 2013;89:57-62
8. De Vries HJC, Van Doornum GJJ, Bax CJ, et al. Multidisciplinary protocol on sexually
transmitted diseases for second line care 2012
9. Dukers-Muijrers NH, Van Liere GA, Hoebe CJ. Re-screening chlamydia trachomatis positive
subjects; a comparison of practices between an STI clinic, general practitioners and
gynaecologists. Sex Transm Infect 2013;89:25-27
10. Gotz HM, Wolfers MEG, Luijendijk A, et al. Retesting for genital chlamydia trachomatis among
visitors of a sexually transmitted infections clinic: randomized intervention trial of home-
versus clinic-based recall. BMC Infectious Diseases 2013;13:239
11. Dukers-Muijrers NH, Morré SA, Speksnijder A, et al. Chlamydia trachomatis test-of-cure
cannot be based on a single highly sensitive laboratory test taken at least 3 weeks after
treatment. PLoS One 2012;7:e34108.
12. Dukers-Muijrers NH, Speksnijder AG, Morré SA, et al. Detection of anorectal and cervicovaginal
Chlamydia trachomatis infections following azithromycin treatment: prospective cohort
study with multiple time-sequential measures of rRNA, DNA, quantitative load and symptoms.
PLoS One 2013; 20;8:e81236.
13. Bourne C, Knight V, Guy R, et al. Short message service reminder intervention doubles
sexually transmitted infection? HIV re-testing rates among men who have sex with men. Sex
Transm Infect 2011;87:229-231
14. Guy R, Wand H, Knight V, et al. SMS reminders improve re-screening in woman and
heterosexual men with chlamydia infection at Sydney sexual health centre: a before-and-
after study. Sex Transm Infect 2013;89:11-15
15. Downing, SG1, Cashman, C, McNamee H, et al. Increasing chlamydia test of re-infection rates
using SMS reminders and incentives. Sex Transm Infect 2013;80:16-9
16. Burton J, Brook G, McSorley J, Murphy S. The utility of short message service (SMS) texts to
remind patients at higher risk of STIs and HIV to reattend for testing: a controlled before and
after study. Sex Transm Infect 2014;90:11-3

50
17. Gaydos CA, Wright C, Wood BJ, et al. chlamydia trachomatis reinfection rates among female
adolescents seeking rescreening in school based health centres. Sex Transm Dis 2008;35:233-7
18. Evans C, Das C, Kinghorn G. A retrospective study of recurrent chlamydia infection in men
and women; is there a role for targeted screening for those at risk? Int J STD AIDS 2009;20:188-
92
19. Kuyper L, de Wit J, Heijman T, et al. Influencing risk behavior of sexually transmitted infection
clinic visitors: efficacy of a new methodology of motivational preventive counseling. AIDS
patient care STDS 2009;23:423-31
20. Eaton LA, Huedo-Medina TB, Kalichman SC, et al. Meta-analysis of single session behavioural
interventions to prevent sexually transmitted infections: implications for bundling prevention
packages. Am J Public Health 2012;102:e34-44
Chapter 3
Determinants of frequent and infrequent
STI testing and STI diagnosis related to test
frequency among men who have sex with men
in the Eastern part of the Netherlands:
a 6-year retrospective study

Carolina (Karlijn) J.G. Kampman

Janneke C.M. Heijne
Petronella (Nelleke) H.M. Kistemaker-Koedijk
Femke D.H. Koedijk
Maartje Visser
Jeannine L.A. Hautvast

Published as a research article in BMJ Open, 2018 May 31;8(5):e020495.

Abstract

Objectives
Men who have sex with men (MSM) remain vulnerable to sexually transmitted
infections (STIs) and are advised to be tested at least twice a year. The aim of this
study was to assess the determinants of test frequency and their associations with an
STI diagnosis.

Design
A 6-year retrospective study.

Setting
5 STI clinics in the Eastern part of the Netherlands.

Participants
MSM whose mean test interval was 6 months or more were grouped as “infrequently
tested” (n=953), and those with mean test intervals less than 6 months were grouped
as “frequently tested” (n=658).

Primary and secondary outcome measures

Test frequency and STI diagnosis and determinants.

Results
MSM who were ever diagnosed with an STI (OR=1.4, 95% CI 1.1 to 1.7), MSM who had
never had STI symptoms (OR=0.8, 95% CI 0.6 to 1.0), and MSM who had ever had sex
with both men and women (OR=0.6, 95% CI 0.5 to 0.8) were more often frequently tested.
Moreover, in both groups, MSM who had ever been notified by a partner (OR=2.2, 95% CI
1.7 to 2.9 infrequently tested; OR=2.0, 95% CI 1.4 to 2.9 frequently tested), MSM who had
ever had STI symptoms (OR=1.6, 95% CI 1.2 to 2.1 infrequently tested; OR=1.8, 95% CI 1.3
to 2.6 frequently tested) and MSM who were ever diagnosed with HIV (OR=2.7, 95% CI
1.5 to 4.6 infrequently tested; OR=6.8, 95% CI 2.6 to 17.5 frequently tested) were more
likely to be diagnosed with an STI.

Conclusions
Among MSM visiting STI clinics, those who were ever diagnosed with HIV were more
often diagnosed with an STI, but did not visit STI clinics more frequently than HIV-
negative MSM. This highlights the necessity of encouraging MSM who are diagnosed
with HIV to have STI tests more frequently.
Introduction

Men who have sex with men (MSM) contribute to the worldwide burden of sexually
transmitted infections (STIs), including HIV [1-3]. Some studies have found that MSM
reported large proportions of diagnoses of HIV (42%), gonorrhoea (43%) and syphilis
(58%) [4,5]. In the Netherlands, MSM accounted for the greatest contribution to STI 3
diagnoses in 2016 at STI clinics; 21% of the tests were positive for one or more STIs [6].
Early detection and treatment are crucial to reduce the risk of STI transmissions
(including HIV) among MSM [7]. Therefore, test frequency is important in reducing
STI transmissions. In Australia, MSM are advised to get a test at least once a year, but
one study reports that this advice is poorly adhered to: the retesting rate at 1 year was
35% [8]. A British study estimates that 55% of the MSM were tested once a year, where
guidelines also recommend HIV tests once a year (and more often for those at ‘higher
risk’) [9].
There were only informal guidelines for test frequency among MSM in the
Netherlands before 2017, based on expert opinion. These informal guidelines
recommended STI testing for MSM at least twice a year. A formal guideline, based
on Dutch epidemiological findings, has now (2017) been drafted, and it advises MSM
to be tested at least twice a year, and high-risk MSM (e.g., MSM who were diagnosed
with HIV or MSM who are commercial sex workers) four times a year. However, the
annual testing uptake among MSM in the Netherlands is low. One Dutch study on STI
consultations in Amsterdam from 2009 to 2013 reports that 35% of the HIV-negative
MSM returned to the STI clinic within 1 year after their initial consultation [10]. Another
Dutch study based on national STI clinic data from 2014 to 2015 reports that 48% of the
MSM were tested more than once during a 1.5-year follow-up. Only 19% of the MSM
were tested consistently every 6 months [11].
No studies have yet simultaneously investigated the relation between MSM test
frequency and STI diagnosis, with the determinants, in the Netherlands. The aim of
this study was to assess the determinants of test frequency and of STI diagnosis among
MSM visiting STI clinics in the eastern part of the Netherlands. The results of the study
could provide more insight into the frequency and relevance of testing according to
the guidelines for certain MSM risk groups.

55
Methods

Study setting and study design

In the Netherlands, general practitioners and STI clinics based in regional public health
services (RPHSs) provide primary STI care. The STI clinics are freely accessible and
government-funded; they aim to reach high-risk groups who might otherwise not seek
timely STI care. The STI clinic at the RPHS is always accessible to MSM, whether or
not reporting STI-related symptoms, while there is a triage system for heterosexuals.
Furthermore, MSM are always tested for five STIs: chlamydia, gonorrhoea, syphilis,
HIV (unless clients opt out) and hepatitis B (when not successfully vaccinated against
hepatitis B) [6].
We performed a 6-year retrospective study (2008–2013) using data from 5 of the
25 Dutch STI clinics. The participating clinics were in the east of the Netherlands,
which is a semirural area. All of them used an online patient registration system in
which sexual preference was a mandatory question. Data from 2013 onwards were
not included due to changes in the patient registration system of the STI clinics. The
definitions of database variables could not be matched.

Study population
We selected all men who reported having sex with men or sex with both women
and men, and men who identified themselves as homosexual or bisexual (hereafter
referred to as MSM). Only MSM who had three or more consultations were included
in the study because three or more consultations were considered to approximate an
actual test frequency. We selected MSM who had a minimum of 18 months of follow-up
after the first consultation (which took place before June 2012, with a follow-up time
extending into 2013) because all MSM had to have sufficient time to return for two
retests. Furthermore, consultations within 35 days of a previous visit were excluded to
ensure that no possible test-of-cure consultations were included.

Data description
For each consultation, the following variables were used: age (<26 years and ≥26 years—
clients younger than 26 years are considered ‘young’ as decided by the national STI clinic
regulations); ethnicity (due to a change in registration, ethnicity was a combination of
variables that consisted of self-defined ethnicity (from 2006 until 2010) and ethnicity
based on (parental) country of birth (from 2011 until 2013); MSM were subsequently
categorised into Dutch, other Western and non-Western); having been notified by a
partner; having STI symptoms; socioeconomic status (SES, based on postal codes (four
digits))—this measure of SES was deduced by postal code-associated data from the
Netherlands Institute for Social Research and is a measure composed of four variables:

56
average income per household, percentage of households with low income, percentage
of residents without a paid job and percentage of households with an average to low
education; number of sexual partners in the last 6 months; being diagnosed with an
STI during the study period; and sexual preference (reported as having sex with men
or sex with men and women). HIV status was considered a separate variable based on
existing literature that indicates that MSM who are diagnosed with HIV are more likely 3
to be diagnosed with an STI [12-15]. MSM were defined as diagnosed with HIV when
they were diagnosed with HIV during the study period or were already diagnosed with
HIV before the study period.

Data analysis
The determinants age, ethnicity and SES were taken from the first consultation in
all analyses because these determinants are reasonably stable over time. The mean
number of partners reported per consultation was used to determine the number
of partners in the analysis. All other determinants were assessed on the basis of the
occurrence of the event within all individual consultations, which resulted in an ‘ever’
and ‘never’ occurring categorisation.
The outcome test frequency was defined as follows: MSM were defined infrequently
tested if their mean test intervals were 6 months or more. They were defined as
frequently tested if their mean test intervals were less than 6 months. A 1-month margin
was taken into account to ensure that a person would not be regarded as infrequently
tested if the mean test interval was only slightly more than 6 months.
The outcome STI diagnosis was defined as follows: any one of the MSM was defined
as being diagnosed with one or more STIs, including chlamydia, gonorrhoea, syphilis
and/or infectious hepatitis B, in one or more body locations (oral, genital or anal) at
one or more consultations during the study period.
If more than 5% of the values were missing for a variable, these missing values
were included in the analysis in a separate category to reduce loss of data. We
performed logistic regression analyses to identify determinants of testing frequency
and STI diagnosis. Collinearity between variables was checked beforehand. We
used the Enter method with multivariable logistic regression to further analyse
determinants with a p value less than 0.20 in univariable analyses. The multivariable
logistic regression was corrected for the number of consultations because the
reporting of an event (e.g., ever having STI symptoms) is more likely when MSM visit
the STI clinic more often. In all analyses, determinants with p<0.05 were considered
statistically significant. We present ORs and 95% CIs to show the associations
between the determinants and the outcomes in tables 1 and 2. We used IBM SPSS
V.22 software for the analyses.

57
Patient and public involvement
The study used routinely collected anonymous surveillance data. Hence, STI clinic
visitors were not directly involved in the development or execution of this study, and
neither could the results be disseminated to them.

58
Results

Study population and test frequency

A total of 5954 MSM visited one of the five participating STI clinics between 2008 and 2013.
A total of 1913 MSM had three or more consultations, of whom 1611 also had a minimal
follow-up time of 18 months after the first consultation and thus were included. The 3
group ‘infrequently tested’ consisted of 953 MSM (59.2%), and the group ‘frequently tested’
consisted of 658 MSM (40.8%).
Table 1 shows that among the infrequently tested MSM, 47.0% were ever diagnosed
with an STI, compared with 64.6% of the frequently tested MSM. Table 1 also compares the
characteristics of the two groups. Multivariable analysis showed that the frequently tested
had more often been diagnosed with an STI (OR 1.4, 95% CI 1.1 to 1.7), were less likely to
ever have reported STI-related symptoms (OR 0.8, 95% CI 0.6 to 1.0) and had less often ever
had sex with men only (OR 0.6, 95% CI 0.5 to 0.8) than the infrequently tested.

Table 1. Characteristics of the frequently and infrequently tested groups and the determinants
of the test frequency for MSM who visited an STI clinic in the east of the Netherlands, 2008–2013
Frequently versus
infrequently tested
Infrequently Frequently Univariable Multivariable
tested (n=953) tested (n=658) analyses analysis
n (%) n (%) OR (95% CI) OR (95% CI)
Median number of consultations
(IQR) 4; 3 to 5 6; 4 to 9
Age (in years at baseline)
<26 242 (25.4) 140 (21.3) ref ref
≥26 711 (74.6) 518 (78.7) 1.3 (1.0–1.6) 0.9 (0.7–1.2)
Ethnicity (baseline)
Dutch 857 (89.9) 584 (88.8) ref nt
Non-western 62 (6.5) 47 (7.1) 1.1 (0.8–1.6)
Other western 34 (3.6) 27 (4.1) 1.2 (0.7–2.0)
Socio-economic status (baseline)
Low 281 (29.5) 183 (27.8) 1.0 (0.7–1.2) nt
Intermediate 349 (36.6) 256 (38.9) 1.1 (0.9–1.4)
High 300 (31.5) 203 (30.9) ref
Missing 23 (2.4) 16 (2.4)

59
Table 1. Continued
Frequently versus
infrequently tested
Infrequently Frequently Univariable Multivariable
tested (n=953) tested (n=658) analyses analysis
n (%) n (%) OR (95% CI) OR (95% CI)
Mean number of partners
<2 122 (12.9) 67 (10.3) ref ref
2 to 5 406 (43.0) 227 (35.0) 1.0 (0.7–1.4) 1.0 (0.7–1.5)
≥5 416 (44.1) 354 (54.6) 1.6 (1.1–2.2) 1.2 (0.8–1.8)
Missing 9 (0.0) 10 (0.0)
Notified by a partner
Never 511 (53.6) 267 (40.6) ref ref
Ever 442 (46.4) 391 (59.4) 1.7 (1.4–2.1) 1.1 (0.9–1.4)
Diagnosed with an STI
Never 505 (53.0) 233 (35.4) ref ref
Ever 448 (47.0) 425 (64.6) 2.1 (1.7–2.6) 1.4 (1.1–1.7)
STI-related symptoms
Never 454 (47.6) 273 (41.5) ref ref
Ever 499 (52.4) 385 (58.5) 1.3 (1.1–1.6) 0.8 (0.6–1.0)
Sexual preference
Sex with men and
women 232 (24.3) 212 (32.2) ref ref
Sex with men only 714 (74.9) 442 (67.2) 0.7 (0.5–0.8) 0.6 (0.5–0.8)
Unknown 7 (0.7) 4 (0.6)
Diagnosed with HIV
Never 860 (90.2) 568 (86.3) ref ref
Ever 93 (9.8) 90 (13.7) 1.5 (1.1–2.0) 0.8 (0.5-1.2)
IQR, interquartile range
Ref, reference
nt, not tested in multivariable model, since p>0.20 in univariate analysis
In bold: significant (p<0.05); due to rounding into 1 decimal 1.0 is not always significant.
Regression analysis corrected for number of consultations

60
STI diagnosis
Table 2 shows the determinants of having an STI diagnosis. The same determinants
of STI diagnosis were identified in both groups: MSM who had ever been notified
by a partner, MSM who had ever had STI-related symptoms and MSM who were
ever diagnosed with HIV were more likely to have an STI diagnosis. In addition,
frequently tested MSM who only had sex with men were more likely to have an STI 3
diagnosis, which was not seen among infrequently tested MSM.

Table 2. Determinants of STI diagnosis in infrequently and frequently tested MSM who visited
an STI clinic in the east of the Netherlands, 2008–2013
Infrequently tested Frequently tested
Univariable Multivariable Univariable Multivariable
regression analysis regression analysis
analysis OR (95% CI)* analysis OR (95% CI)
OR (95%CI) OR (95% CI)
Age (in years at baseline)
<26 ref nt ref nt
≥26 0.8 (0.6–1.1) 0.9 (0.6–1.4)
Ethnicity (baseline)
Dutch ref nt ref nt
Non-western 1.4 (0.8–2.3) 1.0 (0.5–1.9)
Other western 0.8 (0.4–1.7) 1.4 (0.6–3.2)
SES (baseline)
Low 1.3 (0.9–1.7) nt 1.1 (0.7–1.6) nt
Intermediate 1.2 (0.9–1.6) 0.8 (0.6–1.2)
High ref ref
Mean number of partners
<2 ref ref ref ref
2–5 1.0 (0.7–1.6) 0.9 (0.6–1.4) 0.8 (0.5–1.4) 0.9 (0.5–1.7)
≥5 1.6 (1.1–2.4) 1.3 (0.8–2.0) 1.2 (0.7–2.1) 1.3 (0.7–2.4)
Notified by a partner
Never ref ref ref ref
Ever 2.6 (2.0–3.4) 2.2 (1.7–2.9) 2.6 (1.9–3.6) 2.0 (1.4–2.9)
STI-related symptoms
Never ref ref ref ref
Ever 2.0 (1.6–2.7) 1.6 (1.2–2.1) 2.6 (1.9–3.6) 1.8 (1.3–2.6)
Sexual preference
Sex with men and
women ref ref ref ref
Sex with men 1.5 (1.1–2.0) 1.3 (1.0–1.8) 2.0 (1.4–2.8) 1.8 (1.2–2.6)

61
Table 2. Continued
Infrequently tested Frequently tested
Univariable Multivariable Univariable Multivariable
regression analysis regression analysis
analysis OR (95% CI)* analysis OR (95% CI)
OR (95%CI) OR (95% CI)
Diagnosed with HIV
Never ref ref ref ref
Ever 4.7 (2.8–7.7) 2.7 (1.5–4.6) 8.1 (3.7–17.9) 6.8 (2.6–17.5)
nt, not tested in multivariate model, since p>0.20 in univariate analysis
Ref, reference
SES, socio-economic status
STI, sexually transmitted infection
In bold: significant (p<0.05); due to rounding into 1 decimal 1.0 is not always significant.
Regression analysis corrected for number of consultations

62
Discussion

In this study, we found that 59.2% of the included MSM were infrequently tested
(mean test interval ≥6 months) and 40.8% were frequently tested (mean test interval
<6 months). MSM who were ever diagnosed with an STI, MSM who had never had STI
symptoms, and MSM who had ever had sex with men as well as women were more 3
often frequently tested. Moreover, we found that the determinants for STI diagnosis
were the same in both groups. MSM who had ever been notified by a partner, MSM
who had ever had STI symptoms and MSM who were ever diagnosed with HIV were
more likely to be diagnosed with an STI.
This is the first study in the Netherlands that addresses both test frequency and
STI diagnosis among MSM who were and were not diagnosed with HIV. Furthermore,
our study has a long follow-up of 5 years, so a large number of MSM were included
in analyses. However, the study has several limitations. First, it took place in the
eastern part of the Netherlands, which is a semirural area. The study population
and their test behaviour may differ from the rest of the Netherlands. Second, STI
diagnosis was only available for those who came back for repeat testing; they do
not represent the reinfections contracted by all MSM who visit STI clinics. Third,
in this study, only STI clinic consultations were available, so data from STI tests
carried out by general practitioners or other specialists could not be taken into
account. The number of STI consultations per individual might therefore be an
underestimation, and MSM could have been categorised differently if consultations
from other caregivers have been included. Fourth, due to changes in the patient
registration system, we could not include data beyond the year 2013. The STI clinic
has, however, always been freely accessible to MSM over the years. We do not think
there have been any sudden changes in risk behaviour and/or test frequency among
MSM; therefore, we think the data of the current study are still of importance to STI
care nowadays. Fifth, we excluded MSM with only one consultation. We reasoned
that leaving them out would provide us with a more valid overview of test frequency
in those who appear to be a regular client of STI clinics.
With the study methods we chose, this study shows that, of all the MSM with
at least three consultations, 41% were frequently tested and they had a mean test
interval of less than 6 months. The methods of the current study differ widely
from other comparable Dutch studies so comparison is difficult [10,11]. Vriend
and colleagues ’10 study found that 16% of HIV-negative MSM returned for repeat
tests within 6 months. We only included MSM with at least two subsequent tests
and a minimum of 18 months of follow-up, whereas Vriend and colleagues also
included MSM only tested once in their analyses, which made the comparison of
the proportions of the frequently tested group in their study and our study difficult

63
[10]. However, Vriend and colleagues also looked at a consistent 12-month testing
among people with at least 3 years of follow-up (i.e., three or more tests) and found
an uptake of 36%, which is more in line with our study.
Our results show that MSM who had ever been diagnosed with an STI are more
often frequently tested. However, MSM who had ever been notified by a partner and
MSM who had ever had STI-related symptoms are not more likely to be frequently
tested. This is in line with another study which finds that MSM who have been
notified by a partner or who have reported STI symptoms return to the STI clinic
sooner, but are not more likely to be consistently tested every 6 months [11].
Furthermore, our study shows that MSM who had ever had sex with men as well
as women were more often frequently tested. In two other Dutch studies, men who
had sex with both genders less often had repeat tests [10,11]. We do not have a clear
explanation for this discrepancy, but a reporting bias in sexual preference could be
a possible explanation. Further research is needed to gain more insight into this.
Regarding STI diagnosis, we show that MSM who had ever been notified by a
partner, MSM who had ever had STI symptoms and MSM who were ever diagnosed
with HIV were more likely to have an STI diagnosis. These results are in line
with other studies [12-16]. A British analysis using multiple sources of national
surveillance data and population survey data concludes that an increasing
proportion of STIs are being diagnosed in MSM who are diagnosed with HIV, with
the population rate of STIs rising to four times that of HIV-negative or undiagnosed
MSM. Moreover, STI reinfection rates were considerably higher in MSM who were
diagnosed with HIV over a 5-year follow-up period. The authors believe the higher
number of bacterial reinfections in MSM who are diagnosed with HIV are indicative
of rapid transmission in dense sexual networks [17]. An Italian study assessed risk
behaviours before and after being diagnosed with HIV; MSM who are diagnosed
with HIV continue to engage in at-risk practices: a quarter of them did not use
condom during STI episodes, 12.5% of the participants had engaged in sex for
money and 8.4% had paid for sex [18]. Also, serosorting (selecting sex partners of
the same HIV status) or assumed serosorting among MSM who are diagnosed with
HIV may play a role in at-risk practices. Among MSM who are diagnosed with HIV,
the likelihood of unprotected anal intercourse (UAI) is higher when a partner’s
status was known. Furthermore, assumed seroconcordant UAI is associated with
increased STI prevalence [19-21].
By combining the results of the significant determinants of frequent testing and
STI diagnosis, this study demonstrates that MSM who had ever been notified by a
partner and MSM who had ever had STI-related symptoms were more likely to have
an STI diagnosis, but were not more likely to be frequently tested. This means that
MSM who had symptoms or who had been notified by a partner appear to find their

64
way to the STI clinics when necessary, but will not come back frequently. There is
no legislation on partner notification in the Netherlands. Also, partner notification
is performed anonymously; the STI clinic does not know to the full extent who is
being notified.
We also found that MSM who were ever diagnosed with HIV were more often
diagnosed with an STI, but did not visit the STI clinic more frequently than MSM who 3
tested HIV-negative. Other studies also show that MSM who are diagnosed with HIV
are more likely have an STI diagnosis [12-15]. Routine screening for STI of MSM who
were diagnosed with HIV is important because regular screening could help reduce the
incidence of STI diagnoses [22-24]. MSM diagnosed with HIV are not routinely tested
for STI in most HIV care centres, except for annual syphilis and hepatitis C screening.
Dutch STI clinics put great efforts in motivating MSM to test for STIs by outreach
activities at MSM events and providing anonymous online test facilities. This study
highlights the importance of ongoing efforts done by STI clinics in encouraging MSM
who were diagnosed with HIV to be tested for STI frequently.

Acknowledgments

The authors thank all the medical staff of the five participating STI clinics for allowing
us to use their data. We would also like to thank Birgit van Benthem and Koos van der
Velden for their constructive comments on the manuscript.

65
References

1. Sullivan PS, Hamouda O, Delpech V, et al. Re-emergence of the HIV epidemic among men
who have sex with men in North America, Western Europe and Australia, 1996-2005. An of
Epid 2009;19:423
2. European Centre for Disease prevention and Control. STI and HIV prevention in men who
have sex with men in Europe. Stockholm:ECDC;2013
3. Cohen J, Lo YR, Caceres CF, et al. WHO guidelines for HIV/STI prevention and care among MSM
and transgender people: implications for policy and practice. Sex Transm Infect 2013;89:536
4. European Centre for Disease prevention and Control. Surveillance report HIV/AIDS
surveillance in Europe 2013. Stockholm:ECDC;2014
5. European Centre for Disease prevention and Control. Surveillance report Sexually transmitted
infections in Europe 2013. Stockholm:ECDC;2015
6. Visser M, van Aar F, van Oeffelen AAM. Sexually transmitted infections including HIV, in the
Netherlands in 2016. RIVM 2017
7. Center for Disease Control and Prevention. Sexually transmitted diseases treatment advises.
MMWR 2010;59
8. Guy R, Goller JL, Spelman T, et al. Does the frequency of HIV and STI testing among MSM in
primary care adhere with Australian guidelines? STI 2010;86:371
9. McDaid LM, Aghaizu A, Frankis J, et al. Frequency of HIV testing among gay and bisexual
men in the UK: implications for HIV prevention. HIV med 2016;17:683
10. Vriend HJ, Stolte IG, Heijne JC, et al. Repeated STI and HIV testing among HIV-negative men
who have sex with men attending a large STI clinic in Amsterdam: a longitudinal study. Sex
Transm Infect 2015;91:294
11. Visser M, Heijne JC, Hogewoning AA, et al. Frequency and determinants of consistent STI/HIV
testing among men who have sex with men testing at STI outpatient clinics in the Netherlands:
a longitudinal study. Sex Transm Infect 2017;Epub ahead of print
12. Op de Coul ELM, Warning TD, Koedijk FDH. Sexual behaviour and sexually transmitted
infections in sexually transmitted infection clinic attendees in the Netherlands, 2007-2011.
Int J STD&AIDS 2014;25:40
13. Koedijk FDH, Benthem BHB, Vroling EMCD, et al. Increasing sexually transmitted infection
rates in you men having sex with men in the Netherlands, 2006-2012. Em Themes Epidemiology
2014;11:12
14. Schmidt AJ, Hickson F, Weatherburn P, et al. Comparison of the performance of STI screening
services for gay and bisexual men across 40 European cities: results from the European MSM
internet Survey. Sex Transm Infect 2013;80:575
15. Mirandola M, Gios L, Davis J, et al. Socio-demographic factors predicting HIV test seeking
behaviour among MSM in 6 EU cities. Eur J Public Health 2016;epub ahead of print
16. Wilkinson A, El-Hayek C, Fairley CK, et al. Incidence and risk factors associated with
chlamydia in men who have sex with men: a cohort analysis of Victorian Primary Care
Network for Sentinel Surveillance data. Sex Transm Infect 2012;88:319-324
17. Malek R, Mitchell H, Furegato M, et al. Contribution of transmission in HIV-positive men who
have sex with men to evolving epidemics of sexually transmitted infections in England: an
analysis using multiple data sources, 2009-2013. Euro Surveill 2015;16:20

66
18. Camoni L, Dal Conte I, Regine V, et al. Sexual behaviour reported by a sample of Italian MSM
before and after HIV diagnosis. Ann Ist Super Sanita 2011;47:214-9
19. Matser A, Heijman T, Geskus R, et al. Perceived HIV status is a key determinant of unprotected
anal intercourse within partnerships of men who have sex with men in Amsterdam. AIDS
Behav 2014 Dec;18:2442-56
20. Hotton AL, Gratzer B, Mehta SD. Association between serosorting and bacterial sexually
transmitted infection among HIV-negative men who have sex with men at an urban lesbian,
gay, bisexual, and transgender health center. Sex Transm Dis 2012;39:959-64
21. Zablotska IB, Imrie J, Prestage G, et al. Gay men’s current practice of HIV seroconcordant
unprotected anal intercourse: serosorting or seroguessing? AIDS Care 2009;21:501-10
22. Dougan S, Evans BG, Elford J. Sexually transmitted infections in Western Europe among HIV
positive men who have sex with men. Sex Transm Dis 2007;34:783
23. Xirodou M, Vriend HJ, Lugner AK, et al. Modelling the impact of chlamydia screening on the
transmission of HIV among men who have sex with men. BMC Infect Dis 2013;13:436
24. Vriend HJ, Lugner AK, Xiridou M, et al. Sexually transmitted infections screening at HIV
treatment centers for MSM can be cost-effective. AIDS 2013;27:2281-90
Chapter 4
Consultation rate and chlamydia
positivity among ethnic minority clients
at STI clinics in the Netherlands

Saskia B. Ostendorf
Carolina (Karlijn) J.G. Kampman
Christian J.P.A. Hoebe
J. (Koos) van der Velden
Jeannine L.A. Hautvast
Cornelia (Ellen) H.M. van Jaarsveld

Published as a research article in PLoS One, 2021 Feb 19;16(2):e0247130

Abstract

Objectives
Although ethnic minority clients (EMs) from STI endemic countries have a higher risk
for STI, little is known about their STI clinic consultation rate proportionality. The aim
of this study was to assess consultation and chlamydia positivity rates among different
EMs visiting STI clinics in the Netherlands.

Methods
We calculated consultation rates in EM groups by dividing the number of STI
consultations by the total number of inhabitants in the region belonging to an EM,
then compared the EM rates to native Dutch rates. Factors associated with chlamydia
positivity were analysed using multivariate regression analysis.

Results
A total of 23,841 clients visiting an eastern Netherlands STI clinic between 2011 and 2013
were included in the analysis, of which 7% were EMs. The consultation rate of native
Dutch clients was 22.5 per 1000, compared to 8.5 per 1000 among EMs. Consultation
rates in all EMs were lower than in Dutch clients, except for Antillean or Aruban EMs
and Latin American EMs.
The chlamydia positivity rate among all clients was 15.5%, and Antillean or Aruban
ethnicity (27.1%) EMs had the highest rates. Multivariate analysis identified the
following factors associated with chlamydia positivity: Eastern or Northern European
EM, African EM, Antillean or Aruban EM, STI related symptoms, heterosexual
preference, partner in a risk group, receiving a partner notification, and having had
three or more partners in the past six months.

Conclusion
On a population level, most EMs visit STI clinics less often than native Dutch clients,
but they have a higher rate of positive chlamydia diagnoses. STI clinics should increase
outreach activities for EM clients because they are insufficiently reached by current
practices, but contribute substantially to chlamydia incidence rates.
Introduction

Countries or continents endemic for sexually transmitted infections (STI) and HIV
include Turkey, North Africa and Morocco, Suriname, Netherlands Antilles and Aruba,
Eastern Europe, Sub-Saharan Africa, Latin America and Asia [1]. In Western countries,
STIs are usually more prevalent in people originating from these countries or continents
(e.g., ethnic minorities, EMs) than in the rest of the population [2]. For example, the
United Kingdom EMs have been over-represented in STI statistics for more than a
decade [3–5]. One British study found a significant association between ethnic origin
4
and reported STIs in the previous five years, with increased risk in sexually active black
Caribbean and African men compared with white men, and black Caribbean women
compared with white women [4]. Another British study of the general population found
that STI diagnoses were higher in black Caribbean men (8%) and mixed ethnicity women
(7%) than white British participants (4% in men and 3% in women) [6]. A Dutch study
found that 12% of Dutch clients visiting an STI clinic were STI positive, with EM clients
showing higher positivity rates, ranging from a relative risk of 1.14 in Asian minorities
to 1.81 in Antillean/Aruban minorities compared to native Dutch [7]. Another Dutch
study reported that EM STI positivity was highest among Latin American and Eastern
Europe men who have sex with men, and heterosexual men from the Netherlands
Antilles/Aruba (all 25% STI positivity, compared to 20% STI positivity among native
Dutch who visited an STI clinic) [1].
Some studies assessed EM clients’ number of STI clinic consultations to identify
the relative proportion of EM groups attending STI clinics for testing. A British study
showed increasing numbers of clients from Central and East Europe attending STI
clinics following the European Union expansion [8]. Another British study reported that
South Asians, especially women, were reluctant to seek STI clinic care [9]. In 2017, 68%
of the STI clinic attendees in the Netherlands were of Dutch origin. Most EM STI clinic
consultations involved clients from Asia (5%; 7,667/150,593), followed by Surinamese
(5%; 7,536/150,593) and Netherlands Antilles/Aruba clients (3%; 4,087/150,593) [1].
Although these studies assessed the number of consultations for different EMs, most
did not assess the proportional representation of EM populations at STI clinics. One
Dutch study reported proportionally higher consultation rates among some EMs
(Eastern Europeans, Sub-Sahara Africans, Surinamese, Netherlands Antilles/Arubans
and Latin Americans) and lower rates among others (Turkey, North Africa, Asia, and
Western countries). However, this study did not exclude multiple consultations by the
same individual, resulting in a potential overestimation of EMs’ STI clinic consultations
[7]. To inform STI clinic policy, better insight regarding representation of EM clients
at STI clinics is needed. Therefore, the current study aimed to assess to what extent
the STI clinics in the eastern part of the Netherlands reach EM clients by comparing

71
the total number of STI clinic attendees (including first consultations only, per person
per year), to the total number of EM inhabitants. Furthermore, chlamydia positivity
was compared between EM clients and clients with a Dutch origin, controlling for
behavioural and STI risk factors. The study findings can be used to develop methods
for assessing proportionality of EM STI clinic consultation rates compared to a native
population group. Furthermore, the findings regarding EM group representation
combined with knowledge of chlamydia positivity rates, can be used to help STI clinics
develop more effective outreach policies and activities.

72
Methods

Study design and population

We performed a cross-sectional study using convenience samples from five STI clinics
operating within the Public Health Services in the eastern part of the Netherlands.
All clients age 15 to 25 years who visited one of the STI clinics during the study period
(2011 to 2013) were selected for inclusion. Clients who were 25 years or older were
excluded, because Dutch clients of that age cannot consult the STI clinic without any
additional STI risk factors, whereas EM clients may consult regardless of their age
4
and STI risk factors.

Consultation rates
STI clinic data and population data from the Dutch Central Bureau of Statistics were
used to establish STI clinic consultation rates per 1000 people, calculated by dividing
the number of first consultations in a year of STI clinic attendees belonging to a
specific EM (cumulative over the three study years) by the total number of inhabitants
(age 15–25) belonging to that EM in the region (cumulative over the three study years)
multiplied by 1000. We calculated 95% confidence intervals for these rates using
standard methods for single rates (http://vassarstats.net/prop1.html).

Chlamydia positivity
Chlamydia positivity, determined by a laboratory diagnosis of chlamydia following
any consultation at the STI clinic during the study period, included chlamydia
diagnoses in all consultations, including repeat consultations, within one year.

Ethnic minorities
The following EMs were identified: Dutch (The Netherlands), Asian (Asia, excluding
Turkey), Western (West and South Europe, United States, Canada, Virgin Islands,
Newfoundland, Greenland, Belize and Oceania), East and North European (Bulgaria,
former Soviet Union, former Yugoslavia, Hungary, Poland, Romania, Slovakia,
Czech Republic, Denmark, Finland, Iceland, Ireland, Luxembourg, Norway, Sweden,
Switzerland), African (Africa, excluding Egypt and Morocco), Latin American (North
and South America, excluding the United States and Canada), Antillean and Aruban
(Netherlands Antilles and Aruba), Turkish (Turkey), Egyptian and Moroccan (Egypt
and Morocco), Surinamese (Suriname) and ethnicity unknown (country of birth was
not a mandatory question in the client registration system) [1].
EM group assignment was based on the person’s own birth country combined
with the parental birth country. Persons were defined as belonging to an EM when
one or both parents were born outside the Netherlands. When clients’ parents were

73
from different EMs, the client was categorised under the mother’s birth country;
when clients and parents were from different EMs, the client was categorised under
his or her own birth country.

Demographic and behavioural STI risk factors

Demographic variables extracted from the STI database included: gender (women,
men, transgender), and ethnic group; behavioural and STI risk factors included: sexual
preference (heterosexual, homosexual, or bisexual), number of partners in the last six
months (fewer than three, or three or more), STI related symptoms, an STI notification
involving a partner, partner in a risk group (men who have sex with men or a partner
with an ethnic origin). The risk factors ‘intravenous drug use’ and ‘sex work’ were not
included in the analysis because of their low numbers.

Data analysis
First, descriptive statistics were compiled for demographic and behavioural variables
and STI risk factors. Consultation rates in specific ethnic groups were compared
to native Dutch rates using the absence or presence confidence interval overlap.
Chlamydia positivity was calculated separately for each ethnic group. Gonorrhoea,
syphilis, hepatitis B, and HIV were not included in the analysis because of low numbers.
Furthermore, binary logistic regression analyses were performed to identify
determinants associated with chlamydia positivity. Cases with missing data were
excluded from the analysis. Determinants were analysed using univariate analysis and
multivariate backward logistic regression, in which a p<0.05 was considered statistically
significant. Analyses were conducted using IBM SPSS Statistics for Windows, version
21.0 (IBM Inc., Somers, New York, United States).

Privacy and ethics

The data were obtained from the medical records of five STI clinics in a fully anonymised
and de-identified manner. Medical employees and the STI clinic data manager were
responsible for anonymising the dataset used in this study, so the researchers had no
access to patient identifying information.
The study protocol was exempted from formal medical-ethical approval under
prevailing law in the Netherlands (law of medical scientifical research in humans:
https://wetten.overheid.nl/BWBR0009408/2020-01-01) because of the retrospective
observational design using anonymous data from a patient registration system, as
stated by the National Central Committee for Human Studies: www.ccmo.nl and the
guidelines for conduct of good behaviour in research www.federa.org. Therefore,
individual client consent was not required.

74
Results

Population data
The population of 15 to 25 year-olds between 2011 and 2013 remained relatively stable
in the eastern part of the Netherlands, with between 387,318 and 387,924 inhabitants
in this age group. The proportion of EMs in the population also remained stable, with
16.5% having an ethnicity other than Dutch in 2011, and 16.8% in 2013.

STI clinic data

4
In total, the STI clinics were consulted 26,590 times between 2011 and 2013. This
included 2,749 repeat consultations within the same calendar year by the same person,
which were excluded, leaving 23,841 clients in the analysis. Seven percent of the clients
were EMs. Of all clients, 62% were women and 38% men (Table 1).
The native Dutch clients’ consultation rate was 22.5 per 1000 person years,
compared to a mean rate of 8.5 per 1000 among EMs. Consultation rates in clients
originating from Netherlands Antilles and Aruban ethnicity (19.8 per 1000 person
years) were comparable to those in Dutch clients. Latin American clients consulted
the STI clinic more often than Dutch clients (30.5 vs 22.5 per 1000 person years). The STI
clinic consultation rate was significantly lower in all other ethnic groups than in Dutch
ethnicity clients. Turkish and Egyptians/Moroccan clients had the lowest consultation
rates (1.6 and 2.7 per 1000 person years, respectively).

75
 Table 1. Demographic characteristics of 23,841 clients visiting an STI clinic in the eastern part
of the Netherlands in 2011-2013 and consultation rates per 1000 person years by ethnicity

n (%) Consultation rate#

(95%CI)

First consultations Total 23,841 (100) -

Gender Women 14,829 (62.2) -

Men 9,009 (37.8)
Transgender 3 (<0.1)

Ethnicity Dutch 21,753 (91.2) 22.5 (22.1-22.7)

EM total 1643 (7.0) 8.5 (8.1-8.9)
Asian 350 (1.5) 8.0 (7.2-8.9)
Western 334 (1.4) 8.3 (7.6-9.3)
East/North European 283 (1.2) 13.9 (12.4-15.6)
African 214 (0.9) 18.5 (16.2-21.2)
Latin American 163 (0.7) 30.5 (26.3-35.8)
Antillean/Aruban 162 (0.7) 19.8 (16.9-23.1)
Turkish 67 (0.3) 1.6 (1.2-2.0)
Egyptian /Moroccan 36 (0.2) 2.7 (1.9-3.8)
Surinamese 34 (0.1) 4.0 (2.8-5.7)
Unknown 435 (1.8) -

# Number of STI clinic consultations per 1000 person years

- Not applicable
In bold: Significantly different from Dutch ethnicity
Abbreviations: 95%CI= 95% confidence interval

Chlamydia positivity
The chlamydia positivity rate of all consultations (including the 2,749 repeated
consultations) during the study period was 15.5%. The highest chlamydia positivity
rate was found among Antillean and Aruban clients (27.1%), followed by African clients
(24.7%). Dutch ethnicity clients had a 15.4% chlamydia positivity rate. The lowest
chlamydia positivity rates were observed among Latin Americans (12.0%) and Western
Europeans (13.8%), see Table 2. Women and men had similar chlamydia positivity rates
(15.5% and 15.6%, respectively), while clients with a heterosexual preference had a
higher chlamydia positivity rate (16.4%) than clients with a homosexual or bisexual
preference (10.3% and 10.6%, respectively). Clients who had received a partner STI
notification had the highest chlamydia positivity rate (41.8%), followed by clients who
had STI related symptoms (23.0%).

76
 The multivariable analysis showed that clients more likely to have a positive
chlamydia diagnosis than native Dutch clients included those with an Eastern or
Northern European ethnicity (OR = 1.44, 95%CI 1.03 to 2.02), an African ethnicity
(OR = 1.73, 95%CI 1.25 to 2.39) or an Antillean or Aruban ethnicity (OR = 1.95, 95%CI
1.37 to 2.77). Clients who had STI related symptoms (OR = 2.18, 95%CI 2.02 to 2.35), a
heterosexual preference (homosexual preference OR = 0.50, bisexual preference OR
= 0.58), partners in a risk group (OR = 1.27, 95%CI 1.15 to 1.40), received a partner
notification (OR = 5.99, 95%CI 5.52 to 6.50) or had three or more partners in the past
six months (OR = 1.30, 95%CI 1.21 to 1.41) were more likely to be chlamydia positive.
4

Table 2. Chlamydia positivity and determinants of chlamydia positivity in 26,590

consultations at STI clinics in the eastern part of the Netherlands, 2011-2013

Number of Chlamydia Univariate Multivariate

consultations positive analysis analysis
n (%) % (Nc) OR (95%CI) OR (95%CI)*

Ethnicity

Dutch 24,234 (92.8) 15.4 (3,721) 1 1

Asian 377 (1.4) 15.6 (59) 1.02 (0.77-1.35) 0.84 (0.61-1.14)
Western 390 (1.5) 13.8 (54) 0.89 (0.66-1.18) 0.95 (0.70-1.30)
East/North European 349 (1.3) 17.5 (61) 1.17 (0.88-1.54) 1.44 (1.03-2.02)
African 239 (0.9) 24.7 (59) 1.81 (1.34-2.43) 1.73 (1.25-2.39)
Latin American 191 (0.7) 12.0 (23) 0.76 (0.49-1.17) 0.74 (0.46-1.19)
Antillean/Aruban 192 (0.7) 27.1 (52) 2.05 (1.49-2.82) 1.95 (1.37-2.77)
Turkish 81 (0.3) 18.5 (15) - -
Egyptian/Moroccan 39 (0.1) 23.1 (9) - -
Surinamese 47 (0.2) 23.4 (11) - -

Gender

Women 16,460 (61.9) 15.5 (2555) 1 1

Men 10,127 (38.1) 15.6 (1582) 0.99 (0.93-1.06) 0.94 (0.87-1.02)
Transgender 3 (0.0) 0 - -

STI symptoms

No 18,589 (69.9) 12.9 (2404) 1 1

Yes 7,418 (27.9) 23.0 (1706) 2.03 (1.89-2.17) 2.18 (2.02-2.35)
Missing 583 (2.2) - - -

Sexual preference

Heterosexual 23,692 (89.1) 16.4 (3876) 1 1

Homosexual 1,738 (6.5) 10.3 (179) 0.57 (0.48-0.67) 0.50 (0.41-0.60)
Bisexual 686 (2.6) 10.6 (73) 0.61 (0.47-0.78) 0.58 (0.44-0.75)
Missing 474 (1.8) - - -

77
 Table 2. Continued

Number of Chlamydia Univariate Multivariate

consultations positive analysis analysis
n (%) % (Nc) OR (95%CI) OR (95%CI)*

Partner in risk group

No 22,315 (83.9) 15.3 (3416) 1 1

Yes 3,839 (14.4) 18.7 (716) 1.27 (1.16-1.39) 1.27 (1.15-1.40)
Missing 436 (1.6) - - -

Number of partners last 6 months

<3 15,734 (59.2) 14.9 (2341) 1 1

>= 3 9,785 (36.8) 17.6 (1719) 1.22 (1.14-1.31) 1.30 (1.21-1.41)
Missing 1,071 (4.0) - - -

Partner STI notification

No 22,360 (84.1) 11.4 (2559) 1 1

Yes 3,744 (14.1) 41.8 (1564) 5.61(5.19-6.06) 5.99 (5.52-6.50)
Missing 486 (1.8) - - -

N Number of consultations
Nc Number of consultations positive for chlamydia
* All determinants were entered in the multivariable analyses, except for Turkish, Egyptian/
Moroccan en Surinamese EM groups due to low numbers
In bold: OR that are significant (at p<0.05)
1 reference
- Not applicable
Abbreviations: OR = odds ratio , 95%CI= 95% confidence interval

Consultation rates combined with chlamydia positivity

Figure 1 combines the findings from Tables 1 and 2 and displays consultation rates and
chlamydia positivity categorised by EM. Clients with an Eastern or Northern European,
African, Antillean, or Aruban ethnicity had higher chlamydia odds ratios but lower
consultation rates than native Dutch clients. Clients with an Asian or Western ethnicity
had lower consultation rates and slightly lower chlamydia odds ratios that native Dutch
clients (Table 1).

78
 4

Figure 1. Consultation rates and chlamydia odds ratios from multivariable analysis
by ethnicity. Consultation rates significantly lower or equal to Dutch rates are striped and
chlamydia OR significantly higher than Dutch is coloured grey. For significance see Tables 1
and 2.

79
Discussion

Our study shows that EMs visiting the STI clinic are underrepresented compared to
Dutch clients. Western, African, Turkish, Surinamese, East and North European, Asian,
and Egyptian and Moroccan clients consult the STI clinic less often than Dutch clients.
In contrast, Latin American clients visited more often than Dutch clients and clients
from the Netherlands Antilles and Aruba visited the STI clinic equally as often as Dutch
clients.
In addition, clients with Netherlands Antillean and Aruban, African, and East
and North European ethnicity were chlamydia positive more often than Dutch clients.
Considering both consultation rates and chlamydia positivity rates, clients with
Antillean and Aruban, African, and East and North European ethnicity are particularly
important target groups for regional public health services in the eastern Netherlands,
because these EM groups had lower or equal STI clinic consultation rates combined
with higher chlamydia positivity rates than native Dutch clients.

Strengths and limitations

One strength of this study is the high applicability of the proposed innovative approach.
Combining population data and STI clinic data to provide proportional person-based
consultation rates for different ethnicities is an easy and effective method to inform
STI clinic policy.
A second strength is the low risk of bias, since we included a study population of 15-
to 25-year-old EM clients whose STI clinic entry requirements matched those applied to
the native Dutch population, and outcome variable measures were uniformly assessed.
Our results apply to the eastern part of the Netherlands, and are not generalisable to
other Netherlands regions because previous efforts to reach EM groups and provide
intervention can differ between STI clinics. However, the method used to calculate
EM-specific consultation and STI rates is of value for STI clinics both inside and outside
the Netherlands.
One limitation of our study is lack of generalizability to all STIs, since HIV, syphilis,
hepatitis B, and gonorrhoea positivity numbers were small, resulting from the age-
category limitation.
Another limitation concerns case-ascertainment, because the STI clinics did not
collect client residence information, so we therefore assumed that all STI clinic visitors
lived locally. Thus, we cannot rule out that some consultations included in the analyses
belonged to clients living outside the region.
A third limitation is that we only included data on ethnic minorities receiving
STI care from STI clinics, whereas general practitioners also provide STI care in the
Netherlands; this limits the generalizability of our results [1]. It is possible that EMs

80
visit general practitioners more often, perhaps because of health system knowledge or
travel distance. Conversely, testing at STI clinics is free, but general practitioners charge
for testing, which may affect clients’ choice of medical facilities.

Comparison with other studies

Our study’s method of calculating consultation rates best compares with the study by
van Oeffelen et al. [7], who conducted a similar study in four big Netherlands’ cities.
Their study differed from ours in that they included repeat consultations in their rates
and included a wider age range. In general, van Oeffelen et al. found much higher
4
consultation rates, from two (Dutch) to 12 (Surinamese) times as high as in our study.
This might be explained by the two differences described above, plus their STI clinics’
policy of focusing more on EMs attending their clinics.
Consultation rates for the ethnicities in our study were similar to those in van Oeffelen
et al.’s, except for the Dutch (ranking 1 in our study and 6 in van Oeffelen et al.’s) and the
Surinamese (ranking 8 in our study, and 3 in van Oeffelen et al.’s). The higher ranking of
the Dutch in our study may be explained by the Dutch and EM’s equal access to the STI
clinics, stemming from the age restriction we imposed for inclusion. The Surinamese’s
higher consultation rate in van Oeffelen et al.’s study may be related to different ethnic
backgrounds in the Surinamese between the two studies. Oudhof demonstrated that the
Suriname population in Amsterdam comprises more African Surinamese, whereas the
Surinamese in our study region comprises more South-Asian Surinamese [10]. As Hulstein
et al. showed, Surinamese with a South-Asian origin demonstrate lower sexual healthcare
seeking behaviour compared to Surinamese with an African origin, which might explain
the difference in Surinamese EM consultation rates between the two studies [11].
Our study found that most ethnic minorities have a lower STI clinic consultation
rate than the Dutch. However, another Dutch study found that ethnic minorities visit
a general practitioner for STI testing as often as or more often than the Dutch, except
for the Turkish [12]. In a questionnaire study by Goenee, Surinamese and Antilleans
were found to test more often and Turkish and Moroccans less often than the Dutch
[13]. This was confirmed by Hulstein et al. [11].
Potential explanations why EM groups have lower consultation rates remain
unclear. This study did not include potential barriers that may explain why EM groups
have lower consultation rates, such as health literacy, knowledge of health systems,
health seeking behaviour, affordability (e.g. travel cost to the clinic), individual health
concerns or language barriers. These factors have been shown to differ between
ethnicities or social groups and influence healthcare access [14,15]. Further research
is needed to elucidate which factors set EM groups apart, and shape consultation rates
and service access in distinctive ways. This information will be important in tackling
the lower consultation rates among specific EM groups.

81
 We found that Netherlands Antilleans and Aruban, African, and East and North
European ethnicities were more often chlamydia positive than the Dutch. Van Oeffelen
et al. found STI positivity in all ethnicities more often than in the Dutch. Conversely,
they did not find higher chlamydia positivity in East Europeans, which was consistent
with Visser et al., who also did not find higher chlamydia positivity for African ethnicity
[1]. Netherlands Antillean ethnicity had higher chlamydia positive rates in all three
studies. Given the low numbers, we could not analyse Surinamese ethnicity in our
study. However, van Oeffelen et al., Visser et al., and Hulstein et al. found that clients
with Surinamese ethnicity were more often chlamydia positive than the Dutch [1,7,11].
High chlamydia positivity in an EM group visiting an STI clinic does not necessarily
indicate a high chlamydia prevalence in the regional EM population, because high-risk
people may be more likely to visit an STI clinic. Therefore, low chlamydia positivity in
an EM may indicate a true low chlamydia prevalence in the regional EM population,
but could also indicate an under-representation at the STI clinic of the high-risk group
in this EM, or a preference for consulting with a general practitioner.

Conclusion

In this study we demonstrated a highly applicable and innovative method for calculating
consultation rates proportional to local EM populations and provided comprehensive
data on STI clinic consultation and chlamydia positivity rates. Our method was shown
to be robust and simple, and to provide useful information to inform STI clinic policy
and regional interventions. The results indicate that clinics should prioritise reaching
out to ethnicities with a low consultation rate and a high positivity rate.

Acknowledgements

We would like to acknowledge the participating STI clinics of the Regional Public
Health Services in the eastern part of the Netherlands for providing us access to the
anonymised data from their region.

82
References

1. Visser M, Van Aar F, Op de Coul ELM, Slurink IAL, Van Wees DA, Hoenderboom BM, et al.
Sexually transmitted infections in The Netherlands in 2017. RIVM 2018
2. Matser A, Luu N, Geskus R, et al. Higher Chlamydia trachomatis prevalence in ethnic
minorities does not always reflect higher sexual risk behaviour. PLoS One. 2013;8:e67287.
doi: 10.1371/journal.pone.0067287
3. Coyle RM, Miltz AR, Lampe FC, et al. Ethnicity and sexual risk in heterosexual people
attending sexual health clinics in England: a cross-sectional, self-administered questionnaire
study. Sex Transm Infect 2018;94:384-391
4. Fenton KA, Mercer CH, McManus S, et al. Ethnic variations in sexual behaviour in Great
Britain and risk of sexually transmitted infections: a probability survey. Lancet 2005;365:1246–
55
5. Furegato M, Chen Y, Mohammed H, et al. Examining the role of socioeconomic deprivation
in ethnic differences in sexually transmitted infection diagnosis rates in England: evidence
from surveillance data. Epidemiol Infect 2016;144:3253–62
6. Wayal S, Hughes G, Sonnenberg P, et al. Ethnic variations in sexual behaviours and sexual
health markers: findings from the third British National Survey of Sexual Attitudes and
Lifestyles (Natsal-3). Lancet Public Health 2017;2:e458-e472
7. Van Oeffelen AA, Van den Broek IV, Doesburg M, et al. Ethnic and regional differences in STI
clinic use: a Dutch epidemiological study using aggregated STI clinic data combined with
population numbers. Sex Transm Infect 2017;93:46-51
8. Evans AR, Mercer CH, Parutis V, et al. Factors associated with genitourinary medicine clinic
attendance and sexually transmitted infection diagnosis among central and east European
migrants in London. Sex Transm Infect 2011;87:331-6
9. Dhar J, Griffiths CA, Cassell JA, et al. How and why do South Asians attend GUM clinics?
Evidence from contrasting GUM clinics across England. Sex Transm Infect 2010;86:366-70
10. Oudhof K, Harmsen C, Loozen S, et al. Omvang en spreiding van Surinaamse bevolkingsgroepen
in Nederland. Centraal Bureau voor Statistiek, Bevolkingstrends, 2e kwartaal 2011; 97-102
11. Hulstein SH, Matser A, Alberts CJ, et al. Differences in Chlamydia trachomatis seroprevalence
between ethnic groups cannot be fully explained by socioeconomic status, sexual healthcare
seeking behavior or sexual risk behavior: a cross-sectional analysis in the Healthy Life in an
Urban setting (HELIUS) study. BMC Infectious Diseases 2018;18:612
12. Woestenberg PJ, van Oeffelen AAM, Stirbu-Wagner I et al. Comparison of STI-related
consultations among ethnic groups in the Netherlands: an epidemiologic study using
electronic records from general practices. BMC Family Practice 2015 16:70
13. Goenee M, Kedde H, Picavet C. Condoomgebruik en testgedrag in Nederland. Tijdschrift voor
Seksuologie 2012;36:12
14. Pemberton S, Phillimore J, Bradby H, Padilla B, Lopes J, Samerski S, et al. Access to healthcare
in superdiverse neighbourhoods. Health Place 2019;55:128–35 pmid:30559049
15. Wasserman J, Palmer RC, Gomez MM, Berzon R, Ibrahim SA, Ayanian JZ. Advancing Health
Services Research to Eliminate Health Care Disparities. American Journal of Public Health
2019 109:S1, S64–S69 pmid:30699021
Chapter 5
Sexual risk and STI testing behaviour
among Dutch female and male
self-employed sex workers;
a cross-sectional study
using an Internet based survey

Carolina (Karlijn) J.G. Kampman

Charlotte M.M. Peters
Femke D.H. Koedijk
Troy (Triston) S. Berkenbosch
Jeannine L.A. Hautvast
Christian J.P.A. Hoebe

Published as a research article in BMC Public Health, 2022 Jun;22(1):1155

Abstract

Background
Sex workers are men, women or transgender people who have sex in exchange for
money or goods. Self-employed sex workers solicit clients independently from a
third-party. Self-employed sex workers are at risk of acquiring sexually transmitted
infections (STIs) through their work. We performed a cross-sectional study, using an
Internet survey conducted in 2019-2020 aiming to establish sexual risk behaviour and
STI testing behaviour among female and male self-employed sex workers.

Results
A total of 76 female self-employed sex workers (FSW) and 79 male self-employed sex
workers (MSW) completed the survey. Both FSW and MSW more often had sex with
partners of the opposite sex during work (65.8% FSW, 61.6% MSW) and in their private
life (63.3% FSW; 64.5% MSW). During vaginal sex 35.7% of FSW and 29.6% of MSW did
not always use a condom. Inconsistent condom use was observed in 35.7% of FSW and
29.6% of MSW during vaginal sex, 46.2% of FSW and 35.7% of MSW did not always use a
condom during receptive anal sex. The majority of both FSW and MSW tested for STIs
in the past year (67.1% FSW; 67.7% MSW) and 67.5% were aware of the possibility of
low-threshold testing at an STI clinic. In the past year, 11.6% of FSW and 8.1% of MSW
had an STI.

Conclusion
The reported STI positivity rate among self-employed sex workers was not very high.
However, STI prevention efforts remain important considering the low compliance
with condom use during sex work. Moreover, not testing for STIs in the past year was
substantial with one-third of both FSW and MSW and one-third of both FSW and MSW
being unaware of the possibility of low-threshold testing at an STI clinic, warranting
efforts to increase testing uptake in this population.
Background

Sex workers are men, women or transgender men or women who receive income,
employment, survival (e.g., food or shelter), and/or drugs in exchange for sexual
services [1,2,3]. Sex workers are of public health importance because of their high
occupational risk of acquiring sexually transmitted infections (STIs), including
human immunodeficiency virus (HIV), and their risk for further spreading of these
STIs through clients and private partners to the general population [1,4].
Several studies have concluded that inconsistent condom use can contribute to
the spread of STIs [5,6,7]. A systematic review and meta-analysis performed among
female sex workers (FSW) globally reported 19.1% (95% CI: 1.7 to 36.4) engaged in 5
unprotected vaginal sex and 46.4% (95% CI: 9.1 to 83.6) engaged in unprotected
anal sex [8]. A Dutch study performed in three cities reported 81% of sex workers
exhibited consistent condom use among female and male-to-female transgender
sex workers [4]. Another Dutch study suggested that almost half of all sex workers
had engaged in condomless anal sex with clients in the past 6 months [9].
Inconsistent condom use is one of the factors leading to high STI positivity rates
among sex workers worldwide [10-12]. However, STI positivity rates are lower in
Western countries than in other countries. A progress report by the World Health
Organization showed that 11% of sex workers worldwide acquired HIV in 2020,
while in the Netherlands the HIV prevalence among FSW was estimated to be 1.5%,
and only 1.1% of male sex workers (MSW) tested positive for HIV in 2019 in the
Netherlands [4,12,13]. Furthermore, another Dutch study showed that 20.3% of
MSW having sex with men and 20.0% of transgender sex workers were known to be
HIV-positive, compared with none of the MSW having sex with women [9]. The STI
positivity rate among FSW remained relatively stable at approximately 9.5% in the
Netherlands between 2006 and 2013 [14]. Other Dutch studies reported 29–40% STI
positivity among MSW having sex with men, 26% STI positivity among transgender
sex workers and 13% STI positivity among MSW having sex with women, compared
with 9% among FSW [9,15].
Sex workers can be employed by a third-party, such as an agency, manager,
or gatekeeper (pimp), or they can be self-employed. Self-employed sex workers
solicit clients independently from a third-party [2,4,16]. These self-employed sex
workers are harder to reach for healthcare workers, because they are not organized
or centralized such as sex workers who work in a formal indoor or outdoor setting,
where they can be reached by outreach activities [2]. Furthermore, Dutch legislation
only legalizes sex work with a permit, leaving limited work options without a permit
for self-employed sex workers and forcing them to work in illegal circuits, which
increases the risks of exploitation and unsafe work conditions [2,17]. The STI clinics

87
in the Netherlands offer free and anonymous STI testing for sex workers, but it is not
known whether self-employed sex workers are reached by STI clinics. Consequently,
this high-risk population is presumably hidden in sexual health care efforts.
To gain more insight into the group of female and male self-employed sex workers,
we performed a cross-sectional study, using an Internet-based survey to assess and
compare sexual risk behaviour and STI testing behaviour between female and male
self-employed sex workers and to assess determinants of reported STI testing in the
past year. The study outcomes can be used to gain insight into this hidden population,
possibly at risk for STIs, and to inform public health professionals about STI prevention
and tailoring sexual healthcare services for this population.

88
Methods

Study design, population and data collection

We performed a cross-sectional study, using an Internet survey conducted in the
Netherlands from 2019 to 2020. The Internet survey consisted of questions on
sociodemographic characteristics, sexual behaviour, and alcohol and/or drug use while
working. The Internet survey was advertised throughout March 2019 with a banner
on three national websites where sex workers advertise themselves. Additionally, the
mobile phone numbers of sex workers advertising on the Internet, were used to send
text messages with a link to our survey, or were made attentive to our survey during
STI clinic visits and outreach activities. 5
The participants were asked to participate in the survey only once. Participants
who met the definition of self-employed sex workers, were aged 18 years or older
and performed sex work in the past 6 months were included in the analyses. In this
study, we define FSW, MSW, and transgender sex workers (TSW) as self-employed sex
workers if they had engaged in sex in exchange for money or goods and solicited clients
independently of a third-party.
The incentive to participate in the study was the allotment of 50 Euros at the end of
the study period. The survey software program SurveyMonkey (San Mateo, California,
USA) was used to embed the questions and provide data for analysis.

Variables
We assessed the demographic variables of country of birth and the reported highest
level of education, relationship status, and gender of the sex partners in private life
and in work setting. Educational level was defined as follows: low educational level
was pre-primary education, primary education, or first stage of basic education;
intermediate educational level was lower secondary education, or second stage
of basic education; and high educational level was upper secondary education or
tertiary education.
Furthermore, we assessed work-related variables, such as; work years, work
frequency, reasons for self-employed sex work, other job besides sex work, main
jobs, and work location. In addition, the following STI risk behaviour variables were
assessed; types of sex during work and inconsistent condom use during work. When
participants selected “never” or “not always” using a condom during work, this was
considered to be inconsistent condom use. Receiving oral sex and insertive anal sex
were assessed for MSW only, unprotected sex by client demand, asking more money
for unprotected sex, asking more money for special request, alcohol or drug use during
work, more often unprotected sex with alcohol or drugs and group sex were STI risk
behaviour variables. Finally, we assessed STI testing behaviour variables: self-reported

89
STI testing in the past year, STI test location, reasons for STI testing, and having had an
STI in the past year. Having had an STI in the past year was based on self-reporting and
chlamydia, gonorrhoea, syphilis, HIV, hepatitis B, genital warts, herpes, trichomonas,
and scabies were considered STIs.

Data analysis
Descriptive analyses were performed for all variables. The χ2 test was used to test for
differences in proportions between male and female sex workers, as well as factors for
being tested for STI in the past year. A p-value of < 0.05 was considered to be statistically
significant in both analyses. Analyses were conducted using SPSS for Windows (version
26.0; IBM Inc., Somers, New York, USA).

90
Results

Study population
A total of 316 individuals started the survey, 153 of whom were excluded based on an
exclusion criterion (i.e., being younger than 18 years, not being self-employed, and/
or did not perform sex work in the past 6 months), and 163 met the inclusion criteria
and participated in the survey (51.6%). There were 79 FSW (48.5%), 76 MSW (46.6%)
and 8 TSWs (4.9%). In Table 1, we only display the FSW and MSW, as the TSW were not
included owing to low numbers.
Table 1 shows that compared with MSW, FSW more often had a country of birth
other than the Netherlands (34.2% FSW vs. 19.7% MSW, p = 0.043). Most FSW and MSW 5
had an intermediate or high educational level (17.7% FSW and 7.9% MSW had a low
educational level, p = 0.154). Both FSW and MSW more often had sex with opposite
sex partners in their private life (63.3% FSW and 64.5% MSW, p = 0.979) as well as
during work (65.8% FSW and 61.6% MSW, p = 0.085). FSW more often worked in the sex
industry for 1 to 5 years compared with MSW (49.3% FSW and 42.1% MSW, p = 0.027).
MSW worked daily less frequently than FSW (36.7% FSW and 17.4% MSW) and they
more often worked monthly or less than FSW (15.2% FSW and 36.8% MSW, p = 0.016).
Compared with MSW, FSW reported more often that the main reason to engage in self-
employed sex work was “for the money” (60.8% FSW and 40.8% MSW, p = 0.013). MSW
reported “I like sex” more often to be the main reason for self-employed sex work than
FSW (51.3% MSW and 34.2% FSW, p = 0.031). Compared with MSW, FSW worked more
often in a window (8.9% FSW vs. 0.0% MSW, p = 0.008), at a private club (20.3% FSW
vs. 6.6% MSW, p = 0.013) or at a club (12.7% FSW and 2.6% MSW, p = 0.020), while MSW
worked more often at a client’s home than FSW (30.4% FSW vs. 46.1% MSW, p = 0.045).

STI risk behaviour and STI testing

During oral sex, 62.0% of FSW and 62.8% of MSW did not always use a condom
(p = 0.930). When practicing vaginal sex, 35.7% of FSW and 29.6% of MSW did not always
use a condom (p = 0.437). Furthermore, 46.2% of FSW and 35.7% of MSW did not always
use a condom during receptive anal sex (p = 0.339), although these findings were not
significantly different between FSW and MSW. When more money was offered, FSW
consented to unsafe sex and other special requests more often than MSW (87.5% FSW
vs. 58.3% MSW, p = 0.023, for unsafe sex and 59.2% FSW vs 36.6% MSW, p = 0.007, for
special requests). Alcohol use during work was reported by 25.3% of FSW and 18.7% of
MSW (p = 0.300), and drug use by 34.2% of FSW and 28.4% of MSW (p = 0.103).
Regarding STI testing, 67.1% of FSW and 67.7% of MSW underwent STI testing in the
past year (p = 0.946). Most FSW went to an STI clinic for the test (53.2% FSW and 43.2%
MSW, p = 0.359), while most MSW went to a general practitioner (47.7% MSW and 38.3%

91
FSW, p = 0.487). Of all sex workers who participated in this survey, 67.5% were aware
that the STI clinics in the Netherlands offered low threshold STI testing for sex workers
(data not displayed in Table 1). The main reason for STI testing for both FSW and MSW
was routine screening (58.0% FSW and 68.0% MSW, p = 0.710). In the past year, 11.6%
of FSW and 8.1% of MSW reported having an STI (p = 0.500).

Table 1. Self-reported demographic and behavioural characteristics of self-employed female

and male sex workers in the Netherlands (2019-2020)

Female sex Male sex Total p-value

workers workers n (%)*
n (%)* n (%)*

Demographics

Country of birth 0.043

The Netherlands 52 (65.8) 61 (80.2) 113 (72.9)
Other country 27 (34.2) 15 (19.7) 23 (14.8)

Educational level 0.154

Low educational level 14 (17.7) 6 (7.9) 20 (12.9)
Intermediate educational level 37 (46.8) 36 (47.4) 73 (47.1)
High educational level 28 (35.4) 34 (44.7) 62 (40.0)

Relationship status 0.021

Relationship 36 (45.6) 21 (27.6) 57 (36.8)
Single 43 (54.4) 55 (72.4) 98 (63.3)

Gender sex partners in private life 0.979

Same sex 6 (7.6) 6 (7.9) 12 (7.7)
Opposite sex 50 (63.3) 49 (64.5) 99 (63.9)
Both opposite and same sex 23 (29.1) 21 (27.6) 44 (28.4)

Gender work sex partners 0.085

Same sex 2 (2.7) 9 (12.3) 11 (7.5)
Opposite sex 48 (65.8) 45 (61.6) 93 (63.7)
Both opposite and same sex 23 (31.5) 19 (26.0) 42 (28.8)

Sex work

Work years 0.027

<1 year 11 (16.4) 21 (36.8) 32 (25.8)
1-5 year 33 (49.3) 24 (42.1) 57 (46.0)
>5 year 23 (34.3) 12 (21.1) 35 (28.2)

Work frequency past 6 months 0.016

Daily 29 (36.7) 22 (17.4) 46 (29.7)
Weekly 38 (48.1) 31 (40.8) 69 (44.5)
Monthly or less 12 (15.2) 28 (36.8) 40 (25.8)

92
Table 1. Continued

Female sex Male sex Total p-value

workers workers n (%)*
n (%)* n (%)*

Reasons for self-employed sex work

Wanted to be independent 21 (26.6) 6 (7.9) 27 (17.4) 0.002
Bad experience with pimp, partner 8 (10.1) 2 (2.6) 10 (6.5) 0.058
For the money 48 (60.8) 31 (40.8) 79 (51.0) 0.013
Freedom in working hours 31 (39.2) 14 (18.4) 45 (29.0) 0.004
I like sex 27 (34.2) 39 (51.3) 66 (42.6) 0.031
Need money for drugs 9 (11.4) 1 (1.3) 10 (6.5) 0.011
Already had casual partners, made it my job 13 (16.5) 7 (9.2) 20 (12.9) 0.179 5
Because of a friend 10 (12.7) 7 (9.2) 17 (11.0) 0.492
Other 7 (8.9) 4 (5.3) 11 (7.1) 0.383

Other job besides sex work 0.000

Yes 27 (40.3) 41 (71.9) 68 (54.8)
No 40 (59.7) 16 (28.1) 56 (45.2)

Main job 0.084

Sex work 7 (25.9) 4 (10.0) 11 (16.4)
Other job 20 (74.1) 36 (90.0) 56 (83.6)

Work location
Window 7 (8.9) 0 (0.0) 7 (4.5) 0.008
Private club 16 (20.3) 5 (6.6) 21 (13.5) 0.013
At home 28 (35.4) 28 (35.4) 56 (36.1) 0.856
Club 10 (12.7) 2 (2.6) 12 (7.7) 0.020
At client’s home 24 (30.4) 35 (46.1) 59 (38.1) 0.045
Hotel room 27 (34.2) 30 (39.5) 57 (36.8) 0.494
Home of third party 11 (13.9) 12 (15.8) 23 (14.8) 0.744
Care institution 2 (2.5) 6 (7.9) 8 (5.2) 0.131
Swingers club 8 (10.1) 7 (9.2) 15 (9.7) 0.847
Massage parlour 7 (8.9) 2 (2.6) 9 (5.8) 0.097
Streets 7 (8.9) 1 (1.2) 8 (5.2) 0.034
Other 6 (7.6) 8 (10.5) 14 (9.0) 0.524

STI risk behaviour

Types of sex during work

Oral sex 65 (82.3) 68 (89.5) 133 (85.8) 0.199
Vaginal sex 68 (86.1) 60 (78.9) 128 (82.6) 0.242
Receptive anal sex 33 (41.8) 27 (35.5) 60 (38.7) 0.425
Insertive anal sex n.a. 43 (56.6) n.a. n.a.
BDSM or fetish 27 (34.2) 15 (19.7) 42 (27.1) 0.043
Use sex toys 41 (51.9) 42 (55.3) 83 (53.5) 0.675
Erotic massage with manual climax 52 (65.8) 44 (57.9) 96 (61.9) 0.310
Erotic massage with oral climax 44 (55.7) 48 (63.2) 92 (59.4) 0.344

93
 Table 1. Continued

Female sex Male sex Total p-value

workers workers n (%)*
n (%)* n (%)*

Inconsistent condom use during work

When giving oral sex 44 (62.0) 27 (62.8) 71 (62.3) 0.930
When receiving oral sex (only men) n.a. 56 (80.0) n.a. n.a.
With vaginal sex 35 (35.7) 21 (29.6) 46 (32.6) 0.437
With receptive anal sex 18 (46.2) 15 (35.7) 44 (40.7) 0.339
With insertive anal sex (only men) n.a. 14 (25.9) n.a. n.a.

Unprotected sex at clients’ demand 0.861

Yes 24 (32.9) 25 (34.2) 49 (33.6)
No 49 (67.1) 48 (65.8) 97 (66.4)

Ask more money for unprotected sex 0.023

Yes 21 (87.5) 14 (58.3) 35 (72.9)
No 3 (12.5) 10 (41.7) 13 (27.1)

Ask more money for special requests 0.007

Yes 42 (59.2) 26 (36.6) 68 (47.9)
No 29 (40.8) 45 (63.4) 74 (52.1)

Alcohol use during work 0.300

Yes 20 (25.3) 14 (18.7) 34 (21.9)
No 59 (74.7) 62 (81.6) 121 (78.1)

Drug use during work 0.103

Yes 27 (34.2) 17 (22.4) 44 (28.4)
No 52 (65.8) 59 (77.6) 111 (71.6)

More often unprotected sex with alcohol 0.708

or drugs
Yes 13 (43.3) 8 (38.1) 21 (41.2)
No 17 (56.7) 13 (61.9) 30 (58.8)

Group sex during work 0.739

Yes 33 (45.2) 31 (42.5) 64 (43.8)
No 40 (54.8) 42 (57.5) 82 (56.2)

STI testing

STI testing past year (self-reported) 0.946

Yes 47 (67.1) 44 (67.7) 91 (67.4)
No 23 (32.9) 21 (32.3) 44 (32.6)

94
Table 1. Continued

Female sex Male sex Total p-value

workers workers n (%)*
n (%)* n (%)*

STI test location(s) of STI test(s) in past

year^
STI clinic 25 (53.2) 19 (43.2) 44 (48.4) 0.359
General practitioner 18 (38.3) 21 (47.7) 39 (42.9) 0.487
Hospital 5 (10.6) 3 (6.8) 8 (8.8) 0.503
Home-test 2 (4.3) 6 (13.6) 8 (8.8) 0.131
Other 6 (12.8) 1 (2.2) 7 (7.7) 0.060

Main reasons for last STI testing

5
Routine screening 33 (50.8) 34 (68.0) 67 (58.3) 0.710
Partner notification 5 (7.7) 3 (6.0) 8 (7.0) 0.777
Unprotected sex 13 (20.0) 6 (12.0) 19 (16.5) 0.104
STI related symptoms 3 (4.6) 1 (2.0) 4 (3.5) 0.330
Condom failure 7 (10.8) 4 (8.0) 11 (9.6) 0.383
Other 4 (6.2) 2 (4.0) 6 (5.2) 0.433

Had an STI in the past year (self-reported) 0.500

Yes 8 (11.6) 5 (8.1) 13 (9.9)
No 61 (88.4) 57 (91.9) 118 (90.1)

* Percentages may not precisely add up to 100% due to rounding

^ Only answered if positive with regards to STI testing last year, more than one answer was
possible
In bold, statistically significant (p<0.05)
n.a. not applicable

Reported STI testing in the past year

Table 2 shows the factors for self-reported STI testing over the past year. Only “work
years” was significantly associated with STI testing in the past year, although this was
not a linear association. Other determinants were not significantly associated with
undergoing an STI test in the past year.

95
 Table 2. Factors of self-reported STI testing in the past year among self-employed female and
male sex workers in the Netherlands (2019-2020)

STI testing past No STI testing p-value

year past year
n (%)* n (%)*

Demographics

Gender 0.946
Female 47 (67.1) 23 (32.9)
Male 44 (67.7) 21 (32.3)

Country of birth 0.747

The Netherlands 68 (66.7) 34 (33.3)
Other country 23 (69.7) 10 (30.3)

Educational level 0.542

Low educational level 12 (66.7) 6 (33.3)
Intermediate educational level 46 (71.9) 18 (28.1)
High educational level 33 (62.3) 20 (37.7)

Relationship status 0.439

Relationship 33 (63.5) 19 (36.5)
Single 58 (69.9) 25 (30.1)

Gender private sex partners 0.335

Same sex 7 (70.0) 3 (30.0)
Opposite sex 62 (71.3) 25 (28.7)
Both opposite and same sex 22 (57.9) 16 (42.1)

Gender work sex partners 0.538

Same sex 9 (81.8) 2 (18.2)
Opposite sex 57 (67.1) 28 (32.9)
Both opposite and same sex 25 (64.1) 14 (35.9)

Sex work

Work years 0.021

<1 year 20 (62.5) 12 (37.5)
1-5 year 46 (80.7) 11 (19.3)
>5 year 19 (54.3) 16 (45.7)

96
Table 2. Continued

STI testing past No STI testing p-value

year past year
n (%)* n (%)*

Work frequency past 6 months 0.640

Daily 30 (73.2) 11 (26.8)
Weekly 39 (65.0) 21 (35.0)
Monthly or less 22 (64.7) 12 (35.3)

STI risk behaviour

Inconsistent condom use during work

When giving oral sex 0.942 5
Yes 45 (68.2) 21 (31.8)
No 27 (67.5) 13 (32.5)
When receiving oral sex (only men) 0.172
Yes 36 (73.5) 13 (26.5)
No 7 (53.8) 6 (46.2)
With vaginal sex 0.168
Yes 26 (60.5) 17 (39.5)
No 63 (72.4) 24 (27.6)
With receptive anal sex 0.284
Yes 19 (61.3) 12 (38.7)
No 30 (73.2) 11 (26.8)
With insertive anal sex (only men) 0.581
Yes 9 (81.8) 2 (18.2)
No 28 (73.7) 10 (26.3)

Alcohol use during work 0.417

Yes 21 (61.8) 13 (38.2)
No 70 (69.3) 31 (30.7)

Drug use during work 0.516

Yes 28 (63.6) 16 (36.4)
No 63 (69.2) 28 (30.8)

Group sex during work 0.680

Yes 40 (65.6) 21 (34.4)
No 51 (68.9) 23 (31.1)

* Percentages may not precisely add up to 100% due to rounding

In bold, statistically significant (p<0.05)

97
Discussion

Our study shows that self-employed sex workers have a heterosexual preference, both
at work and in private life (approximately two-thirds of FSW and MSW). Approximately
two-thirds of FSW and MSW did not always use a condom while giving oral sex and
one-third with vaginal sex, and half of FSW, and one-third of MSW did not always use
a condom during receptive anal sex.
Not testing for STI in the past year was still substantial with one-third of both FSW and
MSW and one-third of all participating sex workers being unaware of the possibility
getting a low-threshold test at an STI clinic. Although condom use and STI testing are
not consistent among all sex workers, the self-reported STI positivity is relatively low
(around 10%).

Strengths and limitations

Our study provides more insight into the group of self-employed sex workers, which
is of value in addition to the existing literature on sex workers when self-employment
is mostly unknown.
However, this study has several limitations. Overall, the response to our survey was
low, despite relatively intense efforts to recruit participants. Although we clearly stated
that the participation in this study was fully anonymous, we know from interviews that
trust is an issue with sex workers, and therefore, many would likely not participate in
a survey because of anticipated governmental consequences.
Furthermore, the stigmatized subject of the survey might have led to socially
desirable responses. Moreover, the survey relied on self-reporting, which could have
led to a recall bias. This recall bias and socially desirable responses might have yielded
lower outcomes for certain variables, such as having had an STI in the past year.
Of those who participated, the majority had a higher educational level, suggesting
selection-bias. This might result in an underestimation of risk, as lower-educated sex
workers tend to use even fewer condoms during work and have fewer STI consultations
[15]. Due to advertising mainly on heterosexual sex advertising websites, a selection
bias occurred, resulting in an under-representation of MSW who have sex with men
and TSW.

Comparison to other studies

Our study showed that inconsistent condom use for both FSW and MSW ranged from 33%
during vaginal sex to 62% during oral sex (i.e., consistent condom use ranged from 67%
during vaginal sex and 38% during oral sex). Our findings are in line with an Australian study
reporting approximately the same percentages of consistent condom use during sex (33%
during oral sex, 67% during vaginal sex, and 59% during anal sex) among female, male and

98
transgender sex workers [18]. Other studies have shown higher rates of consistent condom
use among Dutch sex workers (around 80%) [4,19]. However, these studies focused on sex
workers in general, whereas we specifically addressed self-employed sex workers, which
suggests they tend to be more vulnerable to STIs. Furthermore, two studies showed that
condom use is influenced by work environments; female sex workers working exclusively
in brothels reported higher rates of condom use compared with those working privately,
however, the self-employment of sex workers was not taken into account [18,19].
Regarding STI testing, our study showed that two-thirds of both FSW and MSW had
reported performing an STI test in the past year. This finding is in line with other study
findings, which also reported STI test rates ranging between 56 and 86% [19,20]. Similar
to condom use, testing for STIs is also influenced by the work environment and one 5
study found that sex workers working in the streets had lower testing rates (56%), than
those who worked in multiple settings (streets, venues, and online, 86%) [20].
For FSW, the findings regarding STI positivity were in line with other studies
[14,15,21]. However, STI positivity rates among MSW were higher in other studies
compared with our results [9,14,22]. These studies had higher numbers of MSW who had
sex with men compared with our study and did not use self-report in a questionnaire,
but used laboratory-confirmed STI diagnoses, which might explain the difference in
STI positivity rates.

Interpretations
Although a lot of effort was put into reaching self-employed sex workers, many did not
participate in the study. Often, there is distrust of public authorities, such as the STI
clinic of the public health service who initiated the study [2]. This is due to the fact that
many cities in the Netherlands have legislations against working from home, with a
risk of being fined or forced to come out as a sex worker when caught, sometimes even
leading to eviction of the sex worker from his or her home [2]. Moreover, self-employed
sex workers need permits to practice their profession. With the application for a permit,
the address of the sex worker is placed on the municipal website, which threatens the
safety of the self-employed sex worker [2]. This legislation forces sex workers to work
in illegal circuits and isolated work locations, disrupting peer support networks and
service access and limiting risk reduction opportunities [11]. In addition to limited risk
reduction opportunities, increasing client demand for condomless sex and concerns
about income reductions if condomless sex is not offered appear to be factors related
to the provision of condomless sex [18].
In contrast, what strengthens their position is that self-employed sex workers
have a similar position on the labour market than other non-sex-related self-employed
workers. They determine their own terms and conditions, choose their own work
settings and times and set their own rates [23].

99
 There are various outreach initiatives in the Netherlands to reach sex workers,
such as offering STI testing at their work location and Internet fieldwork on websites
where sex workers advertise. Considering our study findings that one-third of self-
employed sex workers did not undergo an STI test in the past year and that one-third
of the participants were unaware of the possibility of getting low-threshold STI testing
at an STI clinic, these outreach activities might not be enough to bridge the testing gap.
Although our study provides a starting point for gathering more knowledge on
self-employed sex workers, much is still unknown. Because our study suffered from a
selection bias, more research is needed on the STI risk behaviour and test behaviour of
self-employed sex workers with a lower educational level and non-Dutch self-employed
sex workers. Moreover, self-employed MSW who have sex with men during work and
TSW were underrepresented in our study, which warrants further research on these
groups.

Conclusion

In conclusion, our study shows that approximately two-thirds of FSW and MSW had
performed an STI test in the past year, and the STI positivity rate for this population
was not very high. However, tailored STI prevention strategies remain important
considering the low compliance with condom use during work and the large number
of sexual contacts that might facilitate spread when STI positive. As self-employed sex
workers appear to be a hidden population, this continues to be a challenge with regard
to future policy and research for professionals in the field of sexual healthcare.

Acknowledgements

We would like to acknowledge the participating adult dating websites. Furthermore,

we would like to acknowledge Ilse Gerrits, an STI clinic nurse, who actively made sex
workers aware of the study.

100
References

1. Reeves A, Steele S, Stuckler D, McKee M, Amato-Gauci A, Semenza JC. National sex work policy
and HIV prevalence among sex workers: an ecological regression analysis of 27 European
countries. Lancet HIV 2017;4:e134-e140
2. Kloek M, Dijkstra M. Sekswerk en geweld in Nederland. Aidsfonds 2018
3. European Centre for Disease Prevention and Control. Mapping of HIV/STI behavioural
surveillance in Europe. Stockholm: ECDC; 2009. Retrieved from: https://www.ecdc.europa.
eu/sites/default/files/media/en/publications/Publications/0909_TER_Mapping_of_HIV_STI_
Behavioural_Surveillance_in_Europe.pdf
4. Van Veen MG, Götz HM, van Leeuwen PA, Prins P, van de Laar MJW. HIV and sexual risk
behavior among commercial sex workers in the Netherlands. Arch Sex Behav. 2010;39:714-23 5
5. Magalhães RLB, Sousa LRM, Gir E, Galvão MTG, Oliveira VMC, Reis RK. Factors associated to
inconsistent condom use among sex workers. Rev Lat Am Enfermagem 2019;27:e3226
6. Tracas A, Bazzi AR, Artamonova I, Rangel MG, Staines H, Ulibarri MD. Changes in Condom
Use Over Time Among Female Sex Workers and Their Male Noncommercial Partners and
Clients. AIDS Educ Prev 2016;28:312-24
7. Decker MR, Park JN, Allen ST, Silberzahn B, Footer K, Huettner S, et al. Inconsistent Condom
Use Among Female Sex Workers: Partner-specific Influences of Substance Use, Violence, and
Condom Coercion. AIDS Behav 2020;24:762-774
8. Owen NB, Baggaley RF, Elmes J, Harvey A, Shubber Z, Butler AR, et al. What Proportion of
Female Sex Workers Practise anal Intercourse and How Frequently? A Systematic Review and
Meta-analysis. AIDS Behav 2020; 24: 697–713
9. Drückler S, van Rooijen MS, de Vries HJC. Substance Use and Sexual Risk Behavior Among
Male and Transgender Women Sex Workers at the Prostitution Outreach Center in Amsterdam,
the Netherlands. Sex Transm Dis 2020;47:114-121
10. McBride B, Shannon K, Strathdee SA, Goldenberg SM. Structural determinants of HIV/
STI prevalence, HIV/STI/sexual and reproductive health access, and condom use among
immigrant sex workers globally. AIDS 2021;35:1461-1477
11. Platt L, Grenfell P, Meiksin R, Elmes J, Sherman SG, Sanders T et al. Associations between sex
work laws and sex workers’ health: a systematic review and meta-analysis of quantitative and
qualitative studies. PLoS Med 2018;15:e1002680
12. World Health Organization. Global progress report on HIV, viral hepatitis and sexually
transmitted infections, 2021. Accountability for the global health sector strategies 2016–2021:
actions for impact. Geneva: World Health Organization; 2021
13. Staritsky LE, van Aar F, Visser M, Op de Coul ELM, Heijne JCM, Götz HM, et al. Sexually
transmitted infections in the Netherlands in 2019. RIVM 2020
14. Verscheijden MMA, Woestenberg PJ, Götz HM, van Veen MG, Koedijk FDH, van Benthem
BHB. Sexually transmitted infections among female sex workers tested at STI clinics in the
Netherlands, 2006-2013. Emerg Themes Epidemiol 2015;12:12
15. Verhaegh-Haasnoot A, Dukers-Muijrers NH, Hoebe CJP. High burden of STI and HIV in male
sex workers working as Internet escorts for men in an observational study: a hidden key
population compared with female sex workers and other men who have sex with men. BMC
Infect Dis 2015;15:291

101
16. Flath NL, Brantley MR, Davis WW, Lim S, Sherman SG. Patterns of primary healthcare use
among female exotic dancers in Baltimore, Maryland. Women Health. 2019;59:334-46
17. Campbell R, Sanders T, Scoular J, Pitcher J, Cunningham S. Risking safety and rights: online
sex work, crimes and ‘blended safety repertoires’. Br J Sociol 2019;70:1539-1560
18. Selvey LA, Hallett J, McCausland K, Bates J, Donovan B, Lobo R. Declining Condom Use Among
Sex Workers in Western Australia. Front Public Health. 2018 Nov 27;6:342
19. European Centre for Disease Prevention and Control. Thematic report: Sex workers.
Monitoring implementation of the Dublin Declaration on Partnership to Fight HIV/AIDS in
Europe and Central Asia. ECDC 2015
20. Chien J, Schneider KE, Tomko C, Galai N, Lim S, Sherman SG. Patterns of Sex Work Client
Solicitation Settings and Associations with HIV/STI Risk Among a Cohort of Female Sex
Workers in Baltimore, Maryland. AIDS Behav. 2021 Oct;25(10):3386-3397
21. Van Dulm E, Marra E, Kroone MM, van Dijk AE, Hogewoning AA, Schim van der Loeff MF.
Sexually transmissible infections among female sex workers in Amsterdam between 2011 and
2016: does risk vary by work location? Sex Health. 2020 Aug;17(4):368-376
22. Fournet N, Koedijk FDH, van Leeuwen AP, et al. Young male sex workers are at high risk
for sexually transmitted infections, a cross-sectional study from Dutch STI clinics, the
Netherlands, 2006-2012. BMC Infect Dis 2016;16:63
23. Nelson AJ, Hausbeck Korgan K, Izzo AM, Bessen SY. Client Desires and the Price of Seduction:
Exploring the Relationship Between Independent Escorts’ Marketing and Rates. J Sex Res.
2019:1-17

102
Chapter 6
Sexually transmitted infections in male
heterosexual Dutch clients who visited
German cross-border female sex workers;
a 3 year retrospective study

Carolina (Karlijn) J.G. Kampman

Christian J.P.A. Hoebe
René Koene
Laura Kamp
Klaus Jansen
Femke D.H. Koedijk
Alma Tostmann
Jeannine L.A. Hautvast

Published as a research article in BMC Public Health, 2020 Jul 29;20(1):1182

(Minor corrections added)
Abstract

Background
Some male heterosexual clients prefer to visit a cross-border Female Sex Worker (FSW)
because of cheaper sex and unsafe sex practices, and may therefore be at risk for
sexually transmitted infections (STI). The objective of this study was to assess whether
having commercial cross-border sex is an independent risk factor for being diagnosed
with a STI.

Methods
An observational retrospective study was performed using data of 8 Dutch STI clinics
bordering Germany, between 2011 and 2013. All male heterosexual clients of FSWs
were selected and data on country of FSW visit and occurrence of STI were used for
multivariable regression analysis.

Results
The study population consisted of 2664 clients of FSW. Most clients visited the
Netherlands (82.4%), followed by visits to another country (beyond cross-border) (9.9%)
and cross-border visits (7.8%). Clients of FSW were more likely to be STI positive when
they were younger than 25 years (OR = 0.6, 95%CI 0.4 to 0.8 25–44 years and OR = 0.5,
95%CI 0.4 to 0.7 older than 45 years), had 20 or more sex partners in the last 6 months
(OR = 2.9, 95%CI 1.9 to 4.4), did not use a condom during last sexual contact (OR = 2.2,
95%CI 1.6 to 2.9) and made cross-border visits (OR = 1.7, 95%CI 1.1 to 2.6).

Conclusions
As cross-border visits appears to be a novel independent risk factor for STI in clients
of FSW, this group should therefore be advised on STI prevention.
Background

Female sex workers (FSW) are considered a high risk group for acquiring sexually
transmitted infections (STI), due to factors associated with their work and life, which
makes them socially and physically more vulnerable. These include factors such as
history of multiple sex partners, inconsistent condom use or co-infection with other
STI and factors related to their life such as substance abuse, trauma and poverty [1,2].
There is a potential risk for further spread of STI to the general population through
their sexual contacts with male heterosexual clients with inconsistent condom use and
through sex partners that are not work related. Therefore, FSW and their clients are of
public health importance [3,4,5].
Studies to assess STI positivity in male heterosexual clients of FSW are scarce.
A study from the UK among 6239 randomly selected British men assessed that 11% 6
reported having paid for sex over a period of 5 years. This group accounted for 16%
of all participating men reporting STI diagnoses (chlamydia, gonorrhoea, syphilis,
HIV, genital warts, herpes, trichomonas, pubic lice, hepatitis B). Paying for sex in
the previous 5 years was strongly associated with reporting higher numbers of sex
partners, reporting foreign sex partners outside the UK and reporting an STI diagnosis
[6]. Another British study found that men who paid for sex (MPS) were more likely to
meet sex partners abroad than non-MPS (54% versus 12%) and were more likely to
report having had an STI (9% of MPS, versus 3% non-MPS) [7]. A third British study
demonstrated that 15% (2066/13891) of UK born HIV-positive adults acquired the HIV
infection abroad [8]. These HIV infections were mostly acquired in Thailand (534),
the USA (117) and South Africa (108). Those acquiring HIV infection abroad were
significantly more likely to have acquired it heterosexually and to have reported sex
with a commercial sex worker [8].
In the Netherlands, sex work is legal when a license is obtained. Furthermore, sex
workers who work in brothels and windows are regularly inspected and visited by public
health services, police and the municipality. In Germany, sex work is also legal when
a license is obtained, but sex worker are not always visited by public health services,
this may vary per region. Anecdotal reports from Dutch STI clinic staff suggest that
clients visit cross-border FSW because of cheaper sex offered and unsafe sex practices.
Therefore, the risk for STI may be higher when visiting cross border sex venues. This
study aims to assess whether having cross-border sex is an independent risk factor for
being diagnosed with an STI for clients of FSW living in the Netherlands. The results of
this study can be used to inform sexual health clinics access policy in the Netherlands
and to optimize preventive public health advice towards male heterosexual clients of
cross-border FSW.

107
Methods

Study design and population

We conducted a retrospective cross-sectional study using coded data from eight STI
clinics, operating at Public Health Services (PHS) in the Netherlands covering the
entire Dutch-German border region. The eight STI clinic regions were included with
the following main Dutch cities; Groningen, Emmen, Enschede, Arnhem, Nijmegen,
Eindhoven, Venlo and Maastricht, covering an area with a population of nearly 5
million inhabitants, of 17 million (total Dutch population).
The study population was defined as all self-identified heterosexual men who
attended one of the participating STI clinics in 2011, 2012 or 2013 and reported being
a client of FSW in the past 6 months. Men who identified themselves as bisexual or
homosexual were excluded. An FSW is defined as a woman who was indicated by the
client to be an FSW, and who accepted money from the client for their sexual encounter.
Clients of FSWs were defined as heterosexual men paying a woman for sex. Hereafter,
we refer to these male heterosexual STI clinic clients, who reported being a client of
FSW as ‘client’.

Data analysis
For all included client records the following data were used; demographic data (age,
sex, country of birth) and sexual behaviour (number of sex partners in the last 6 months
(FSW-partners and non-FSW partners) and condom use during last sexual contact).
Clients were regarded STI positive when one or more STIs were diagnosed, including
chlamydia, gonorrhoea, syphilis, HIV and/or infectious hepatitis B, at one or more body
locations (oral, genital, or anal) at consultation. Other STI were not routinely tested,
and therefore not included in analyses.
STI clinics record whether a patient is a client of a FSW, but the country where a
client visits a FSW is not routinely registered. Therefore, for all included client records,
open text fields were manually explored to identify whether and which country of
FSW visit was entered by the STI clinic professional. Country of visit is defined as the
country or countries of FSW visit, as reported by the client. A client who visits an FSW in
Germany was categorized as ‘cross-border visit’; FSW visit in the Netherlands as ‘visiting
the Netherlands’; FSW visits to another country than the Netherlands or cross-border,
as ‘visiting another country’. As visiting numbers to other countries besides Germany
and the Netherlands were low, we further combined these countries at the level of
continents. If a client visited Germany and another country, they were categorized
under ‘cross border visit’.

108
 Clients who did not have a registered and named country of visit were assumed to
be visiting the Netherlands. This decision was made based on the assumption that FSW
visits of STI clinic patients are most likely to be within the (Dutch) region where STI care
is provided and thus logically the default option and most prevalent option is actually
Dutch. Therefore, we expect the blank option very likely to be the ‘Dutch’ option as STI
nurses tend to omit an official registration for this common category. This assumption
was confirmed when interviewing STI clinic staff on this matter. Therefore, clients with
an unregistered country of visit were categorized under ‘visiting’ the Netherlands. This
‘blank’ option was the case in 80% of the registrations. We did perform a sensitivity
analysis based on known country of visit to estimate the validity of our assumption that
an unregistered country of visit most likely indicated a visit in the Netherlands. 20% of
clients (535/2664) had a named country of visit that was entered in the open text field.
Of these, most clients visited another country than the Netherlands (but not Germany) 6
(42.8%, 229/535), followed by visits to Germany (38.7%, 207/535) and visits within the
Netherlands (18.5%, 99/535). These low numbers of clients visiting the Netherlands
substantiate our assumption that there is a gross under registration of clients visiting
an FSW in the Netherlands.
First, descriptive statistics of demographic and sexual behaviour characteristics
were performed. Subsequently, numbers and percentages of being positive for any
STI were described, categorized in continents. Binary logistic regression analyses
were performed to identify determinants associated with STI positivity. Determinants
associated with a p value of < 0.20 in univariable analysis were further analysed by
multivariable logistic regression. STI positivity was the outcome measure and ‘country
of FSW visit’ was the dependent variable. A p value of < 0.05 in multivariable analysis
was considered to be statistically significant. Odds ratios (ORs) and 95% confidence
intervals (CIs) were presented to show the association between the determinants and
the outcome. Analyses were conducted using SPSS for Windows, version 25.0 (IBM Inc.,
Somers, New York, United States).

109
Results

Study population
As shown in Table 1, the total study population consisted of 2664 clients. Most clients
visited an FSW in the Netherlands (2194/2664, 82.4%), followed by FSW visits to another
country (263/2664, 9.9%) and cross-border FSW visits (207/2664, 7.8%). The continent
most visited besides the Netherlands and cross-border, was Asia (122/2664, 4.6%).
In total, 10.4% (n = 277/2664) of the clients were diagnosed with one or more STIs,
non-stratified by country of visit. Chlamydia was the most diagnosed STI with 8.0%
(214/2664) of clients being diagnosed, followed by gonorrhoea (2.4%, 63/2664), syphilis
(0.3%, 9/2664), 0.2% of the clients tested positive for infectious hepatitis B (5/2664) and
0.1% of clients were diagnosed with HIV (2/2664). STI positivity was highest in clients
who made cross-border FSW visits (15.5%), followed by clients who visited an FSW in
the Netherlands (10.2%) and clients who visited an FSW in another country (8.4%).

110
Table 1. Characteristics of clients categorized in country of FSW visit (n=2664)

Clients visiting Clients with cross- Clients visiting All visited

the Netherlands border visits another country countries
n=2194 n=207 n=263 n=2664
n (%) n (%) n (%) n (%)

Age
<25 years 434 (19.8) 38 (18.4) 54 (20.5) 526 (19.7)
25-44 years 1173 (53.5) 103 (49.8) 148 (56.3) 1424 (53.5)
>45 years 587 (26.8) 66 (31.9) 61 (23.2) 714 (26.8)

Country of birth
Netherlands 1848 (84.2) 174 (84.1) 215 (81.7) 2237 (84.0)
Other 346 (15.8) 33 (15.9) 48 (18.3) 427 (16.0)

Number of sex partners last 6 months (FSW and non-FSW)

0-2 780 (35.6) 58 (28.0) 92 (35.0) 930 (34.9) 6
3-5 788 (35.9) 67 (32.4) 95 (36.1) 950 (35.7)
6-20 379 (17.3) 55 (26.6) 49 (18.6) 483 (18.1)
>20 147 (7.9) 24 (11.6) 23 (8.7) 221 (8.3)
Missings 73 (3.3) 3 (1.4) 4 (1.5) 80 (3.0)

Condom used during last sexual contact

Yes 929 (42.3) 95 (45.9) 107 (40.7) 1131 (42.5)
No 1246 (56.8) 108 (52.2) 149 (56.7) 1503 (56.4)
Missings 19 (0.9) 4 (1.9) 7 (2.7) 30 (1.1)

STI diagnosed at consultation

Yes 223 (10.2) 32 (15.5) 22 (8.4) 277 (10.4)
No 1971 (89.8) 175 (84.5) 241 (91.6) 2387 (89.6)

Continent/country of FSW visit* n (%) STI positivity

n (%)

Other European 66 (25.1) 6 (9.1)

Asia 122 (46.4) 11 (9.0)
Africa 29 (11.0) 2 (6.9)
Oceania 1 (0.4) 0 (0.0)
North America 7 (2.7) 0 (0.0)
South America 17 (6.5) 1 (5.9)
Multiple continents 9 (3.4) 2 (22.2)

percentages may not precisely add up to 100% due to rounding

*Clients reporting visiting a FSW abroad, but no country of visit was reported, are not displayed
(n=12)

111
STI positivity and predictors
The predictors for STI positivity among clients are shown in Table 2. In multivariable
analysis clients were more likely to be STI positive when they were younger than
25 years of age (OR = 0.6, 95%CI 0.4 to 0.8 in the age group 25–44 years and OR = 0.5, 95%CI
0.4 to 0.7 in the age group older than 45 years), had 20 or more sex partners in the last
6 months (OR = 2.9, 95%CI 1.9 to 4.4), did not use a condom during last sexual contact
(OR = 2.2, 95%CI 1.6 to 2.9) and made cross-border FSW visits (OR = 1.7, 95%CI 1.1 to 2.6).

Table 2. Demographic and behavioral predictors for STI positivity among clients of FSW
(n=2664)

Univariable Multivariable
regression analysis regression analysis
OR(95%CI) OR(95%CI)

Age, median years (IQR)

<25 years ref ref
25-44 years 0.5 (0.4-0.7) 0.6 (0.4-0.8)
>45 years 0.5 (0.3.0.7) 0.5 (0.4-0.7)

Country of birth
Netherlands ref ns
Other 1.3 (0.9-1.8)

Number of sex partners last 6 months (FSW and non-FSW)

0-2 ref ref
3-5 1.4 (1.0-1.9) 1.3 (0.9-1.8)
6-20 1.3 (0.9-1.9) 1.3 (0.9-1.9)
>20 2.9 (2.0-4.4) 2.9 (1.9-4.4)

Condom used during last sexual contact

Yes ref ref
No 2.2 (1.6-2.9) 2.2 (1.6-2.9)

Country of FSW visit

Netherlands ref ref
Cross-border 1.7 (1.1-2.5) 1.7 (1.1-2.6)
Another country 0.8 (0.5-1.3) 0.8 (0.5-1.2)

ref, reference
ns, not significant
In bold: significant (p<0.20 in univariable and p<0.05 in multivariable analysis)

112
Discussion

This is the first study assessing STI risk of clients who had sex with an FSW in another
country. Study outcomes showed that the majority of clients visited FSW in the
Netherlands (82,4%), followed by visits to another country (263/2664, 9.9%) and cross-
border visits of FSW to Germany (207/2664, 7.8%). STI positivity was highest among
clients who made cross-border FSW visits to Germany (15.5% versus 10.2% visiting the
Netherlands and 8.4% visiting another country). STI risk was significantly associated
with being a client with cross-border sex in Germany (OR = 1.7). Three independent
risk factors for STI positivity were 20 or more sex partners in the last 6 months, being
younger than 25 years and not using a condom during last sexual contact.

Limitations 6
The main limitation of this study is that the country where commercial sex took place was
not systematically recorded, as in the majority (80%) of records no country was mentioned.
Nevertheless, we categorized clients who didn’t have a registered country of visit under
‘visiting the Netherlands’. This assumption that most of such data entries were the default
option (Dutch) was in general confirmed by STI clinic staff.
Another limitation of this study is that only clients who visited a Dutch STI clinic in a
region bordering Germany were selected. Therefore, the results are not generalizable to
the rest of the Netherlands. Nevertheless, clients living further away from the border are
less likely to visit a FSW in Germany. However, this study shows that the behavioural aspect
(condom use, number of sex partners) remains of great importance in being diagnosed
with an STI.
A third limitation is that it was not assessed whether condom use during the last sexual
contact was with an FSW, or with another sexual contact. However, we assume that clients
who reported not having used a condom during last sexual contact are clients who are more
prone to or prefer to not use a condom in general.
One last limitation is that we could only include heterosexual men, based on their own
identification instead of behaviour. This might have given false information, as it is known
that there are men who identify themselves as heterosexual, but have sex with men as well.
We do, however, think that this is a minor limitation, because the nurses at the STI clinic
tend to thoroughly ask the clients about their behaviour and sexual preferences.

Cross-border sex is an independent predictor for STI

Our study showed an overall STI positivity rate among clients of 10.4% which was
comparable to other Dutch studies reporting similar proportions (9–10%) [9-13]. This
indicates that our study population could be generalizable for all Dutch clients of FSW.
From 2015 onwards, clients of FSW are no longer considered a high risk group by the

113
Dutch Ministry of Health based on the balance of limited financial resources and relative
low STI positivity (10% among clients of FSW versus 18% among all female STI clinic
attendees, 19% among all heterosexual men and 21% among men who have sex with
men [9]). Because of this policy they are no longer eligible for free and anonymously
consultations at Dutch STI clinics. Due to the relatively low STI positivity among clients
of FSW, reconsidering this changed public health policy has proven to be of lesser need.
Our study showed that making cross-border visits to Germany to an FSW is an
independent STI risk factor, compared to visiting the Netherlands or another country.
There are other studies that show that making cross-border visits poses a higher risk of
getting an STI, but these studies describe primarily high levels of STI positivity among
(clients of ) FSW in countries bordering Ethiopia, Vietnam and Mexico [14-17]. These
countries are difficult to compare to European countries, due to different cultural
context.
A possible explanation for a higher STI risk in Dutch clients, when visiting FSW
in Germany as suggested by anecdotal information is the relatively higher number of
Eastern European FSWs in German sex venues compared to Dutch. In an outreach study
performed in Germany among ‘difficult to reach’ FSW who were not in contact with
counselling and treatment institutions, 88% of the FSWs were not born in Germany.
The risk of acquiring an STI was increased for FSWs born outside Germany, who work
in large sex venues [18]. In a recent study performed among FSW in the Netherlands,
48% were of non-Dutch origin and 12% were of Eastern European origin [19]. Therefore,
condom use is always of importance when visiting an FSW and this message should be
stressed whenever clients take an STI test.

Other predictors for STI

Our study showed that clients who did not use a condom were more often STI positive.
There is a well-known relationship between condom use and reducing the risk of getting
an STI [20,21]. Though national data is difficult to generalise, due to very different
national legislative, administrative and cultural contexts, there are studies that also
report on the relationship between decreasing condom use by FSWs and an increasing
STI positivity among FSWs [22-25]. An Italian study assessing condom use among clients
of FSW showed that cumulatively, 87 and 85% of vaginal and anal intercourses were
respectively reported as regularly protected by condom [26]. A Chinese study found that
clients were 10 times more likely to have an STI (either self-reported or tested) than
non-client Chinese men, and they were equally likely to use condoms inconsistently
with their spouses [5]. Therefore, clients who prefer to make cross-border visits, should
be motivated to use a condom.

114
 A high number of sex partners (more than 20) showed to be more likely to cause
a higher risk of STI which is a confirmation of many previous studies like two British
studies which reported a strong association with reporting larger numbers of sex
partners and STI positivity in a group that paid for sex in the past 5 years [6,7].

Public health implications

Working together internationally is the key in lowering STI prevalence in clients of
FSW. A group of Dutch clients visit Germany because it is nearby, relatively cheap sex
is offered, and unsafe sex may be practised. STI clinics in the border regions should
therefore make an effort to educate clients who visit Germany and who are young,
have multiple sex partners and do not use a condom on sexual risk behaviour. Also,
more research is needed to assess reasons for unsafe sex practices among clients as
well as FSW. 6
Furthermore, more effort should be made to reach FSW who are not in contact with
counselling and treatment institutions [18]. Government aided educational programs
in promoting condom use among FSW have also proven to be beneficial in achieving
positive sexual health outcomes [27,28]. These joined efforts could enhance wellbeing
of FSW, increase knowledge among clients and could eventually lower STI prevalence
in both FSW and clients of FSW.

115
Conclusion

The main study finding is that Dutch clients who make cross-border visits to FSW
in Germany, are more likely to be STI positive than clients who visit a FSW in the
Netherlands or in another country. Furthermore, study findings showed three other
independent predictors; clients younger than 25 years of age, clients who have multiple
sex partners (> 20 in last half year) and clients who did not use condoms were more
likely to be STI positive, which might inform a targeted approach in this potential risk
group. When clients of FSW meet this high risk profile, regular STI testing and eventual
treatment should be considered. Furthermore, STI prevention advice should focus on
clients of FSW who make cross-border visits in Germany.

Acknowledgements

We would like to acknowledge the participating STI clinics of the Regional Public
Health Services in the regions bordering Germany (GGD Groningen, GGD Drenthe,
GGD Twente, GGD Noord- en Oost Gelderland, GGD Gelderland Midden, GGD
Gelderland Zuid, GGD Noord Limburg, GGD Zuid Limburg) for providing us access to
the anonymised data from their region.

116
References

1. Abad N, Baack BN, O’Leary A, Mizuno Y, Herbst JH, Lyles CM. A Systematic Review of HIV and
STI Behavior Change Interventions for Female Sex Workers in the United States. AIDS Behav
2015;19:1701-19
2. Baral S, Beyrer C, Muessig K, Poteat T, Wirtz AL, Decker MR, et al. Burden of HIV among
female sex workers in low-income and middle-income countries: a systematic review and
meta-analysis. Lancet Infect Dis 2012;12:538-549
3. Cwikel JG, Lazer T, Press F, Lazer S. Sexually transmissible infections among female sex
workers: an international overview with an emphasis on hard-to-access populations. Sex
Health 2008;5:9-16
4. Poon AN, Li Z, Wang N, Hong Y. Review of HIV and other sexually transmitted infections
among female sex workers in China. AIDS Care 2011;23:5-25
5. Huang ZJ, Wang W, Martin MC, Nehl EJ, Smith BD, Wong FY. “Bridge population”: sex workers
or their clients? STI prevalence and risk behaviors of clients of female sex workers in China. 6
AIDS Care 2011 Jun;23:45-53
6. Jones KG, Johnson AM, Wellings K, Sonnenberg P, Field N, Tanton C, et al. The prevalence
of, and factors associated with, paying for sex among men resident in Britain: findings from
the third National Survey of Sexual Attitudes and Lifestyles (Natsal-3). Sex Transm Infect
2015;91:116-23
7. Ward H, Mercer CH, Wellings K, Fenton K, Erens B, Copas A, et al. Who pays for sex? An
analysis of the increasing prevalence of female commercial sex contacts among men in
Britain. Sex Transm Infect 2005;81:467-71
8. Rice B, Gilbart VL, Lawrence J, Smith R, Kall M, Delpech V. Safe travels? HIV transmission
among Britons travelling abroad. HIV Med 2012;13:315-7
9. Van Oeffelen AAM, van Aar F, van den Broek IVF, Op de Coul ELM, Woestenberg PJ, Heijne
JCM, et al. Sexually transmitted infections, including HIV, in the Netherlands in 2014. RIVM
2015
10. Van Aar F, Koedijk FDH, van den Broek IVF, Op de Coul ELM, Soetens LC, Woestenberg PJ, et
al. Sexually transmitted infections, including HIV, in the Netherlands in 2013. RIVM 2014
11. Verscheijden MMA, Woestenberg PJ, Götz HM, van Veen MG, Koedijk FDH, van Benthem
BHB. Sexually transmitted infections among female sex workers tested at STI clinics in the
Netherlands, 2006 – 2013. Emerg Themes Epidemiol. 2015;12:12
12. Visser M, van Aar F, van Oeffelen AAM, van den Broek IVF, Op de Coul ELM, Hofstraat SHI,
et al. Sexually transmitted infections, including HIV, in the Netherlands in 2016. RIVM 2017
13. Verhaegh-Haasnoot A, Dukers-Muijrers NH, Hoebe CJ. High burden of STI and HIV in male
sex workers working as internet escorts for men in an observational study: a hidden key
population compared with female sex workers and other men who have sex with men. BMC
Infect Dis 2015;15:291
14. Gezie LK, Taye BW, Ayele. Time to unsafe sexual practice among cross-border female sex
workers in Metemma Yohannes, North West Ethiopia. BMC Public Health 2015 Jul 28;15:710
15. Nguyen VT, Nguyen TL, Nguyen DH, Le TT, Vo TT, Cao TB, et al. Sexually transmitted infections
in female sex workers in five border provinces of Vietnam. Sex Transm Dis 2005;32:550-6

117
16. Robertson AM, Syvertsen JL, Ulibarri MD, Rangel MG, Martinez G, Strathdee SA. Prevalence
and correlates of HIV and sexually transmitted infections among female sex workers and their
non-commercial male partners in two Mexico-USA border cities. J Urban Health 2014;91:752-
67
17. Uribe-Salas F, Conde-Glez CJ, Juarez-Figueroa L, Hernández-Castellanos A. Sociodemographic
dynamics and sexually transmitted infections in female sex workers at the Mexican-
Guatemalan border. Sex Transm Dis 2003;30:266-71
18. Jansen K. Prävalenz von Chlamydien, gonorrhoe und Trichomonaden bei „Schwer
erreichbaren“ Sexarbeiterinnen in Berlin, Hamburg und NRW. RKI HIV&more 4, 2014
19. Kloek M, Dijkstra M. Sekswerk en geweld in Nederland. Soa AIDS Nederland 2018
20. Monsell E, McLuskey J. Factors influencing STI transmission in middle-aged heterosexual
individuals. Br J Nurs 2016;25:676-80
21. Falasinnu T, Gilbert M, Hottes TS, Gustafson P, Ogilvie G, Shoveller J. Predictors identifying
those at increased risk for STDs: a theory-guided review of empirical literature and clinical
guidelines. Int J STD AIDS 2015;26:839-51
22. Lim RB, Wong ML, Cheun ON, Tham DK, Tai BC, Chan R. Factors associated with consistent
condom use and STIs among foreign female entertainment workers: results from a cross-
sectional survey in Singapore. Sex Transm Infect. 2017;93:118-124
23. Chen Y, Abraham Bussell S, Shen Z, Tang Z, Lan G, Zhu Q, et al. Declining Inconsistent
Condom Use but Increasing HIV and Syphilis Prevalence Among Older Male Clients of Female
Sex Workers: Analysis From Sentinel Surveillance Sites (2010-2015), Guangxi, China. Medicine
2016;95:e3726
24. Sahay S, Deshpande S, Bembalkar S, Kharat M, Parkhe A, Brahme RG, et al. Failure to Use
and Sustain Male Condom Usage: Lessons Learned from a Prospective Study among Men
Attending STI Clinic in Pune, India. PLoS One 2015;10:e0135071
25. O’Connor CC, Berry G, Rohrsheim R, Donovan B, et al. Sexual health and use of condoms
among local and international sex workers in Sydney. Genitourin Med 1996;72:47-51
26. Mulieri I, Santi F, Colucci A, Fanales Belasio E, Gallo P, Luzi AM. Sex workers clients in
Italy: results of a phone survey on hiv risk behaviour and perception. Ann Ist Super Sanita
2014;50:363-8
27. Okafor UO, Crutzen R, Aduak Y, Adebajo S, Van den Borne HW. Behavioural interventions
promoting condom use among female sex workers in sub-Saharan Africa: a systematic review.
Afr J AIDS Res 2017;16:257-268
28. Chow EP, Tung K, Tucker JD, Muessig KE, Su S, Zhang X, et al. Behavioral Interventions
Improve Condom Use and HIV Testing Uptake Among Female Sex Workers in China: A
Systematic Review and Meta-Analysis. AIDS Patient Care STDS 2015;29:454-60

118
Chapter 7
Sexual behaviour and STI testing
among Dutch swingers:
A cross-sectional Internet based survey
performed in 2011 and 2018

Carolina (Karlijn) J.G. Kampman

Jeannine L.A. Hautvast
Femke D.H. Koedijk
Marieke E.M. Bijen
Christian J.P.A. Hoebe

Published as a research article in PLoS One, 2020 Oct 1;15(10):e0239750

Abstract

Background
Swingers, heterosexuals who, as couples, practice mate swapping or group sex with
other couples or heterosexual singles, are at risk for sexually transmitted infections
(STIs). Therefore, the aim of this study was to assess changes in sexual behaviour and
STI testing behaviour, as well as predictors of STI testing.

Methods
Two cross-sectional studies were performed, using the same internet survey in
2011 and 2018. For trend analysis, sexual behaviour and STI testing behaviour were
used. Socio-demographics, swinger characteristics, sexual behaviour, and psycho-
social variables were used to assess predictors of STI testing in the past year, using
multivariable regression analysis.

Results
A total of 1173 participants completed the survey in 2011, and 1005 in 2018. Condom
use decreased for vaginal (73% vs. 60%), oral (5% vs. 2%), and anal sex (85% vs. 75%).
STI positivity was reported in 23% and 30% of the participants, respectively, although
testing for STI was comparable between both years (~65%).
The following predictors of STI testing were significant: being female (OR = 1.9,
95%CI: 1.2–2.9), having a high swinging frequency (>12 times a year, OR = 3.7, 95%CI:
1.9–7.3), swinging at home (OR = 1.6, 95%CI: 1.0–2.7), receiving a partner notification
(OR = 1.7, 95%CI: 1.2–2.6), considering STI testing important (OR = 4.3, 95%CI: 2.2–8.5),
experiencing no pressure from a partner to test (OR = 0.6, 95%CI: 0.3–0.9), partners test
for STI regularly (OR = 10.0, 95%CI: 6.2–15.9), perceiving STI testing as an obligation
(OR = 2.1, 95%CI: 1.3–3.5), experiencing no barriers such as being afraid of testing (OR
= 1.9, 95%CI: 1.2–3.1), limited opening hours (OR = 1.6, 95%CI: 1.0–2.4), and forgetting
to plan appointments (OR = 3.0, 95%CI: 2.0–4.6).

Conclusions
Swingers exhibit self-selection for STI testing based on their sexual behaviour.
However, STI prevention efforts are still important considering the increasing numbers
of reported STIs, the decreased use of condom use, and the one-third of swingers who
were not tested in the previous year.
Introduction

Swingers are heterosexuals who, as couples, practice mate swapping or group sex with
other couples or heterosexual singles. Although swingers self-identify as heterosexual,
they frequently engage in same-sex sexual activities. Swingers are at risk for sexually
transmitted infections (STIs), as they engage in unprotected sex with multiple sexual
partners and substance misuse [1–3]. Swingers can transmit STIs within their own
sexual network and to other sex partners outside their network through overlapping
sexual partnerships. These concurrent sexual partnerships and potential bridging
make them a target population of public health importance [1,4].
Only a few studies have estimated STI positivity rates among swingers. A Dutch
study by Dukers et al found a Chlamydia trachomatis (CT) positivity rate of 8% and a
Neisseria gonorrhoea (NG) positivity rate of 4% among swingers, which was lower
than the STI positivity rate among all heterosexuals attending the STI clinic [5]. In the
Dutch surveillance data, the overall STI positivity rate among swinger men was 16%,
7
and 11% among swinger women [6]. A Belgian study by Platteau et al found that 81 out
of 313 swingers who reported ever being tested for STI had ever had an STI diagnosis [7].
A Dutch study by Dukers et al showed that swingers take an STI test more often
than men who have sex with men (MSM), or heterosexual men and women [5]. Another
Dutch study by Spauwen et al showed that, overall, 72%, 62%, and 56% of swingers who
consulted the STI clinic, reported that regular STI testing, partner notification, and
condom use when engaging in sex, respectively, is the norm in the swinger community
[8].
Before 2015, swingers were eligible for free and anonymous consultations at Dutch
STI clinics. However, since 2015, based on the relatively low STI incidence, they were
no longer eligible at STI clinics and have therefore been advised to consult a general
practitioner (GP) for STI testing. This change in health policy since 2015 might hamper
proper STI control in swingers, because STI testing at GPs is not free and anonymous,
and swingers might refrain from identifying themselves as a swinger.
Lack of testing in swingers might implicate a potential rise in STI prevalence, and
therefore testing behaviour among swingers is relevant as this might have a public
health impact. To our knowledge, no studies have been conducted on to determine
whether STI testing behaviour in swingers changes over time. Therefore, we performed
cross-sectional studies in 2011 and 2018, using an internet survey, to compare sexual
behaviour and STI testing behaviour, and to assess the influence of possible socio-
demographic, behavioural, and psycho-social predictors of testing behaviour. The
study outcomes can be used to evaluate current STI testing policy for swingers and
provide information about the optimal STI clinic accessing policy and optimal STI test
advice.

123
Methods

Study design, population, and data collection

Two cross-sectional studies were performed using an internet survey with the same
questions in 2011 and in 2018. The content of the internet survey was developed based
on information gathered in semi-structured interviews with swingers. The psycho-
social variables were developed based on these interviews combined with the theory
of planned behaviour [9–11]. The survey consisted of questions on socio-demography,
swinger characteristics, sexual behaviour, STI test behaviour, and psycho-social
determinants.
To recruit a broad sample of swingers in the Netherlands, both internet surveys
were advertised at national websites that are frequently visited by swingers, including
swinger websites, swinger club websites, and swinger dating websites. A banner with
a link to the survey was published on the participating websites. Participants were
requested to fill in the survey alone (not together as a couple) and were asked to only
participate in the survey once per study. Participants who did not meet the definition
of swinging (being part of a heterosexual couple and having sex with others, or being
single and having sex with heterosexual couples), participants who were younger than
18 years, and those who did not swing in the past year were excluded from the analysis.
The incentive to participate in the study was the chance to win one of five dinner
cheques with a value of 50 euros at the end of both study periods. Both internet surveys
remained online for two months.
The survey software program Survey Monkey was used to embed the questions and
provide the data for the analysis. Surveys that were not fully completed were excluded
from analysis.

Variables
Data on the following socio-demographic variables were collected: age at time of
filling in survey, highest reported level of education (low educational level is pre-
primary education; primary education or first stage of basic education; intermediate
educational level is lower secondary education or second stage of basic education and
high educational level is upper secondary education or tertiary education), gender,
sexual preference, and relationship status (single or in a relationship). We combined
the variables gender and sexual preference, as we expected sexual preference in men
to be of greater public health importance than sexual preference in women.
Furthermore, the following swinger characteristics were analysed: swinging years
(how many years engaged in swinging), swinging frequency (swinging how many times
in the past year), and swinging location (at home, sexclub, hotel, party or holiday,
answered by ‘yes’ or ‘no’).

124
 The following sexual behaviour variables were collected: mean number of partners
during swinging, ever received a partner notification for an STI during swinging period,
having had condomless sex during vaginal, oral, and/or anal sex and when changing
partners, ever had an STI during swinging period (chlamydia, gonorrhoea, syphilis,
HIV, hepatitis B, genital warts, Herpes genitalis, Trichomonas vaginalis, and scabies
were considered STIs), and drug and alcohol use during swinging.
Additionally, the following STI testing behaviour variables were collected: STI
testing in the past year, STI testing location, and reasons for STI testing.
Lastly, psycho-social variables were collected as part of the following domains: STI
risk perception, attitudes towards STI testing, social norm regarding STI testing, and
self-efficacy and barriers regarding STI testing.

Data analysis
We included only fully completed surveys in our data analysis. Descriptive analyses
were performed for all variables, separately for both years. The χ2 test was used for
7
testing differences in proportions between outcomes from 2011 and 2018. A p-value of
<0.01 was considered to be statistically significant.
Univariable and multivariable logistic regression analyses were performed to
identify predictors for the outcome measure ‘STI testing in the past year’, separately
for both years. The results of the univariable and multivariable regression analysis
were comparable between both years, except for the following predictors from the
univariable regression analysis: gender, number of partners while swinging, condom
change when changing partners, drug use, and the STI risk perception predictors
‘Swinging partners don’t have many STIs’ and ‘STI consequences are not severe’. Since
most variables in the regression analyses for both years separately were comparable,
a combined logistic regression analysis was performed to identify predictors for
the outcome measure ‘STI testing in the past year’ for 2011 and 2018 together. As the
demographic variables age and education were significantly different between 2011
and 2018, all predictors were adjusted for these demographics, as well as study year,
in the combined logistic regression analyses. Backward logistic regression was used
in multivariable analysis to further analyse the influence of predictors on STI testing.
All variables with a p-value < 0.01 in univariable analyses were included. Predictors
with p<0.01 were considered statistically significant in the multivariable analysis. Odds
Ratios (ORs) and 99% Confidence Intervals (CIs) were presented to show the associations
between the predictors and the outcomes in Table 2.
Analyses were conducted using SPSS for Windows, version 25.0 (IBM Inc., Somers,
New York, United States).

125
Medical ethical approval
The study was formally exempted from full medical ethical approval, as stated by the
medical ethical committee of the Radboudumc Nijmegen (nr: 2018–4217) and according
to Dutch Law. Data were obtained using the online survey tool ‘Survey Monkey’ and
were registered in a fully anonymized and de-identified manner. To enter the prize
pool for random allotment of dinner cheques, respondents were directed to a separate
survey where they could enter their email address (only used for sending the incentive
when applicable).

126
Results

Study population
In 2011, a total of 2152 participants started the survey, of which 1173 completed it
(54.5%). In 2018, a total of 1478 participants started the survey, of which 1005 completed
it (68.0%). Between both surveys, there were slight differences in the participating study
population of swingers. In 2018, participating swingers were slightly older (mean age
43.4 years in 2011 vs. 46.5 years in 2018), had a higher educational level (59% vs. 50%),
had slightly higher numbers of swinging years (mean 6.5 vs. 7.9 years), and had small
differences in swinging locations (e.g. in 2011 84% were swinging at home vs. 79% in
2011). Gender, sexual preference, swinging frequency, relationship status, number of
swinging partners and drug and alcohol use while swinging were equally distributed
in both years; see Table 1.

STI and sexual behaviour

7
Swingers who participated in 2018 reported having had an STI more often than swingers
who participated in 2011 (23% vs. 30%). Furthermore, in 2018, participating swingers
reported using a condom less often than participating swingers in 2011 (for example,
73% used a condom during vaginal sex vs. 59%); see Table 1.

Table 1. Socio-demographic, sexual behaviour, STI testing behaviour and psycho-social

variables of swingers in The Netherlands (2011, 2018)

2011 2018 Total p value

(n=1173) (n=1005) (n=2178)

n (%) n (%) n (%)

Socio-demographic variables

Age* <0.001
18-30 109 (9.3) 74 (7.4) 183 (8.4)
31-40 290 (24.8) 208 (20.7) 498 (22.9)
41-50 542 (46.3) 347 (34.6) 889 (40.9)
51-60 203 (17.3) 308 (30.7) 511 (23.5)
≥61 27 (2.3) 66 (6.6) 93 (4.3)

Education <0.001
Low educational level 135 (11.5) 66 (6.6) 201 (9.3)
Intermediate educational level 452 (38.7) 347 (34.7) 799 (36.8)
High educational level 582 (49.8) 588 (58.7) 1170 (53.9)

127
 Table 1. Continued

2011 2018 Total p value

(n=1173) (n=1005) (n=2178)

n (%) n (%) n (%)

Gender and sexual preference (men) 0.019

Bisexual men 324 (27.6) 311 (30.9) 635 (29.9)
Heterosexual men 443 (37.8) 402 (40.0) 845 (38.8)
Women 406 (34.6) 292 (29.1) 698 (32.0)

Relationship status 0.013

Relationship 1036 (88.3) 851 (84.7) 1887 (86.6)
Single 137 (11.7) 154 (15.3) 291 (13.4)

Swinger characteristics

Swinging years* <0.001

0-5 years 658 (56.3) 488 (48.6) 1146 (52.7)
6-10 years 326 (27.9) 282 (28.1) 608 (28.0)
11-20 years 160 (13.7) 187 (18.6) 347 (16.0)
≥21 years 25 (2.2) 47 (4.7) 72 (3.3)

Swinging frequency 0.030

1-2 times a year 161 (13.8) 119 (11.9) 280 (12.9)
3-12 times a year 692 (59.0) 635 (63.1) 1327 (61.0)
>12 times a year 320 (27.2) 251 (25.0) 571 (26.2)

Swinging location#
At home 927 (79.0) 847 (84.3) 1774 (81.5) 0.002
Sexclub 728 (62.1) 561 (55.8) 1289 (59.2) 0.003
Hotel 194 (16.5) 283 (28.1) 477 (21.9) <0.001
Party 158 (13.5) 144 (14.3) 302 (13.9) 0.563
Holidays 147 (12.5) 115 (11.4) 262 (12.0) 0.436

Sexual behaviour variables

No. partners during swinging^ 0.766

1-2 900 (76.7) 643 (64.0) 1543 (70.8)
3 or more 252 (21.5) 186 (18.5) 438 (20.1)

Ever received partner notification for an 0.289

STI during swing period
Yes 508 (43.3) 458 (45.6) 966 (44.4)
No 665 (56.7) 547 (54.4) 1212 (55.6)

Vaginal sex with condom during swinging <0.001

Always 813 (72.7) 589 (58.9) 1402 (66.7)
Not always 306 (27.3) 393 (40.0) 699 (33.3)

Oral sex with condom during swinging <0.001

Always 55 (4.9) 18 (1.8) 73 (3.5)
Not always 1072 (95.1) 964 (98.2) 2036 (96.5)

128
Table 1. Continued

2011 2018 Total p value

(n=1173) (n=1005) (n=2178)

n (%) n (%) n (%)

Anal sex with condom during swinging <0.001

Always 630 (84.6) 499 (74.6) 1129 (79.8)
Not always 115 (15.4) 170 (25.4) 258 (20.2)

Condom change when changing partners 0.005

Always 987 (91.9) 796 (88.2) 1783 (90.2)
Not always 87 (8.1) 107 (11.8) 194 (9.8)

Drug use during swinging* 0.258

Yes 572 (48.8) 513 (51.2) 1085 (49.9)
No 601 (51.2) 489 (48.8) 1090 (50.1)

Alcohol use during swinging 0.364

Yes 911 (77.7) 764 (76.0) 1675 (76.9)
No 262 (22.3) 241 (24.0) 503 (23.1) 7
Ever had an STI during swing period <0.001
Yes 266 (22.7) 298 (29.7) 564 (25.9)
No 907 (77.3) 707 (70.3) 1614 (74.1)

STI testing variables

STI testing past year 0.291

Yes 777 (66.2) 644 (64.1) 1421 (65.2)
No 396 (33.8) 361 (35.9) 757 (34.8)

STI testing location <0.001

STI clinic 496 (63.8) 291 (45.3) 787 (55.5)
General practitioner 196 (25.2) 260 (40.5) 456 (32.1)
Hospital 76 (9.8) 33 (5.1) 109 (7.7)
Home-test 3 (0.4) 47 (7.3) 50 (3.3)
Multiple test locations 4 (0.5) 6 (0.9) 10 (0.7)
Other 2 (0.3) 5 (0.8) 7 (0.5)

Reasons for STI testing 0.064

Routine screening 610 (78.5) 476 (73.8) 1086 (76.4)
Partner notification 47 (6.0) 60 (9.3) 107 (7.5)
Unprotected sex 46 (5.9) 52 (8.1) 98 (6.9)
STI related symptoms 31 (4.0) 27 (4.2) 58 (4.1)
Other 43 (5.5) 30 (4.7) 73 (5.1)

129
 Table 1. Continued

2011 2018 Total p value

(n=1173) (n=1005) (n=2178)

n (%) n (%) n (%)

Psycho-social variables

STI risk perception (%agree)$

Risk of getting an STI is really small 438 (53.9) 327 (32.5) 765 (35.1) 0.019
Swing partners don’t have many STI 632 (37.7) 509 (50.6) 1141 (52.4) 0.132
Swingers are a risk group for STI 896 (76.4) 814 (81.0) 1710 (78.5) 0.009
STI consequences are not severe 68 (5.8) 42 (4.2) 110 (5.1) 0.086

Attitudes towards STI testing (%agree)$

STI testing is important for me 999 (85.2) 854 (85.0) 1853 (85.1) 0.901
STI tests are unpleasant 251 (21.4) 222 (22.1) 473 (21.7) 0.696
Testing as prevention 71 (6.1) 86 (8.6) 157 (7.2) <0.024

Social norm regarding STI testing (%agree)$

Partners consider testing important 1005 (85.7) 879 (87.5) 1884 (86.5) 0.224
Peer pressure to test 704 (60.0) 590 (58.7) 1294 (59.4) 0.535
Partner pressure to test 724 (61.7) 606 (60.3) 1330 (61.1) 0.497
Most swingers test for STI 736 (62.7) 561 (55.8) 1297 (59.6) 0.001
Partner tests for STI regularly 739 (63.0) 592 (58.9) 1331 (61.1) 0.051
STI testing is an obligation 890 (75.9) 768 (76.4) 1658 (76.1) 0.767

Self-efficacy and barriers regarding STI testing (%agree)$

Make time 285 (24.3) 217 (21.6) 502 (23.0) 0.135

Afraid of needles 132 (11.3) 99 (9.9) 431 (10.6) 0.289
Afraid of test result 89 (7.6) 62 (6.2) 151 (6.9) 0.194
Afraid of test procedure 92 (7.8) 88 (8.8) 180 (8.3) 0.440
Coming out as a swinger 165 (14.1) 209 (20.8) 374 (17.2) <0.001
Expensive 148 (12.6) 451 (44.9) 599 (27.5) <0.001
Afraid to see acquaintances 126 (10.7) 126 (12.5) 252 (11.6) 0.192
Limited opening hours for STI testing 272 (23.2) 260 (25.9) 532 (24.4) 0.146
Secrecy for steady partner 46 (3.9) 40 (4.0) 86 (3.9) 0.944
Forget to make an appointment 148 (12.6) 151 (15.0) 299 (13.7) 0.104

percentages may not precisely add up to 100% due to rounding

* Missings are not displayed
# category ‘other’ swinging location was filled in by 42 participants in 2011 and 44 participants
in 2018
^ in 2018 169 participants had sex only with others and 30 participants had sex with own partner
only in 2011 and 2018
$ for these variables the indicated options were tested separately with a agree/disagree/neutral
categorization, the selected % is shown in the title of the variable
In bold: A p-value of <0.01 was considered to be statistically significant

130
Predictors of STI testing in the past year
The predictors of the outcome measure ‘STI testing in the past year’ are shown in Table
2. In multivariable analysis, women tested more often for STIs in the past year than
men (OR = 1.9, 95% CI 1.2 to 2.9). Furthermore, swingers who had a higher swinging
frequency tested more often than swingers with a lower swinging frequency (OR =
3.7, 95% CI 1.9 to 7.3). Swingers who swing at home tested more often than swingers
who do not swing at home (OR = 1.6, 95% CI 1.0 to 2.7). Furthermore, swingers who
were notified of an STI by a partner during the swinging period tested more often
than swingers who had not received a notification by a partner for an STI during the
swinging period (OR = 1.7, 95% CI 1.2 to 2.6).
Concerning psycho-social variables related to STI testing, variables of the domains
of attitude, social norm, and self-efficacy and barriers were significant predictors,
whereas no variables of the risk perception domain were significant predictors.
Important significant variables were that swingers who perceive STI testing to be
important (OR = 4.3, 95% CI 2.2 to 8.5), who indicate that their partner tests for STIs
7
regularly (OR = 10.0, 95% CI 6.2 to 15.9), and who perceive STI testing to be an obligation
(OR = 2.1, 95% CI 1.3–3.5), tested more often for STIs than swingers who perceived
differently. Otherwise, swingers who felt partner pressure to test had tested less often
for STIs in the past year (OR = 0.6, 95% CI 0.3 to 0.9) than swingers who did not.
Furthermore, swingers who indicated not being afraid of the test procedure (OR
= 1.9, 95% 1.2 to 3.1), did not perceive limited opening hours for STI testing (OR = 1.6,
95%CI 1.0 to 2.4), and who indicated not forgetting to make an appointment (OR =
3.0, 95%CI 2.0 to 4.6) tested more often for STIs than swingers who indicated having
opposite opinions regarding these issues.

131
 Table 2. Predictors of STI testing in the past year among swingers in The Netherlands (2011
and 2018, n=2178), adjusted for year, age and education

Univariable analysis Multivariable analysis

aOR (99%CI) aOR (99%CI)

Socio-demographic variables

Gender and sexual preference (men)

Bisexual men 1.3 (1.0-1.7) 1.2 (0.8-1.9)
Heterosexual men ref ref
Women 1.7 (1.2-2.2) 1.9 (1.2-2.9)

Relationship status
Relationship ref nt
Single 1.1 (0.8-1.6)

Swinger characteristics

Swinging years
0-5 years ref nt
6-10 years 1.1 (0.8-1.4)
11-20 years 1.1 (0.7-1.5)
≥21 years 1.0 (0.5-2.0)

Swinging frequency
1-2 times a year ref ref
3-12 times a year 2.9 (2.0-4.1) 2.0 (1.1-3.5)
>12 times a year 6.3 (4.1-9.6) 3.7 (1.9-7.3)

Swinging location (ref=no)*

At home 2.8 (2.1-3.7) 1.6 (1.0-2.7)
Sexclub 0.8 (0.6-1.0) nt
Hotel 1.3 (1.0-1.7) nt
Party 1.6 (1.1-2.3) ns
Holidays 1.3 (0.9-1.9) nt

Sexual behaviour variables

No. partners during swinging

1-2 ref ns
3 or more 1.5 (1.1-2.1)

Ever received partner notification during

swing period
Yes 3.8 (2.9-4.9) 1.7 (1.2-2.6)
No ref ref

Vaginal sex with condom during swinging

Always ref nt
Not always 1.0 (0.8-1.4)

132
Table 2. Continued

Univariable analysis Multivariable analysis

aOR (99%CI) aOR (99%CI)

Oral sex with condom during swinging

Always ref nt
Not always 1.2 (0.6-2.3)

Anal sex with condom during swinging

Always ref nt
Not always 0.9 (0.6-1.3)

Condom change when changing partners

Always ref nt
Not always 0.6 (0.4-0.9)

Drug use during swinging

Yes 2.9 (2.2-3.7) 1.3 (0.9-2.0)
No ref ref

Alcohol use during swinging 7

Yes 0.7 (0.5-0.9) nt
No ref

Ever had an STI during swinging-period

Yes 3.5 (2.5-4.8) 1.4 (0.9-2.3)
No ref ref

Psycho-social variables

STI risk perception (ref=agree/neutral)*

Risk of getting an STI is small 1.9 (1.5-2.5) ns

Swing partners don’t have many STI 1.2 (0.8-1.9) nt
Swingers are a risk group for STI 0.8 (0.5-1.2) nt
STI consequences are not severe 1.4 (1.0-1.8) ns

Attitudes towards STI testing (ref=disagree/neutral)*

STI testing is important for me 15.4 (10.1-23.5) 4.3 (2.2-8.5)

STI tests are unpleasant 0.6 (0.4-0.8) ns
Testing as prevention 0.6 (0.4-1.0) ns

Social norm regarding STI testing (ref=disagree/neutral)*

Partners consider testing important 10.8 (7.2-16.2) ns

Peer pressure to test 2.9 (2.3-3.7) ns
Partner pressure to test 5.2 (4.0-6.6) 0.6 (0.3-0.9)
Most swingers test for STI 4.0 (3.1-5.1) ns
Partner tests for STI regularly 16.5 (12.3-22.1) 10.0 (6.2-15.9)
STI testing is an obligation 8.1 (6.0-10.9) 2.1 (1.3-3.5)

133
 Table 2. Continued

Univariable analysis Multivariable analysis

aOR (99%CI) aOR (99%CI)

Self-efficacy and barriers regarding STI testing (ref=agree/neutral)*

Make time 3.6 (2.8-4.6) ns

Afraid of needles 2.8 (2.1-3.7) ns
Afraid of test result 2.1 (1.6-2.8) ns
Afraid of test procedure 5.4 (4.1-7.2) 1.9 (1.2-3.1)
Coming out as swinger 3.8 (2.9-4.9) ns
Testing is expensive 2.4 (1.8-3.1) ns
Afraid to see acquaintances 2.6 (1.9-3.3) ns
Limited opening hours 2.8 (2.2-3.5) 1.6 (1.0-2.4)
Secrecy steady partner 3.5 (2.5-5.0) ns
Forget to make appointment 5.4 (4.1-7.0) 3.0 (2.0-4.6)

ref, reference
*for these variables the indicated options were each tested separately with a yes/no or agree/
disagree/neutral categorization, the reference being shown in the title of the variable
In bold: significant (p<0.01 in univariable and p<0.01 in multivariable analysis), ns: not
significant, nt: not tested

134
Discussion

Statement of principal findings

Our study of two cross-sectional Dutch surveys showed that swingers reported reduced
use of condoms in 2018 (for example, in 2011, 73% used a condom during vaginal sex,
compared to 59% in 2018) and reported having had an STI more often (23% versus
30%) than swingers who participated in 2011. However, a similar majority of swingers
reported testing for STIs in both years (66% in 2011 and 64% in 2018) and regarded
testing for STIs as important (85% in 2011 and 85.0% in 2018). We thus recognize an
increased STI positivity rate and increase in sexual risk behaviour between 2011 and
2018 in swingers, although testing behaviour remained the same.
The following predictors for STI testing in swingers were assessed and appeared
to be positive: swingers with a higher swinging frequency (>12 times a year OR = 3.7),
swingers who were notified of an STI by a partner (OR = 1.7), swingers who swing at
home (OR = 1.6), swingers who feel that STI testing is an obligation (OR = 2.1), swingers
7
whose partners test for STIs regularly (OR = 10.0), and swingers who state that STI
testing is important (OR = 4.3) tested for STI more often.

Strengths and weaknesses

A strength of this study was that a large number of swingers participated in the survey
in both years (55% and 68%). Due to changed public health policy, it has become more
difficult for swingers to be tested at STI clinics after 2015, and swingers are therefore
harder to reach for studies through STI clinics. Posting the advertisement online has
proven to be effective in reaching swingers and has shown the willingness among
swingers to participate in research and voice their opinions.
Another strength of this study is the measurement of psycho-social variables,
such as STI risk perception, attitudes, social norms, and self-efficacy regarding
STI testing besides the more often measured sexual behaviour variables. With the
use of these variables, clearer insight has been obtained into reasons and beliefs
of swingers possibly influencing STI testing behaviours. Addressing these reasons
in public health messages might lower existing barriers for swingers who are still
hesitant to undergo testing, even though almost two-thirds are already regularly
tested.
However, a general limitation of our study is a possible sampling bias. First,
only swingers who visit a swinger dating website were invited to participate. As a
consequence, generalizability to the entire population of swingers in the Netherlands
might be affected, although we know from field work and other studies that most
swingers are registered at these websites.

135
 Though we did perform semi-structured interviews with swingers and used the theory
of planned behaviour as input for our survey, we did not validate our survey. Therefore, we
do not know for sure if our survey is measuring what we intended to measure. Our results
should be read bearing this in mind.
Third, STI diagnosis was self-reported over their period of swinging years, though
self-reported STI history may not be an appropriate proxy for true STI history. Therefore,
self-reported STI diagnosis might hamper translation into the prevalence or incidence of
STI [12].
Lastly, in this study, no identifying information was available, and therefore we do
not know if the same swingers participated in both surveys. Study findings show that
participants in 2018 were older and reported more swinging years than those in 2011. This
might indicate that some swingers participated in both years, which might have led to
overestimation of some outcomes.

Comparison to other studies

This study shows that the majority of participating swingers tested for STIs in the past
year (66.2% in 2011 and 64.1% in 2018). A Canadian study, however, stated that swingers
‘rarely’ access STI health services (< 40.8% visited STI health services) [13]. Since public
health policy changed in 2015, it is more difficult for swingers to access STI clinics in the
Netherlands. This change in policy is reflected in our study findings, which shows that
instead of testing at an STI clinic, swingers report visiting their general practitioner or
ordering a home test more often than in 2011. This is in line with national data on declining
STI clinic attendance of swingers [6].
Furthermore, this study shows a substantial percentage of self-reported STI diagnosis
during swinging years (22.7% in 2011 and 29.7% in 2018). This finding is in line with a Belgian
study performed by Platteau et al, which reported that 26% of the swingers have had an STI
[7]. Several other studies have reported about STI positivity rates among swingers, but they
reported lower STI incidences ranging from 8 to 13%, because of a shorter time span in
which the STI was diagnosed or reported [1,5,7]. Our study shows that swingers who have
a higher swinging frequency and those who were notified by a partner during a swinging
period, tested more often for STI. There are no other studies that have found a similar
relationship. There are, however, studies that have shown associations between a high STI
positivity rate among swingers who have received a partner notification, swingers who had
STI related symptoms, swingers with a previous STI, and swingers who had unprotected
sex [5,8,13].
Our study also assessed psycho-social variables as predictors for STI testing in the
past year. There are no other studies on psycho-social predictors of STI testing among
swingers. There are, however, studies among students on predictors of STI testing. These
studies show that attitude was positively associated with STI testing among students, as

136
were perceived social norms towards STI testing, high STI risk perception, and the absence
of perceived STI test barriers. These findings are in line with our study, except for high STI
risk perception, as, in our multivariable analysis, we did not have significant results in this
domain [14,15].
Our study also shows that within the domain of self-efficacy and barriers, swingers
who are not afraid of the test procedure, who do not experience limited opening hours,
and who do not forget to make an appointment test for STIs, tested more often than those
swingers experiencing the opposite. There are no studies that have assessed self-efficacy
and barriers towards STI testing among swingers, but there are studies performed on self-
efficacy and test barriers among MSM. One Canadian study among MSM reported that
perceived lack of health knowledge among testing providers and limited clinical capacity
were two major barriers towards STI testing [16]. A Dutch study among MSM found that
burdensome testing procedures, among others, was a barrier towards STI testing [17].

Significance of the study

7
Our study findings show that swingers in the Netherlands test for STIs regularly, even after
the change in public health policy that made swingers no longer eligible at STI clinics for
free and anonymous STI testing. Therefore, reconsidering this changed public health policy
on swingers has proven to be of lesser need.
Although swingers test for STIs regularly, the location of STI testing has changed, when
comparing study results of 2011 and 2018. Participating swingers in 2018 reported visiting
a GP more than participating swingers in 2011. However, as studies show that GPs may
omit testing for all STIs and all body locations, especially when swingers do not identify
themselves as such and being MSM while swinging, which means that education is needed
for GPs [18–23].
Participating swingers in 2018 reported making use of a home-based STI test more
often than participating swingers in 2011. Home-based testing has advantages, such as
a wider reach, being anonymous, and no need to travel for an STI test. However, there
are also downsides to home-based testing, such as poor quality of the STI test and lack of
opportunity to obtain sexual health counselling [24–26]. Fortunately, a list of test facilities
proven to be of good quality is already present in the Netherlands. Monitoring these online
and home-based test facilities will continue to be needed in the future.
It is of concern that swingers did report a higher STI positivity rate during their
swinging years, when comparing results from 2011 with 2018. However, participants
in 2018 were older and had more swinging years than participants in 2011. Therefore,
participating swingers in 2018 had a greater time period to report having had an STI than
participating swingers in 2011. However, condom use with any kind of sex had decreased
when comparing 2011 to 2018. These findings indicate that primary prevention targeting
swingers to prevent them from getting STIs is still needed.

137
Conclusion

This study shows that two-third of swingers tested for STIs in the past year. STI testing
is perceived as important, and barriers for testing such as fear or logistical challenges
are infrequently reported. Swingers show a self-selection for STI testing based on their
sexual risk behaviour, such as swingers who receive a partner notification and swingers
with a high swinging frequency undergoing more testing for STIs. Taking swingers into
account as a target group for STI prevention efforts is still important considering the
high reported STI positivity rate, the decreased use of condoms, and the one-third of
swingers who were not tested in the previous year.

Acknowledgements

We would like to acknowledge the participating swinger websites during our 2011
and 2018 survey. Furthermore, we would like to thank Editage (www.editage.com) for
English language editing.

138
References

1. Spauwen LW, Niekamp AM, Hoebe CJPA, et al. Drug use, sexual risk behaviour and sexually
transmitted infections among swingers: a cross-sectional study in The Netherlands. Sex
Transm Infect 2015;9:31-6
2. Dukers-Muijrers NH, Niekamp AM, Brouwers EE, et al. Older and swinging; need to identify
hidden and emerging risk groups at STI clinics. Sex Transm Infect 2010;86:315–17
3. Niekamp AM, Mercken AG, Hoebe CJPA, et al. A sexual affiliation network of swingers,
heterosexuals practicing risk behaviours that potentiate the spread of sexually transmitted
infections: a two-mode approach. Social Networks 2013;35:223–36
4. Gorbach PM, Stoner BP, Aral SO, et al. “It takes a village”: understanding concurrent sexual
partnerships in Seattle, Washington. Sex Transm Dis 2002;29:453–62
5. Dukers-Muijrers NHTM, van Rooijen MS, Hogewoning A, et al. Incidence of repeat testing and
diagnoses of Chlamydia trachomatis and Neisseria gonorrhoea in swingers, homosexual and
heterosexual men and women at two large Dutch STI clinics, 2006-2013. Sex Transm Infect
2017;93:383-389
6. Visser M, Van Aar F, van Oeffelen AAM, et al. Sexually transmitted infections including HIV,
in the Netherlands in 2016. RIVM 2017 7
7. Platteau T, van Lankveld J, Ooms L, et al. Sexual Behavior and Sexually Transmitted Infections
Among Swingers: Results From an Online Survey in Belgium. J Sex Marital Ther 2017;43:709-
719
8. Spauwen LWL, Niekamp AM, Hoebe CJPA, et al. Do swingers self-identify as swingers when
attending STI services for testing? A cross-sectional study. Sex Transm Infect 2018
9. Westmaas AH1, Kok G, Vriens P, Götz H, Richardus JH, Voeten H. Determinants of intention
to get tested for STI/HIV among the Surinamese and Antilleans in the Netherlands: results of
an online survey. BMC Public Health 2012;12:961
10. Martin-Smith HA, Okpo EA, Bull ER. Exploring psychosocial predictors of STI testing in
University students. BMC Public Health 2018;18:664
11. Tyson M, Covey J, Rosenthal HE. Theory of planned behavior interventions for reducing
heterosexual risk behaviors: A meta-analysis. Health Psychol 2014;33:1454-67
12. Cunningham NJ, Beymer M, Javanbakht M, Shover CL, Bolan RK. Concordance Between Self-
Reported STI History and Biomedical Results Among Men Who Have Sex With Men in Los
Angeles, California. Sex Transm Infect 2017;93::514-519
13. O’Byrne P, Watts JA. Exploring sexual networks: a pilot study of swingers’ sexual behaviour
and health-care-seeking practices. Can J Nurs Res 2011;43:80-97
14. Wolfers ME, Kok G, Mackenbach JP, de Zwart O. Correlates of STI testing among vocational
school students in the Netherlands. BMC Public Health 2010;10:725
15. Wombacher K, Dai M, Matig JJ, Harrington NG. Using the integrative model of behavioral
prediction to understand college students’ STI testing beliefs, intentions, and behaviors. J
Am Coll Health 2018t;66:674-682
16. Scheim AI, Travers R. Barriers and facilitators to HIV and sexually transmitted infections
testing for gay, bisexual, and other transgender men who have sex with men. AIDS Care
2017;29:990-995
17. Heijman T, Zuure F, Stolte I, Davidovich U. Motives and barriers to safer sex and regular STI
testing among MSM soon after HIV diagnosis. BMC Infect Dis 2017;17:194

139
18. Den Heijer CD, van Liere GA, Hoebe CJ, van Bergen JE, Cals JW, Stals FS, Dukers-Muijrers NH.
Who tests whom? A comprehensive overview of Chlamydia trachomatis test practices in a
Dutch region among different STI care providers for urogenital, anorectal and oropharyngeal
sites in young people: a cross-sectional study. Sex Transm Infect 2016;92:211-7
19. Peters RP, Verweij SP, Nijsten N, Ouburg S, Mutsaers J, Jansen CL, van Leeuwen AP, Morré SA.
Evaluation of sexual history-based screening of anatomic sites for chlamydia trachomatis and
neisseria gonorrhoeae infection in men having sex with men in routine practice. BMC Infect
Dis 2011;11:203
20. Trienekens SC, van den Broek IV, Donker GA, van Bergen JE, van der Sande MA. Consultations
for sexually transmitted infections in the general practice in the Netherlands: an opportunity
to improve STI/HIV testing. BMJ Open 2013;3:e003687
21. Joore IK, Reukers DF, Donker GA, van Sighem AI, Op de Coul EL, Prins JM, Geerlings SE,
Barth RE, van Bergen JE, van den Broek IV. Missed opportunities to offer HIV tests to high-risk
groups during general practitioners’ STI-related consultations: an observational study. BMJ
Open 2016;6:e009194
22. Joore IK, van Roosmalen SL, van Bergen JE, van Dijk N. General practitioners’ barriers and
facilitators towards new provider-initiated HIV testing strategies: a qualitative study. Int J
STD AIDS 2017;28:459-466
23. Wijers JNAP, van Liere GAFS, Hoebe CJPA, Cals JWL, Wolffs PFG, Dukers-Muijrers NHTM.
Test of cure, retesting and extragenital testing practices for Chlamydia trachomatis and
Neisseria gonorrhoeae among general practitioners in different socioeconomic status areas:
A retrospective cohort study, 2011-2016. PLoS One 2018;13:e0194351
24. Den Daas C, Sukel B, Bos H, van den Broek I. Evaluation and enumeration of online test
providers for sexually transmitted infections, specifically chlamydia, in the Netherlands. Sex
Transm Infect 2019;95:380-385
25. Fajardo-Bernal L, Aponte-Gonzalez J, Vigil P, Angel-Müller E, Rincon C, Gaitán HG,
Low N. Home-based versus clinic-based specimen collection in the management of
Chlamydia trachomatis and Neisseria gonorrhoeae infections. Cochrane Database Syst Rev
2015;29:CD011317
26. Gilbert M, Thomson K, Salway T, Haag D, Grennan T, Fairley CK, Buchner C, Krajden M,
Kendall P, Shoveller J, Ogilvie G. Differences in experiences of barriers to STI testing between
clients of the internet-based diagnostic testing service GetCheckedOnline.com and an STI
clinic in Vancouver, Canada. Sex Transm Infect 2019;95:151-156

140
Chapter 8
General discussion
Introduction

Sexually transmitted infections (STI) continue to be a major public health concern

worldwide, urging the STI clinics of the Public Health Services in the Netherlands to
optimize STI care and control by monitoring and evaluating their policy regarding STI
risk groups. This thesis aims to contribute to optimal STI care, STI control and STI policy,
from a STI clinic point of view by studying the following three foci; 1. Optimizing STI
care in groups who are currently eligible for STI clinic care; young heterosexuals under
the age of 25 years, and men who have sex with men (MSM), 2. Reaching groups that are
eligible, but possibly underrepresented at the STI clinics; ethnic minority clients and
self-employed sex workers, and 3. Considering groups that are not eligible for STI clinic
care anymore owing to Dutch policy; clients of female sex workers and swingers.
By studying these groups, our understanding of the suitability of our STI clinic
care and control in comparison to the risk- and test behaviour and STI positivity of
these groups is improved, resulting in recommendations for future policy and therefore
optimizing care and control of STI.

1. Optimizing STI care in current eligible STI risk groups: young heterosexuals and 8
men who have sex with men
Young people and MSM were identified as STI risk groups since the opening of the STI
clinics. Consequently, these groups have had access to free of charge, and anonymous
STI clinic care, and have always been well represented among all STI clinic attendees [1].
Our studies described in chapter 2 and 3 focus on STI care among young heterosexuals
and MSM, identifying subgroups among them who are more likely to be STI positive,
and therefore, have more impact on the rise of STI than the rest of the group. Focusing
on these high impact subpopulations may yield beneficial effects in containing the STI
epidemic among the entire population.
Although regular testing is not advised for all young people, retesting within four to
six months after a chlamydia- or gonorrhoea diagnosis, is advised by national guidelines
[2]. Our study shows that retesting young heterosexuals who are chlamydia-positive is
indeed effective, given the high reinfection rates upon retesting (20.4% versus the overall
chlamydia positivity rate of 15.9% amongst all eligible young people attending an STI
clinic during our study period). Our finding of high reinfection rates is in line with other
studies conducted among young people who were chlamydia and/or gonorrhoea positive
at initial consultation, with varying reinfection rates between 18% and 22% [3-5].
According to Dutch guidelines, MSM are advised to test at least twice a year, and
high-risk MSM (e.g. HIV-positive MSM, MSM who are sex workers and MSM who take pre-
exposure prophylaxis (PrEP) to reduce risks of infection with Human Immunodeficiency
Virus (HIV)), are advised to test four times a year [2]. Our study findings show that a little

145
under 60% of the included MSM were infrequent testers, meaning that their mean test
interval was 6 months or longer. Of these infrequently testing MSM, MSM who were
ever diagnosed with HIV were more likely to have an STI diagnosis upon testing. With
our study set up, we tried to approximate an actual STI test frequency, but the design of
this study makes it difficult to compare our results with other studies. In a recent study
performed in the United Kingdom, adherence to STI test guidelines of MSM was below
national recommendations, irrespective of HIV status [6]. Another study found that high
risk MSM generally had higher testing rates, but other MSM, such as students, had lower
testing rates, suggesting the need for further ways to enhance testing in specific MSM
communities [7]. Two recent Dutch studies assessing characteristics of clients who were
frequently tested, and repeatedly infected with chlamydia or gonorrhoea, established
that MSM and HIV positive clients were mostly not retested after a gonorrhoea infection,
and subsequently, reinfections were missed [8]. Clients who were frequently tested and
repeatedly infected with chlamydia. were clients aged < 25 years, and clients coinfected
with HIV or gonorrhoea [9]. In conclusion, STI disproportionately affect MSM, with
marked increases in most STIs in recent years, making testing and retesting, especially
of HIV positive MSM, a necessity to track and trace STI early, in order to prevent further
spread among the entire MSM population. STI testing and retesting of MSM is still
suboptimal in the Netherlands, and the STI clinics are tasked to improve testing uptake
among MSM, but the financial support for this task is limited.
Retesting STI positive young people as well as STI positive MSM is also advised in
various other international studies and guidelines [10-14]. As both our studies show,
young heterosexuals and MSM seem to utilize STI clinics, when STI related symptoms
arise, or when they are notified by a partner, but the retesting advice seems to be largely
ignored by STI positive clients.
One way to increase retesting uptake is to send a text message reminder. Our
study shows that sending a text message reminder yielded higher retest rates (31%),
in comparison with the historical control group (9%), consisting of young clients
diagnosed with chlamydia, who retested under their own initiative within 5 to 8 months
after initial chlamydia diagnosis. Sending a text message reminder to increase retest
uptake is also found in many other studies [15-19]. Furthermore, a British study found
that sending a text message containing the web link of an e-STI testing and results
service, almost doubled testing, compared with a group that received a text message
with the link of a website, simply listing the locations, contact details, and websites
of seven local sexual health clinics [20]. Another step to increase retest uptake is by
offering a home-test for retesting, studies have established that retest rates were higher
with a home-test compared with a clinic-test [21-23]. ‘Network testing’, i.e., providing
incentivized testing to participants and up to six referred individuals within their social
network, has also shown to increase testing uptake among high risk MSM [24].

146
 Our studies did not measure whether young heterosexuals and/or MSM visit any
other healthcare provider than an STI clinic, for STI testing. Considering that roughly
half to two-third of patients go to the general practitioner (GP) for STI testing, and
STI related questions, it is likely that a proportion of the retesting is carried out by
the GP [1,25-28]. However, there is no standard exchange of information between the
GPs and the STI clinics, due to physician-patient privilege, and patient confidentiality.
Furthermore, most HIV positive MSM are in the care of HIV treatment centers, where
they are mostly not routinely tested for STI, except for annual syphilis and hepatitis C
screening, and only conduct STI testing, when STI related symptoms arise.
Though testing and retesting is advised for STI positive young people and MSM,
and especially HIV positive MSM, it is poorly adhered to. The STI clinics could increase
STI testing uptake, by sending text message reminders for retesting, as well as more
novel initiatives to increase retesting, such as internet-accessed STI testing and results,
network testing and home-collection of STI tests [20,21,24,29] .

2. Reaching underrepresented STI risk groups: ethnic minorities and self-employed

sex workers
One of the core tasks of the STI clinics is to provide sexual healthcare including STI 8
testing for vulnerable and/or hard to reach groups, with a high risk of being infected
with an STI, such as ethnic minorities and sex workers. Our studies regarding ethnic
minority clients (chapter 4) and self-employed sex workers (chapter 5), assessed the
attendance at the STI clinics for both groups, and determines whether their sexual risk
behaviour, and STI positivity rates yields an urgency to improve and develop strategies
for STI clinics to reach them.
Our study among ethnic minority clients shows that this group indeed visits the STI
clinics less often than native Dutch clients: only 7% of all clients were ethnic minority
clients during our study period (2011-2013). Furthermore, the consultation rate of the
ethnic minority population is lower with 8.5 per 1000 person years, compared with
22.5 per 1000 person years among native Dutch, while chlamydia positivity rates were
higher for the majority of ethnic minority clients, compared with native Dutch clients.
The reasons for hampered healthcare seeking behaviour in ethnic minority people
are multifold: fear and distrust of healthcare institutions may lead to barriers seeking
healthcare, as well as social and cultural discrimination, language barriers, provider
bias (or the perception that these may exist), as well as affordability (e.g., travel cost to
the clinic, costs of healthcare itself ) [30-34].
Another possible explanation of the lower STI clinic consultation rates of ethnic
minorities, is that ethnic minorities visit a GP more often than an STI clinic for STI
testing, as was shown by a Dutch study where all ethnic minority patients visit a GP
as often as, or more often than native Dutch, except for Turkish people [26]. However,

147
these study findings were contradicted by another Dutch study that showed that the
age and ethnicity of patients who consulted a GP for STI testing were comparable with
those of the clients attending an STI clinic [27].
The STI clinics in the Netherlands do not have an optimal strategy to reach ethnic
minorities. Some STI clinics have an STI test facility situated at asylum centers, thereby
providing STI consultations for only a small proportion of the entire Dutch ethnic
minority population. Efforts to increase testing uptake among ethnic minority people
are described in a British study performed among young, multi-ethnic students, in
which efforts were made to increase STI testing uptake by offering STI testing in a
non-medical setting, offering a small financial incentive to be tested for STI and by
increasing knowledge about STI [35]. A German study established that particular
knowledge gaps about STI were more prevalent in African ethnic minorities, making
it evident that filling this knowledge gap could increase STI testing uptake [36].
For sex workers, more or less the same reasons for hampered healthcare seeking
behaviour apply, as well as Dutch legislation on sex work, forcing sex workers to
disclose themselves to governmental institutions. Often, the STI clinics of the municipal
Public Health Services are perceived as a controlling institution, thus acting as an STI
test barrier for sex workers [37-39].
Our study on self-employed sex workers shows that the participating male and
female self-employed sex workers do not always use a condom during work; about
one-third of female and male self-employed sex workers always used a condom whilst
giving oral sex, two-thirds with vaginal sex and half of female sex workers and two-
third of male sex workers always used a condom during with receptive anal sex, which
is the most high risk sex, in terms of becoming infected with HIV and other STI [40-42].
Other studies also established inconsistent condom use among sex workers [43-45].
Furthermore, our study shows that one-third of the participating self-employed sex
workers did not test for STI in the past year, despite the fact that Dutch guidelines
advise a test frequency for male and transgender sex workers of four times a year,
and twice a year for female sex workers [2]. Reaching sex workers for STI testing is
also difficult in many other countries and the World Health Organization highlights
the importance of focusing on inequalities and populations left behind, including
sex workers [46-49].
Initiatives to increase STI testing among sex workers include STI clinic visits
to locations where mostly female sex workers work, and testing them for STI on a
voluntarily basis. These outreach activities take a great deal of effort, financial means,
and time, and are not always a priority within an STI clinic. Many STI clinics perform
internet fieldwork on websites where sex workers advertise, making it possible for
them to chat with an STI clinic professional, and occasionally being made aware of a a
walk-in STI testing facility at the STI clinic, specifically for sex workers. A recent Dutch

148
study performed among migrant sex workers highlighted that having a relationship of
trust with healthcare providers, can also facilitate HIV testing [50]. Other possible ways
to increase testing among sex workers are HIV self-testing, and the use of mobile test
facilities (with a peer guiding sex workers to the facility) [51-53].
In conclusion, ethnic minority clients are underrepresented at the STI clinics,
compared with native Dutch clients, and with one third of self-employed sex workers
not testing for STI in the past year, while STI prevalences and potential transmission
determinants (such as a high number of partners), remain in place, they should test
for STI more often too. Both studies show that there are improvements that can be
made in reaching ethnic minorities and sex workers, thereby optimizing STI testing
and treatment, and thus STI control among ethnic minorities and sex workers.

3. Considering non-eligible STI risk groups: clients of sex workers and swingers
In 2015, a policy change regarding STI risk groups, and their eligibility for STI clinic
care, was implemented. As a consequence of this policy change, clients who visit a sex
worker, and clients who have multiple partners (3 or more in the last 6 months), were
no longer considered an STI risk group eligible for free of charge, and anonymous STI
testing at the STI clinics. As the majority of swingers mostly had the eligibility criterion 8
of having had 3 or more partners in the last 6 months as their sole risk factor, they were
excluded from STI clinic care from 2015 onwards.
In chapter 6 we established an association between having sex with a sex workers
in cross-border Germany, and being STI positive. STI positivity upon testing was 10%
for clients of sex workers who visited a sex worker in the Netherlands, 16% for clients
who visited a sex worker in cross-border Germany, and 9% among clients who visited
a sex worker in any other country. Although sex tourism (travel planned specifically
for the purpose of sex), especially to Asian countries, is widely known in literature,
cross-border sex tourism in Europe, is less studied [54-56]. A possible explanation
of higher rates of STI among clients of sex workers having commercial sex cross-
border, is the relatively high number of non-German female sex workers working
in German venues (88%), compared with lower numbers of non-Dutch female sex
workers working in Dutch venues (48%) [37,57]. In a German study conducted among
hard to reach female sex workers, migrant female sex workers were known to have
higher STI positivity rates compared with native German sex workers, which is in
line with other studies conducted globally [57-59]. Also, the healthcare organization
of Germany differs to the Netherlands; in the Netherlands, sex workers who work in
a centralized place (streets, brothels, windows, et cetera) are visited and voluntarily
tested for STI by the STI clinics, while in Germany, outreach activities vary per region,
making accessible healthcare a challenge in some regions, especially for hard to reach
sex worker populations [60].

149
 Research shows that interventions to reduce transmission of HIV and other STI
among sex workers and their clients are effective, but there is limited evidence for the
effectiveness of these interventions in high-income countries such as the Netherlands
and Germany [61,62]. Nevertheless, when clients of sex workers visit an STI clinic,
and certainly when having commercial sex in cross-border Germany is reported,
motivational interviewing and other condom use promotional efforts should be made
to encourage clients of sex workers to perform safe sex [63,64]. At the same time, more
effort should be made by Germany and the Netherlands to reach sex workers who are
not in contact with healthcare, and programs should focus on enhancing the ability
of sex workers to negotiate condom use, enhance wellbeing among sex workers and
empower them [65-68].
In chapter 7 we compared the sexual risk behaviour and STI testing behaviour
among swingers in 2011 and 2018. When comparing both years, we found that consistent
condom use among swingers decreased for vaginal (73% vs. 60%), oral (5% vs. 2%),
and anal sex (85% vs. 75%). Adding to our study findings, a more recent Dutch study
found that condomless vaginal (46%) and anal sex (22%), was higher in drug-using
swingers than in non-drug-using swingers (34% for condomless vaginal sex and 13%
for condomless anal sex) [69]. A recent Swedish study found much lower consistent
condom use rates compared with our study; 47% of swinger-women and 39% of swinger-
men always used a condom during vaginal sex [70]. These differing results might be
explained by a dissimilar study set up; our study consisted of an online Internet survey,
while the researchers in the Swedish study made visits to two swinger clubs.
Regarding STI testing, our study showed that approximately 65% of the participating
swingers in both study years reported STI testing in the past year, which is encouraging,
given the policy change in 2015.
In conclusion, changing public health policy regarding clients of sex workers and
swingers and to enable them access to the STI clinics again is not necessary at this time,
because of their low STI prevalence and the fact that the majority of both groups still
test for STI regularly. However, continued efforts to bring preventive messages across
to both groups is required, especially to clients who visit a sex worker cross-border,
and to swingers, given the decrease in condom use and the increase of STI positivity
among swingers.

150
Results of this thesis in the context of the Dutch national
action plan

In 2018, the national action plan of STIs, HIV and sexual health 2017-2022 was published
[71]. This action plan presents an integral public health approach for the coming five
years and has six cornerstones; sexuality education, surveillance and monitoring, and
specific objectives for STI, HIV, unwanted pregnancies, and sexual violence, see below
[71].

The six cornerstones of the national action plan:

Overarching cornerstones:
1. Monitoring and surveillance: overarching cornerstone aiming to gain insight
in the number of STI, unwanted pregnancies, and sexual violence. Furthermore,
aiming to monitor the implementation and impact of interventions aiming to
reduce STI, unwanted pregnancies, sexual violence, and providing a foundation
for prevention and policy.
2. Promoting a healthy sexual life (based on sexuality education): a second
overarching cornerstone aiming to establish a healthy and safe sexual development, 8
by providing information, education, prevention, observing problems, and
providing support.

Specific targets for STI, HIV, unwanted pregnancies and sexual violence, especially for vulnerable
groups:
3. Prevention and control of STI: a cornerstone aiming to develop an effective
strategy to reduce the long term complications of chlamydia, halve the number
of new gonorrhoea cases and syphilis cases, and decrease the number of acute
hepatitis B and C infections to zero. Also part of this cornerstone is promoting the
acceptation of chronic STI, and sexual diversity by society.
4. Prevention and control of HIV: a cornerstone that aims for no AIDS (acquired
immunodeficiency syndrome) deaths, halve the number of new HIV diagnoses
(95% knows their HIV status, 95% of people living with HIV are under treatment,
95% has an undetectable viral load and 90% of people living with HIV have a good
quality of life: i.e., reduction of stigma and/or discrimination), and normalizing
testing for HIV and treatment for HIV.
5. Prevention of unwanted pregnancies: a cornerstone aiming at the availability of
information, counseling, and obtaining birth control provided at a low threshold,
especially for hard to reach/vulnerable groups, which yields a reduction in
unwanted pregnancies.

151
6. Prevention of sexual violence: a cornerstone aiming to promote respectful
social and sexual interactions within all educational levels, awareness of the
effects of gender stereotype norms, and interventions for groups at risk for
sexual violence

Our thesis adds to this national action plan in the following ways;

1. Optimizing STI care in current eligible STI risk groups: young heterosexuals
and men who have sex with men
One of the objectives in the national action plan is to reduce long term complications
resulting from chlamydia (cornerstone 3). Our study on young heterosexuals
in chapter 2, shows that retesting chlamydia positive youngsters, is beneficial
in tracing repeat infections. There are a number of studies that have shown an
association between repeat chlamydia infections and the risk of reproductive tract
morbidity in women [72-75]. However, it is difficult to determine whether the risk
of these adverse outcomes is due to an increase in cumulative infection time or a
higher probability of progression with each subsequent infection [76].
Next to primary prevention of STI, case detection and management of STI
plays a prominent role in Dutch guidelines [2]. Despite implementing a range of
interventions (including screening young people for chlamydia) to decrease STI
in the Netherlands, the population prevalence of chlamydia (of 3-4%) did not
decrease over time [77-79]. Furthermore, these interventions also did not decrease
the number of chlamydia related complications [80-83]. Therefore, focusing on STI
risk groups, and on retesting individuals who have tested positive for an STI in the
past year, could add to a more targeted approach in battling chlamydia (and possibly
the reduction of long term complications resulting from chlamydia) [84,85].
One element of cornerstone 3 and 4 of the national action plan, is to halve
the number of new annual cases of syphilis, gonorrhoea, and HIV [71]. Regarding
HIV, the Netherlands is on track to meet that target; the annual number of newly
diagnosed HIV infections has fallen from almost 1270 new cases in 2008, to 411
new cases in 2020 [86]. Regarding syphilis and gonorrhoea, the Netherlands is not
on track to meet this target; the number of gonorrhoea cases remains stable (6764
cases in 2017, and 6867 cases in 2020) and there is a slight increase in syphilis cases
(1228 new cases in 2017, and 1430 new cases in 2019) [1,87]. As most cases of syphilis,
gonorrhoea and HIV are found in MSM (96% of syphilis cases, 77% of gonorrhoeae
cases and 93% of HIV cases), this risk group seems to be a logical starting point to
attempt to halve the number of cases, by testing and treating new cases early, thus
preventing further spread of STI among MSM [1]. Our study on MSM in chapter 3
concluded that frequent retesting of HIV positive MSM is beneficial, as they were

152
categorized as ‘infrequent testers’, and had a high STI positivity rate upon testing.
Finding ways to increase STI testing uptake among HIV positive MSM may, in turn,
decrease the number of cases of gonorrhoeae and syphilis.
There are a number of initiatives to increase STI testing among MSM in the
Netherlands. There is an initiative to provide HIV rapid testing carried out by lay
persons, which is appreciated because of the low threshold to test, no test costs, and the
absence of waiting lists or triaging, when booking an appointment [88]. Another Dutch
initiative is directed specifically towards non-Western migrant MSM, and uses social
network testing with HIV self-tests, and web-based support. This is designed to address
barriers to regular HIV testing, such as being seen while being tested, disclosure of
sexual identity, and the stigma related to HIV, and sexual practices [89,90]. Another
example of a Dutch initiative is that healthcare providers from an HIV treatment center,
were invited to offer free STI home-sampling kits to HIV positive MSM, which increased
testing uptake (although the return of sampling kits needed improvement, and syphilis
diagnoses were challenging with self-taken blood sampling) [91]. Although these efforts
are valuable in reaching MSM, often targeting non-disclosed MSM, they are not yet
common practice in the Netherlands.
8
2. Reaching underrepresented STI risk groups: ethnic minorities and self-employed
sex workers
The national action plan specifically directs attention towards vulnerable groups,
such as people with a low social economic status, people with a lower educational
level, ethnic minorities, non-disclosed MSM, and sex workers [71]. We studied two
of these vulnerable groups, and we concluded that ethnic minority clients were
underrepresented at the STI clinics compared with native Dutch clients, and that one-
third of the self-employed sex workers did not test for STI in the past year. Keeping
track of these hard to reach groups is therefore increasingly challenging, also partly
due to the small capacity the STI clinics have to perform outreach [71]. GPs might play
a role in testing these groups, but studies show that GPs predominantly test non-key
populations, such as women and older individuals [1,92-94]. Furthermore, the costs of
an STI test at the GP are not always fully reimbursed, due to a mandatory out-of-pocket
payment, which might prevent people from going to the GP for an STI consultation [93].
The action plan explains that these hard to reach groups need a tailored approach,
and innovative methods to reach them [71]. Such methods include outreach, internet
fieldwork, online testing facilities, home-testing, and testing at an approved commercial
testing facility (and possibly providing financial means to these providers to perform
a share of the STI care), next to STI clinic care [71]. However, there are difficulties with
commercial testing facilities, such as: unknown reliability of the facility, and quality of
the STI tests, as well as a lack of opportunity to provide sexual health education, partner

153
management and other preventive messages [95,96]. Furthermore, some of these hidden,
or hard to reach groups, may also battle with the stigma attached to sexual preference
and/or being STI positive, thus hampering health care seeking behaviour (regardless of
a tailored approach, and the use of innovative methods to reach them) [71].
In conclusion, our study shows that ethnic minority clients are underrepresented
at the STI clinics. This finding is in line with the national action plan stating they
are hard to reach, and that a tailored approach to reach them is necessary. Moreover,
mainly Dutch sex workers and sex workers with an intermediate or high educational
level prevailed in our study on self-employed sex workers. This shows that non-Dutch
sex workers, and sex workers with a lower educational level were not reached, thus
hindering further insight into this group.

3. Considering non-eligible STI risk groups: clients of sex workers and swingers
The first cornerstone of the national action plan states that various data sources
implemented in the Netherlands, provide a sound insight into the demographics and
risk factors of persons who perform an STI test. These people are predominantly STI
risk groups attending an STI clinic, a GP, or an HIV treatment center [71]. Although
these data sources give insight into STI trends among STI risk groups, we do not have a
clear insight into the STI prevalence in the overall Dutch population, and/or in groups
that are not considered an STI risk group. Though there have been studies monitoring
STI prevalence by selecting a population sample, such as the studies to assess the
seroprevalence of HIV, hepatitis B and C, and chlamydia screening studies, these
studies are cross-sectional and are therefore limited in time span [77,78]. For groups
that are not considered STI risk groups, our studies on clients of female sex workers,
and swingers, partially fill the gap by performing practice based research, together with
academic collaborative centers, to further explore questions arising from the work field.
Our study on clients of female sex workers is an example of this; based on anecdotal
reports from clients of female sex workers, indicating that unprotected commercial
sex is more easily attainable in cross-border Germany than in the Netherlands, we
researched whether these clients (who were still eligible for STI clinic care at the time),
were more likely to be STI positive than clients who visited a Dutch sex worker, or a
sex worker abroad (in any other country than Germany), which was indeed the case.
Moreover, as most swingers were no longer eligible to use an STI clinic for testing
(based on the sole eligibility criterion of "having three or more partners in the last six
months" being excluded), there was no insight into their STI risk behaviour, and their
STI testing behaviour from 2015 onwards. Our study showed that roughly two-thirds
of the participating swingers in both study years, did perform an STI test in the past
year, but that the STI testing location shifted from predominantly being the STI clinic
in 2011, to the GP and home-testing in 2018.

154
 The national action plan proposes that next to in depth research, like our studies,
there are additional ways to gain insight into STI prevalences within the Dutch
population, such as implementing a notification from other STI care providers to
the Public Health Service, of clients with a certain STI. Improving the monitoring of
STI consultations at the GP and hospitals also provide more insight, as well as using
data from laboratories, health insurance companies and pharmacies, and setting up a
registration system for commercial STI testing and home-based testing [71].
In conclusion, the current Dutch surveillance system is mainly based on monitoring
STI risk groups attending an STI clinic, which serves as a sentinel surveillance system.
However, this system is influenced by changes in eligibility of STI risk groups, which may
alter the representativeness and continuity of the data. Therefore, additional research
is necessary to maintain insight into the STI prevalence in the Dutch population, and
in groups which are not considered STI risk groups.

Strengths and limitations

A strength of this thesis is that the studies described focus on various groups at risk 8
of STI, or possibly at risk of STI, and/or groups that are hard to reach, and who are
possibly of interest to the STI clinics for public health reasons. Not only current STI
risk groups, but groups that are no longer eligible for STI clinic care are studied, thus
providing policy makers and professionals with a broader view of groups which could
be of interest.
Another strength of this thesis is that the studies are carried out by professionals
working in the field of sexual health within the Public Health Service, in synergy with
the academic collaborative centers. Professionals observe daily practice directly,
and from this form ideas about what knowledge is missing, and what topics should
be studied more thoroughly (which might be more difficult for national institutes
performing research). Furthermore, the ability to implement research findings into
daily practice is direct, as it is close at hand.
In addition, we put a great deal of effort in trying to reach self-employed sex
workers online, and we did manage to add more knowledge about self-employed sex
workers to existing literature. Although there are many studies about sex workers, the
subpopulation of self-employed sex workers remains markedly unknown, with respect
to their STI risk behaviour and STI testing behaviour.
This thesis also has limitations. One limitation derives from our studies that
used online surveys, which is the case for the studies on self-employed sex workers
and swingers. Results based on online surveys suffer from a selection bias, given the
fact that most participants in both studies were Dutch and most participants had a

155
higher educational level, of whom, the majority test for STI regularly. Additionally,
by using an online survey, both studies could be subject to a recall bias and socially
desirable answering. Although these limitations should be taken into consideration
when interpreting study findings, the studies still provide useful knowledge on both
self-employed sex workers and swingers, and challenge researchers to conduct further
studies on the topic.
A second limitation is that not all possible STI risk groups have been researched.
A possible underrepresented STI risk group at the STI clinics could be people with a
lower educational level. A recent Dutch study found an association between lower
educational levels and being STI positive [97]. Furthermore, our study group of self-
employed sex workers, only contained a small number of male sex workers who have
sex with men; a group that might also be underrepresented at the STI clinics. There are
Dutch studies showing that this group is more likely to be STI positive than male sex
workers who have sex with women [98-100].
A final limitation of this thesis is that we did not include data from the GP, HIV
treatment centers, and other STI care providers. According to surveillance data, roughly
half to two-thirds of all patients visit the GP for an STI consultation in the Netherlands
[25,93]. In 2017, the GP registered roughly 307,000 STI related episodes, while the STI
clinics together registered a little over 150,000 STI consultations [28]. Our study findings
are not generalizable to alle STI care providers, and this should be kept in mind when
reading this thesis.

Recommendations

The findings of this thesis lead to recommendations for public health practice and policy
and for future research and monitoring, which will be discussed in this paragraph.

Recommendations for public health practice and policy

Our studies described in this thesis have yielded several recommendations for public
health practice and policy. Overall, reaching groups that are underrepresented or
undergo STI testing at a suboptimal frequency remains a challenge, as does working
together with other parties, in order to reach these groups.

• As young chlamydia positive heterosexuals demonstrate a high reinfection rate

upon retesting, this group should be notified of a retesting need at six months after
initial diagnosis. Although this testing policy is implemented in the Netherlands,
sending a standardized text message to alert clients on the retest is not. Also, more
innovative methods to alert and motivate clients to retest should be explored.

156
• To reduce the occurrence of other STI in HIV positive MSM, this group should be
tested more frequently, preferably adhering to Dutch guidelines of 3-monthly STI
testing. Working together with HIV treatment centers in motivating clients to test
more frequently; possibly by offering home-based testing, and other low-threshold
testing initiatives, is recommended.
• Given the low consultation rates of ethnic minority groups, and higher chlamydia
positivity rates among them (compared with native Dutch clients), more effort
should be made to reach ethnic minorities. Examples of these efforts include
offering STI testing in a non-medical setting, using peers and social networking,
and increasing STI knowledge among ethnic minority people.
• The selection bias in our study on self-employed sex workers shows that the STI
clinics need to put more effort into building trust between the STI clinics and
self-employed sex workers. We have learned from daily practice, that reaching
out online, and subsequently providing sex workers with a mobile phone number
of (preferably) one employee of the STI clinic (known by name and face), could
improve trust in the STI clinic.
• Working together with the German counterpart of the Public Health Service, in
order to reduce the transmission of STI between cross-border sex workers, and 8
Dutch clients of sex workers, should become commonplace. In order to achieve
this, a good cross-border working relationship should be built by arranging
meetings in which policy is exchanged, and a joint strategy could be developed.

Recommendations for future research and monitoring possible STI risk groups
Groups that are considered STI risk groups are carefully monitored by the STI clinics
in the Netherlands, but this system is influenced by changes in eligibility of STI risk
groups. Furthermore, insight into groups that are not considered an STI risk group is
sparse, so too is insight into STI test barriers and facilitators of groups that are at risk
for STI.

• More research is needed to understand which socio-cognitive determinants of STI

testing play a role in ethnic minority groups, as well as research into barriers and
facilitators which influence the intent to receive an STI test. This future research
might provide us with the beginnings of a better reach of ethnic minorities.
• Our study on self-employed sex workers was subject to a selection bias. Most
participants were of Dutch origin, had a higher educational level, and had a
heterosexual work preference. Future research should focus on assessing the
occurrence of risk behaviour, and test behaviour among non-Dutch self-employed
sex workers, sex workers with a lower educational level, and male sex workers who
have sex with men during work.

157
• Similarly, the swingers who participated in our studies predominantly had an
intermediate or high level of education. Future research should focus on STI risk
behaviour, and test behaviour among swingers with a low level of education.
• More research is needed on innovative methods to increase testing and retesting:
outreach, home-based STI testing, internet-based STI testing, offering a small
incentive for STI testing, social network testing, and using peers to increase testing.
Subsequently, future research should focus on which of these methods are most
suitable for each specific group, and should be tailored to these groups.
• Periodically, in depth research and regional and national surveys, should be carried
out on groups that are thought to be at risk of STI infections. This research should
also include groups who are no longer eligible for STI care at the STI clinic, and on
groups who are thought to be underrepresented at the STI clinic. Monitoring these
groups to obtain trends in STI risk behaviour and STI testing behaviour is useful,
and could lead to a reconsideration of STI policy.

Conclusion

This thesis aims to contribute to optimal STI care, STI control, and STI policy from an
STI clinic perspective. To achieve this aim, we studied groups that are currently in STI
clinic care, groups that are presumably underrepresented at the STI clinics and groups
that are no longer eligible for STI clinic care. The outcomes of this thesis can be used
to inform and guide policy makers and STI clinic professionals, in considering policy,
and developing and selecting targeted interventions towards groups with a high STI
risk and/or a low STI test frequency, and thereby optimizing STI care overall.
First, our studies on current STI risk groups show that fine-tuning STI testing
policy, by retesting chlamydia positive heterosexuals, and increasing test frequency
among HIV positive MSM, can yield a more efficient test strategy. Second, our study on
ethnic minority clients shows they are underrepresented at the STI clinic, and our study
on self-employed sex workers shows they are hard to reach (given the selection bias
that occurred). More effort should be made to reach these groups. Finally, our studies
on non-eligible groups, shows that clients of sex workers who visit a cross-border sex
worker, are at risk of an STI, even though the overall STI positivity is low. Swingers
show a rationale self-selection for STI testing, thus reconsidering STI policy regarding
these groups is not necessary.
Given the rise of STI in the Netherlands, the limited financial resources of the STI
clinics, and the increasing demand for STI testing, continued monitoring, and in depth
research of STI risk behaviour and test behaviour in -possible- risk groups is warranted.
This should go together with research on STI test barriers and facilitators of groups at

158
risk of STI, but with a low, or suboptimal test frequency. Not only should this research
be conducted by national institutes, but also by professionals working within the field
of STI care, in synergy with the academic collaborative centers, as was presented in
this thesis.

159
References

1. Staritsky LE, van Aar F, Visser M, Op de Coul ELM, Heijne JCM, Götz HM, et al. Sexually
transmitted infections in the Netherlands in 2019. RIVM 2020
2. Rijksinstituut voor Volksgezondheid en Milieu. Het consult seksuele gezondheid. RIVM 2018.
Retrieved from: https://lci.rivm.nl/draaiboeken/consult-seksuele-gezondheid
3. Rose SB, Garrett SM, Stanley J, Pullon SRH. Retesting and repeat positivity following diagnosis
of Chlamydia trachomatis and Neisseria gonorrhoea in New Zealand: a retrospective cohort
study. BMC Infect Dis 2017;17:526
4. Kollars K, Plegue M, Riley M. Testing for Chlamydia Reinfection Among Adolescent Patients
in Different Clinical Settings: How Are We Doing? PRiMER. 2017;1:16
5. Dukers-Muijrers NH, Van Liere GA, Hoebe CJ. Re-screening chlamydia trachomatis positive
subjects; a comparison of practices between an STI clinic, general practitioners and
gynaecologists. Sex Transm Infect 2013;89:25-27
6. Curtis TJ, Rodger AJ, Burns F, Nardone A, Copas A, Wayal S. Patterns of sexualised recreational
drug use and its association with risk behaviours and sexual health outcomes in men who
have sex with men in London, UK: a comparison of cross-sectional studies conducted in 2013
and 2016. Sex Transm Infect 2020;96:197-203
7. Wong NS, Tang W, Han L, Best J, Zhang Y, Huang S, et al. MSM HIV testing following an online
testing intervention in China. BMC Infect Dis 2017;17:437
8. Wijers J, Hoebe C, Dukers-Muijrers N, Wolffs P, van Liere G. The Characteristics of Patients
Frequently Tested and Repeatedly Infected with Neisseria gonorrhoeae. Int J Environ Res
Public Health 2020;17:1495
9. Wijers JNAP, Dukers-Muijrers NHTM, Hoebe CJPA, Wolffs PFG, van Liere GAFS. The
characteristics of patients frequently tested and repeatedly infected with Chlamydia
trachomatis in Southwest Limburg, the Netherlands. BMC Public Health 2020;20:1239
10. Centers for Disease Control and Prevention. Sexually Transmitted Infections Treatment
Guidelines, 2021. CDC 2021. Retrieved from: https://www.cdc.gov/std/treatment-guidelines/
STI-Guidelines-2021.pdf
11. European Centre for Disease Prevention and Control. Technologies, strategies and approaches
for testing populations at risk of sexually transmitted infections in the EU/EEA. ECDC2021.
Retrieved from: https://www.ecdc.europa.eu/sites/default/files/documents/Technologies-
strategies-approaches-testing-populations-at-risk-for-STIs.pdf
12. Looker KJ, Buitendam E, Woodhall SC, Hollis E, Ong KJ, Saunders JM, Dunbar K, Turner
KME. Economic evaluation of the cost of different methods of retesting chlamydia positive
individuals in England. BMJ Open 2019;9:e024828
13. Public Health England. Consultation Report: Routine offer of re-test to young adults testing
positive for chlamydia (Consultation findings and evidence summary). PHE 2016. Retrieved
from: https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/508364/
NCSP_Report_Consultation_on_Re-testing_of_Positive_Chlamydia_Cases_August_2013_
FINAL.pdf
14. Nwokolo NC, Dragovic B, Patel S, Tong CY, Barker G, Radcliffe K. 2015 UK national guideline
for the management of infection with Chlamydia trachomatis. Int J STD AIDS 2016;27:251-67

160
15. Bourne C, Knight V, Guy R, et al. Short message service reminder intervention doubles sexually
transmitted infection? HIV re-testing rates among men who have sex with men. Sex Transm
Infect 2011;87:229-231
16. Guy R, Wand H, Knight V, et al. SMS reminders improve re-screening in woman and heterosexual
men with chlamydia infection at Sydney sexual health centre: a before-and-after study. Sex
Transm Infect 2013;89:11-15
17. Downing, SG1, Cashman, C, McNamee H, et al. Increasing chlamydia test of re-infection rates
using SMS reminders and incentives. Sex Transm Infect 2013;80:16-9
18. Muhindo R, Mujugira A, Castelnuovo B, Sewankambo NK, Parkes-Ratanshi R, Kiguli J, et al.
Text message reminders and peer education increase HIV and Syphilis testing among female
sex workers: a pilot quasi-experimental study in Uganda. BMC Health Serv Res 2021;21:43
19. Nyatsanza F, McSorley J, Murphy S, Brook G. ‘It’s all in the message’: the utility of personalised
short message service (SMS) texts to remind patients at higher risk of STIs and HIV to reattend
for testing-a repeat before and after study. Sex Transm Infect 2016;92:393-5
20. Wilson E, Leyrat C, Baraitser P, Free C. Does internet-accessed STI (e-STI) testing increase
testing uptake for chlamydia and other STIs among a young population who have never tested?
Secondary analyses of data from a randomised controlled trial. Sex Transm Infect 2019;95:569-
574
21. Gotz HM, Wolfers MEG, Luijendijk A, et al. Retesting for genital chlamydia trachomatis among
visitors of a sexually transmitted infections clinic: randomized intervention trial of home-
versus clinic-based recall. BMC Infectious Diseases 2013;13:239 8
22. Chow K, Edi R, Gin G, Morris SR. Attitudes of women participating in a clinical trial on point-
of-care testing and home testing for STIs. Int J STD AIDS 2020;31:1352-1358
23. Banerjee P, Thorley N, Radcliffe K. A service evaluation comparing home-based testing to
clinic-based testing for Chlamydia and gonorrhoea in Birmingham and Solihull. Int J STD AIDS
2018;29:974-979
24. Issema R, Songster T, Edgar M, Davis B, Lee T, Harris J, et al. HIV-Positive Individuals Who
Report Being in Care Are Less Likely to Be Co-Infected With an STI; an Analysis of “Network
Testing,” A Service Program Offering HIV and STI Testing Services to Individual at Risk for HIV.
Open Forum Infect Dis 2018;5(suppl_1):S671-S672
25. Den Heijer CD, van Liere GA, Hoebe CJ, van Bergen JE, Cals JW, Stals FS, Dukers-Muijrers NH.
Who tests whom? A comprehensive overview of Chlamydia trachomatis test practices in a Dutch
region among different STI care providers for urogenital, anorectal and oropharyngeal sites in
young people: a cross-sectional study. Sex Transm Infect 2016;92:211-7
26. Woestenberg PJ, van Oeffelen AA, Stirbu-Wagener I, van Benthem BH, van Bergen JE, van den
Broek IV. Comparison of STI-related consultations among ethnic groups in the Netherlands: an
epidemiologic study using electronic records from general practices. BMC Fam Pract 2015;16:70
27. Trienekens SC, van den Broek IV, Donker GA, van Bergen JE, van der Sande MA. Consultations
for sexually transmitted infections in the general practice in the Netherlands: an opportunity
to improve STI/HIV testing. BMJ Open 2013;3:e003687
28. Slurink IAL, Van Aar F, Op de Coul ELM, Heijne JCM, Van Wees DA, Hoenderboom BM, et al.
Sexually transmitted infections in the Netherlands in 2018. RIVM 2019
29. Van Rooijen MS, Koekenbier RH, Hendriks A, de Vries HJ, van Leeuwen P, van Veen MG.
Young Low-Risk Heterosexual Clients Prefer a Chlamydia Home Collection Test to a Sexually
Transmitted Infection Clinic Visit in Amsterdam, the Netherlands, A Cross-Sectional Study. Sex
Transm Dis 2016;43:710-716

161
30. Healey JF, Stepnick A, O’Brien E. Race, ethnicity, gender, & class : the sociology of group conflict
and change. Thousand Oaks, California 2018. ISBN 9781506346946
31. Centers for Disease Control and Prevention. STIs in racial and ethnic minorities. ECDC; 2018.
Retrieved from: https://www.cdc.gov/STI/stats17/minorities.htm
32. Berk ML, Schur CL. The effect of fear on access to care among undocumented Latino immigrants.
J Immigr Health 2001;3:151–156
33. Pemberton S, Phillimore J, Bradby H, Padilla B, Lopes J, Samerski S, et al. Access to healthcare
in superdiverse neighbourhoods. Health Place 2019;55:128–35
34. Wasserman J, Palmer RC, Gomez MM, Berzon R, Ibrahim SA, Ayanian JZ. Advancing Health
Services Research to Eliminate Health Care Disparities. American Journal of Public Health
2019;109:S64–S69
35. Fleming C, Drennan VM, Kerry-Barnard S, Reid F, Adams EJ, Sadiq ST, et al. Understanding the
acceptability, barriers and facilitators for chlamydia and gonorrhoea screening in technical
colleges: qualitative process evaluation of the “Test n Treat” trial. BMC Public Health 2020;20:1212
36. Koschollek C, Kuehne A, Müllerschön J, Amoah S, Batemona-Abeke H, Dela Bursi T, et al.
Knowledge, information needs and behavior regarding HIV and sexually transmitted infections
among migrants from sub-Saharan Africa living in Germany: Results of a participatory health
research survey. PLoS One 2020;15:e0227178
37. Kloek M, Dijkstra M. Sekswerk en geweld in Nederland. Aidsfonds 2018
38. Albright E, D’Adamo K. Decreasing Human Trafficking through Sex Work Decriminalization.
AMA J Ethics 2017;19:122-126
39. Campbell R, Sanders T, Scoular J, Pitcher J, Cunningham S. Risking safety and rights: online sex
work, crimes and ‘blended safety repertoires’. Br J Sociol 2019;70:1539-1560
40. Elmes J, Silhol R, Hess KL, Gedge LM, Nordsletten A, Staunton R, et al. Receptive anal sex
contributes substantially to heterosexually acquired HIV infections among at-risk women in
twenty US cities: Results from a modelling analysis. Am J Reprod Immunol 2020;84:e13263
41. Meng X, Zou H, Fan S, Zheng B, Zhang L, Dai X, et al. Relative Risk for HIV Infection Among
Men Who Have Sex with Men Engaging in Different Roles in Anal Sex: A Systematic Review and
Meta-analysis on Global Data. AIDS Behav 2015 May;19:882-9
42. Rodger AJ, Cambiano V, Bruun T, Vernazza P, Collins S, van Lunzen J, et al. Sexual Activity
Without Condoms and Risk of HIV Transmission in Serodifferent Couples When the HIV-
Positive Partner Is Using Suppressive Antiretroviral Therapy. JAMA 2016;316:171-81
43. Magalhães RLB, Sousa LRM, Gir E, Galvão MTG, Oliveira VMC, Reis RK. Factors associated to
inconsistent condom use among sex workers. Rev Lat Am Enfermagem 2019;27:e3226
44. Amirkhanian YA. Review of HIV vulnerability and condom use in central and eastern Europe.
Sex Health 2012;9:34-43
45. Tracas A, Bazzi AR, Artamonova I, Rangel MG, Staines H, Ulibarri MD. Changes in Condom Use
Over Time Among Female Sex Workers and Their Male Noncommercial Partners and Clients.
AIDS Educ Prev 2016;28:312-24
46. World Health Organization. Global progress report on HIV, viral hepatitis and sexually
transmitted infections, 2021. Accountability for the global health sector strategies 2016–2021:
actions for impact. Geneva: WHO; 2021. Licence: CC BY-NC-SA 3.0 IGO
47. Lillie TA, Persaud NE, DiCarlo MC, Gashobotse D, Kamali DR, Cheron M, et al Reaching the
unreached: Performance of an enhanced peer outreach approach to identify new HIV cases
among female sex workers and men who have sex with men in HIV programs in West and
Central Africa. PLoS One 2019;14:e0213743

162
48. Campos PE, Buffardi AL, Cárcamo CP, García PJ, Buendia C, Chiappe M, et al. Reaching the
unreachable: providing STI control services to female sex workers via mobile team outreach.
PLoS One 2013;8:e81041
49. McGrath-Lone L, Marsh K, Hughes G, Ward H. The sexual health of female sex workers
compared with other women in England: analysis of cross-sectional data from genitourinary
medicine clinics. Sex Transm Infect 2014;90:344-50
50. Tokar A, Osborne J, Hengeveld R, Lazarus JV, Broerse JEW. ‘I don’t want anyone to know’:
Experiences of obtaining access to HIV testing by Eastern European, non-European Union
sex workers in Amsterdam, the Netherlands. PLoS One 2020;15:e0234551
51. Makhakhe NF, Meyer-Weitz A, Struthers H, McIntyre J. The role of health and advocacy
organisations in assisting female sex workers to gain access to health care in South Africa.
BMC Health Serv Res 2019;19:746
52. Shava E, Manyake K, Mdluli C, Maribe K, Monnapula N, Nkomo B, et al. Acceptability of oral
HIV self-testing among female sex workers in Gaborone, Botswana. PLoS One 2020;15:e0236052
53. Napierala S, Desmond NA, Kumwenda MK, Tumushime M, Sibanda EL, Indravudh P, et al.
HIV self-testing services for female sex workers, Malawi and Zimbabwe. Bull World Health
Organ 2019;97:764-776
54. Lu TS, Holmes A, Noone C, Flaherty GT. Sun, sea and sex: a review of the sex tourism literature.
Trop Dis Travel Med Vaccines 2020;6:24
55. Avery AK, Zenilman JM. Sexually Transmitted Diseases and Travel: From Boudoir to Bordello.
Microbiol Spectr 2015;3 8
56. Bishop S, Limmer M. Negotiating the Edge: The Rationalization of Sexual Risk Taking Among
Western Male Sex Tourists to Thailand. J Sex Res 2018 Sep;55:871-879
57. Jansen K. Prävalenz von Chlamydien, gonorrhoe und Trichomonaden bei „Schwer
erreichbaren“ Sexarbeiterinnen in Berlin, Hamburg und NRW. RKI HIV&more 4, 2014
58. Platt L, Grenfell P, Fletcher A, Sorhaindo A, Jolley E, Rhodes T, Bonell C. Systematic review
examining differences in HIV, sexually transmitted infections and health-related harms
between migrant and non-migrant female sex workers. Sex Transm Infect 2013;89:311-9
59. McBride B, Shannon K, Strathdee SA, Goldenberg SM. Structural determinants of HIV/
STI prevalence, HIV/STI/sexual and reproductive health access, and condom use among
immigrant sex workers globally. AIDS 2021;35:1461-1477
60. Castañeda H. Structural vulnerability and access to medical care among migrant street-based
male sex workers in Germany. Soc Sci Med 2013;84:94-101
61. Wariki WM, Ota E, Mori R, Koyanagi A, Hori N, Shibuya K. Behavioral interventions to reduce
the transmission of HIV infection among sex workers and their clients in low- and middle-
income countries.Cochrane Database Syst Rev 2012;2:CD005272
62. Ota E, Wariki WM, Mori R, Hori N, Shibuya K. Behavioral interventions to reduce the
transmission of HIV infection among sex workers and their clients in high-income countries.
Cochrane Database Syst Rev 2011;12:CD006045
63. Miller NH. Motivational interviewing as a prelude to coaching in healthcare settings. J
Cardiovasc Nurs 2010;25:247-51
64. Flannigan J. Promoting sexual health: practical guidance on male condom use. Nurs Stand
2007;17-23;21:51-7
65. Mahapatra B, Walia M, Patel SK, Battala M, Mukherjee S, Patel P, et al. Sustaining consistent
condom use among female sex workers by addressing their vulnerabilities and strengthening
community-led organizations in India. PLoS One 2020;15:e0235094

163
66. Free C, Roberts I, McGuire M. Sex workers’ accounts of condom use: implications for condom
production, promotion and health policy. J Fam Plann Reprod Health Care 2007;33:107-11
67. Okafor UO, Crutzen R, Aduak Y, Adebajo S, Van den Borne HW. Behavioural interventions
promoting condom use among female sex workers in sub-Saharan Africa: a systematic review.
Afr J AIDS Res 2017;16:257-268
68. Chow EP, Tung K, Tucker JD, Muessig KE, Su S, Zhang X, et al. Behavioral Interventions
Improve Condom Use and HIV Testing Uptake Among Female Sex Workers in China: A
Systematic Review and Meta-Analysis. AIDS Patient Care STDS 2015;29:454-60
69. Evers YJ, Dukers-Muijrers NHTM, Kampman CJG, van Liere GAFS, Hautvast JLA, Koedijk FDH,
et al. Prevalence of drug use during sex among swingers and perceived benefits and risks - a
cross-sectional internet survey in the Netherlands. Sex Transm Infect 2020;96:40-46
70. Andersson N, Ejnestrand J, Lidgren Y, Allard A, Boman J, Nylander E. Are Swedish swingers
a risk group for sexually transmitted infections? Int J STD AIDS 2021;32:427-434
71. David S, van Benthem B, Deug F, van Haastrecht P. Nationaal Actieplan soa, hiv en seksuele
gezondheid : 2017-2022. RIVM 2018. Retrieved from: https://www.rivm.nl/bibliotheek/
rapporten/2018-0034.pdf
72. Davies B, Turner KM, Frølund M, et al. Risk of reproductive complications following
chlamydia testing: a population-based retrospective cohort study in Denmark. Lancet Infect
Dis 2016;16:1057–64
73. Davies B, Ward H, Leung S, et al. Heterogeneity in risk of pelvic inflammatory diseases
after chlamydia infection: a population-based study in Manitoba, Canada. J Infect Dis
2014;210(suppl 2):S549–55
74. Bakken IJ, Skjeldestad FE, Lydersen S, Nordbø SA. Births and ectopic pregnancies in a large
cohort of women tested for Chlamydia trachomatis. Sex Transm Dis 2007;34:739–43
75. Den Heijer CDJ, Hoebe C, Driessen JHM, Wolffs P, van den Broek IVF, Hoenderboom BM, et
al. Chlamydia trachomatis and the risk of pelvic inflammatory disease, ectopic pregnancy,
and female infertility: a retrospective cohort study among primary care patients. Clin Infect
Dis 2019;69:1517–25
76. Haggerty CL, Gottlieb SL, Taylor BD, Low N, Xu F, Ness RB. Risk of sequelae after hlamydia
trachomatis genital infection in women. J Infect Dis 2010;201 (suppl 2):S134–55
77. Van Bergen JE, Fennema JS, van den Broek IV, Brouwers EE, de Feijter EM, Hoebe CJ, et
al. Rationale, design, and results of the first screening round of a comprehensive, register-
based, Chlamydia screening implementation programme in the Netherlands. BMC Infect Dis
2010;10:293
78. Van den Broek IV, van Bergen JE, Brouwers EE, Fennema JS, Götz HM, Hoebe CJ, et al.
Effectiveness of yearly, register based screening for chlamydia in the Netherlands: controlled
trial with randomised stepped wedge implementation. BMJ 2012;345:e4316
79. De Wit GA, Over EA, Schmid BV, van Bergen JE, van den Broek IV, van der Sande MA, et al.
Chlamydia screening is not cost-effective at low participation rates: evidence from a repeated
register-based implementation study in The Netherlands. Sex Transm Infect 2015;91:423-9
80. Hoenderboom BM, van Bergen JEAM, Dukers-Muijrers NHTM, Götz HM, Hoebe CJPA, de
Vries HJC, et al. Pregnancies and Time to Pregnancy in Women With and Without a Previous
Chlamydia trachomatis Infection. Sex Transm Dis 2020;47:739-747
81. Van Bergen JEAM, Hoenderboom BM, David S, Deug F, Heijne JCM, van Aar F, et al. Where
to go to in chlamydia control? From infection control towards infectious disease control. Sex
Transm Infect 2021;97:501-506

164
82. Price MJ, Ades AE, Soldan K, Welton NJ, Macleod J, Simms I, et al. The natural history of
Chlamydia trachomatis infection in women: a multi-parameter evidence synthesis. Health
Technol Assess 2016;20:1-250
83. Low N, Redmond S, Uusküla A, van Bergen J, Ward H, Andersen B, et al. Screening for genital
chlamydia infection. Cochrane Database Syst Rev 2016;9:CD010866.
84. Pillay J, Wingert A, MacGregor T, Gates M, Vandermeer B, Hartling L. Screening for chlamydia
and/or gonorrhea in primary health care: systematic reviews on effectiveness and patient
preferences. Syst Rev 2021;10:118
85. Coombe J, Goller J, Vaisey A, Bourne C, Sanci L, Bateson D, et al. New best practice guidance
for general practice to reduce chlamydia associated reproductive complications in women.
Aust J Gen Pract 2021;50:50–4
86. Van Sighem AI, Wit FWNM, Boyd A, Smit C, Matser A., van der Valk M. Monitoring Report
2021, Human Immunodeficiency Virus (HIV) Infection in the Netherlands. Amsterdam:
stichting hiv monitoring, 2021. Retrieved from: www.hiv-monitoring.nl
87. Visser M, van Aar F, Op de Coul ELM, Slurink IAL, van Wees DA, Hoenderboom BM, den Daas
C, et al. Sexually transmitted infections in the Netherlands in 2017. RIVM 2018
88. Krabbenborg N, Spijker R, Żakowicz AM, de Moraes M, Heijman T, de Coul EO. Community-
based HIV testing in The Netherlands: experiences of lay providers and end users at a rapid
HIV test checkpoint. AIDS Res Ther 2021;18:34
89. Den Daas C, Geerken MBR, Bal M, de Wit J, Spijker R, Op de Coul ELM; PREVENT study group.
Reducing health disparities: key factors for successful implementation of social network 8
testing with HIV self-tests among men who have sex with men with a non-western migration
background in the Netherlands. AIDS Care 2020;32:50-56
90. Op de Coul E, den Daas C, Spijker R, Heijman T, de Vos M, Götz H, et al; PREVENT
Collaborators. Web-Supported Social Network Testing for HIV Among Men Who Have Sex
With Men With a Migration Background: Protocol for a Mixed Methods Pilot Study. JMIR Res
Protoc 2020;9:e14743
91. Leenen J, Hoebe CJPA, Ackens RP, Posthouwer D, van Loo IHM, Wolffs PFG, et al. Pilot
implementation of a home-care programme with chlamydia, gonorrhoea, hepatitis B, and
syphilis self-sampling in HIV-positive men who have sex with men. BMC Infect Dis 2020;20:925
92. Bogers SJ, Twisk DE, Beckers LM, Götz HM, Meima B, Kroone M, et al. Who is providing HIV
diagnostic testing? Comparing HIV testing by general practitioners and sexual health centres
in five regions in the Netherlands, 2011-2018. Sex Transm Infect 2021;27:sextrans-2021-055109
93. Slurink I, Groen K, Gotz HM, Meima A, Kroone MM, Hogewoning AA, et al. Contribution of
general practitioners and sexual health centres to sexually transmitted infection consultations
in five Dutch regions using laboratory data of Chlamydia trachomatis testing. Int J STD AIDS
2020;31:517-525
94. De Graaf H, Van den Borne M, Nikkelen S, Twisk D, Meijer S. Seks onder je 25e, seksuele
gezondheid van jongeren in Nederland anno 2017. Soa AIDS Nederland en Rutgers 2017.
Retrieved from: https://www.seksonderje25e.nl/files/uploads/Onderzoeksboek%20Seks%20
onder%20je%2025e%202017.pdf
95. Gilbert M, Thomson K, Salway T, Haag D, Grennan T, Fairley CK, et al. Differences in
experiences of barriers to STI testing between clients of the internet-based diagnostic testing
service GetCheckedOnline.com and an STI clinic in Vancouver, Canada. Sex Transm Infect
2019;95:151-156

165
96. Den Daas C, Sukel B, Bos H, van den Broek I. Evaluation and enumeration of online test
providers for sexually transmitted infections, specifically chlamydia, in the Netherlands. Sex
Transm Infect 2019;95:380-385
97. Slurink IAL, Götz HM, van Aar F, van Benthem BH. Educational level and risk of sexually
transmitted infections among clients of Dutch sexual health centres. Int J STD AIDS
2021;32:1004-1013
98. Verhaegh-Haasnoot A, Dukers-Muijrers NH, Hoebe CJ. High burden of STI and HIV in male
sex workers working as internet escorts for men in an observational study: a hidden key
population compared with female sex workers and other men who have sex with men. BMC
Infect Dis 2015;15:291
99. Fournet N, Koedijk FD, van Leeuwen AP, van Rooijen MS, van der Sande MA, van Veen MG.
Young male sex workers are at high risk for sexually transmitted infections, a cross-sectional
study from Dutch STI clinics, the Netherlands, 2006-2012. BMC Infect Dis 2016;16:63
100. Drückler S, van Rooijen MS, de Vries HJC. Substance Use and Sexual Risk Behavior Among
Male and Transgender Women Sex Workers at the Prostitution Outreach Center in Amsterdam,
the Netherlands. Sex Transm Dis 2020;47:114-121

166
Appendices
Summary
Samenvatting
Dankwoord
About the author
List of publications
Research Data Management
PhD portfolio
Summary

Groups at risk of sexually transmitted infections (STI) are eligible for testing at the
governmental funded STI clinics, which provide free of charge and anonymous STI
testing and sexual health consultations, alongside other STI testing providers. These
STI risk groups are determined based on a high STI prevalence and incidence, and
specifically focuses on people who are hard to reach, and/or people who are vulnerable.
This thesis focuses on optimizing care and control of STI in these STI risk groups, by
studying (1) ways to increase care and control of STI among two current STI risk groups,
(2) the reach of the STI clinics and the STI risk and test behaviour of two presumably
underrepresented STI risk groups, and (3) the STI risk and test behaviour in two groups
who are not eligible for free and anonymous STI clinic care anymore.

Optimizing STI care in current STI risk groups

Chapter 2: Young heterosexual clients

A large proportion of the STI clinic clients are young heterosexual clients. Furthermore,
the majority of chlamydia infections is found in this group, compared with other STI
risk groups. In this chapter, we hypothesized that young heterosexual people with a s
chlamydia infection are prone to reinfections. After receiving a text message reminder
6 months after initial chlamydia diagnosis, 31% of the participants returned for a
retest, compared with 9% of the historical control group that did not receive a text
message reminder. Furthermore, 20% of the participants were chlamydia-positive
upon retesting, compared with an overall chlamydia positivity rate of 16% among all
young heterosexual STI clinic attendees, during the study period. These study results,
as well as similar results from other studies, have provided input for the new policy
implemented in 2015 stating that clients who are diagnosed with an STI in the previous
year, are advised to perform a retest.

Chapter 3: Men who have sex with men

Dutch guidelines advise men who have sex with men (MSM) to test at least twice a year,
and high-risk MSM (e.g., MSM living with the Human Immunodeficiency Virus (HIV),
MSM who are commercial sex workers and MSM who take pre-exposure prophylaxis
to reduce risks of HIV infection) four times a year. To assess the test frequency and the
STI positivity upon testing among MSM attending an STI clinic in the eastern part of
the Netherlands, we performed a 6-year retrospective study. We categorized MSM as
infrequent or frequent testers, depending on a mean test interval of 6 months or more,
or less than 6 months, respectively. Our main study finding shows that MSM who were

171
ever diagnosed with HIV were more often diagnosed with an STI, but did not visit an
STI clinic more frequently than known HIV negative MSM. This highlights the necessity
of encouraging MSM who are diagnosed with HIV to have STI tests more frequently.

Reaching underrepresented STI risk groups

Chapter 4: Ethnic minority clients

Ethnic minority clients mostly originate from STI endemic countries, and therefore
have a higher risk of STI than native Dutch clients. However, little is known about
their STI consultation rate at the STI clinics compared with native Dutch clients. We
assessed that only 7% of all consultations at the STI clinics from 2011 to 2013, were
performed by ethnic minority clients. The consultation rate of native Dutch clients
was 22.5 per 1000 person years, compared with 8.5 per 1000 among ethnic minority
clients, showing that ethnic minority clients are indeed underrepresented at the STI
clinics. Regarding chlamydia positivity, native Dutch clients had a 15% positivity rate,
and the highest rate was found in Antillean or Aruban clients (27%). When combining
consultation rates with chlamydia positivity, we found that clients with an Eastern
or Northern European, African, Antillean or Aruban ethnicity, had higher chlamydia
positivity rates, but lower consultation rates than native Dutch clients, warranting more
effort to reach these groups.

Chapter 5: Self-employed sex workers

Self-employed sex workers solicit clients independently from a third-party. Due to
Dutch legislation, and less centralization of self-employed sex workers, this group
remains mostly hidden from the STI clinics. We assessed their sexual risk behaviour
and STI test behaviour, by using an internet survey, in 2019-2020. The main findings
show that one-third of self-employed female and male sex workers did not always us
a condom during vaginal sex. These percentages were higher for receptive anal sex
in both female and male sex workers (46% and 36% respectively). Two-third of self-
employed sex workers reported being tested for STI in the past year, and only 12% of
female sex workers, and 8% of male sex workers reported having had an STI in the
past year. Unfortunately, there was a selection bias in our study; most participants
were native Dutch, had a higher educational level, and/or had sex with the opposite
sex during work, warranting more research on opposing groups (non-Dutch, low level
of education, and with a same sex preference during work).

172
Considering non-eligible STI risk groups

Chapter 6: Clients of female sex workers

Clients of sex workers (as a sole eligibility criterion) are no longer eligible for STI clinic
care in the Netherlands from 2015 onwards, based on low STI prevalences. There are
clients who prefer to visit a female sex worker in cross-border Germany because of
cheaper and unsafe sex offered (based on anecdotal reports), possibly placing them at
risk of STI. By using data of eight Dutch STI clinics bordering Germany, we assessed
whether having commercial cross-border sex is a risk factor for being diagnosed with
an STI. Study results show that clients predominantly visited a Dutch sex worker
(82%), 10% visited a sex worker abroad (other than Germany), and 8% made a cross-
border visit. Further analyses show that visiting a cross-border sex worker is a risk
factor of being STI positive (OR=1.7). This study shows that reconsidering STI policy
regarding clients of sex workers is of lesser need, but working together with the German
counterpart of the Public Health Service is needed, in order to establish a decrease in
STI positivity in clients and possibly in sex workers.

Chapter 7: Swingers
Until 2015, most swingers (heterosexuals who, as couples, practice mate swapping or
group sex with other couples or heterosexual singles) attended an STI clinic based on s
the sole eligibility criterion of "having had 3 or more sex partners in the last 6 months",
which was abandoned from 2015 onwards. We performed two cross-sectional studies,
using an internet survey in 2011 and 2018, to assess changes in sexual behaviour and STI
testing, before and after this policy change. We determined that condom use decreased
for vaginal (73% vs. 60%), oral (5% vs. 2%), and anal sex (85% vs. 75%). Although testing
for STI was comparable between both years (~65%), the reported STI positivity increased
from 23% to 30%. Similar to clients of sex workers, reconsidering STI policy for swingers
is not needed, but performing research on groups that possibly suffered from a policy
change needs continued attention and effort.

General discussion

With our studies on three groups, we have aimed to contribute to optimize STI care, STI
control, and STI policy, from an STI clinic perspective. The outcomes of this thesis can
be used to inform and guide policy makers and STI clinic professionals, in considering
policy, and developing and selecting targeted interventions towards groups with a high
STI risk and/or a low STI test frequency, thereby optimizing STI care overall.

173
 Given the rise of STI in the Netherlands, the limited financial resources of the
STI clinics, and the increasing demand for STI testing, continued monitoring, and in
depth research of STI risk behaviour, and test behaviour in -possible- risk groups is
warranted. This should go together with research on STI test barriers and facilitators,
of groups at risk of STI, but with a low, or suboptimal test frequency. Not only should
this research be conducted by national institutes, but also by professionals working
within the field of STI care, in synergy with the academic collaborative centers, as was
presented in this thesis.

174
Samenvatting

De Centra Seksuele Gezondheid (CSG) bieden gratis en anonieme consulten seksuele

gezondheid aan, waaronder ook het testen op seksueel overdraagbare aandoeningen
(soa). Deze consulten zijn specifiek voor de zogenaamde risicogroepen, die bepaald zijn
op basis van een hoge soa prevalentie en incidentie en vooral zijn gericht op kwetsbare
personen en/of personen die moeilijk te bereiken zijn.
In dit proefschrift worden verschillende manieren beschreven om de soa-zorg
en bestrijding rondom deze risicogroepen te optimaliseren. Daarvoor zijn er drie
verschillende groepen bestudeerd: (1) twee groepen die sinds de start van de CSG
aangemerkt zijn als risicogroep, (2) twee groepen die het CSG mogelijk te weinig
bezoeken en (3) twee groepen die de het risicogroep-label hebben verloren.

Het optimaliseren van soa-zorg in huidige risicogroepen

Hoofdstuk 2: Jonge heteroseksuele cliënten

Een groot deel van de bezoekers van het CSG zijn jonge heteroseksuele cliënten.
In vergelijking met andere risicogroepen, worden de meeste chlamydia-infecties
vastgesteld in deze groep. In dit hoofdstuk hebben we gekeken naar het aantal
herinfecties bij chlamydia positieve heteroseksuele jongeren en het effect van een
herinnerings-SMS op hertesten, die ze ontvingen 6 maanden na de chlamydia-diagnose. s
Hierop kwam 31% terug voor een hertest, terwijl in de historische controle groep (die
bestond uit jongeren die geen herinnerings-SMS kregen) 9% terug kwam voor een
hertest. Van de studiegroep die terugkwam voor een hertest had 20% opnieuw een
chlamydia-diagnose, dit is hoger dan de chlamydia positiviteit van 16% onder alle
heteroseksuele jongeren tijdens de studieperiode. Deze en vergelijkbare resultaten van
andere studies hebben ertoe geleid dat er een beleidswijziging plaatsvond in 2015; alle
cliënten die een soa hebben gehad in het afgelopen jaar wordt vanaf 2015 geadviseerd
een hertest te doen.

Hoofdstuk 3: Mannen die seks hebben met mannen

Nederlandse soa-richtlijnen adviseren mannen die seks hebben met mannen (MSM)
om zich tenminste twee keer per jaar te laten testen op soa, en hoog risico MSM zelfs
vier keer per jaar (onder hoog risico MSM vallen onder andere MSM die leven met het
humaan immunodeficiëntie-virus (HIV), MSM die pre-expositie profylaxe gebruiken
om de HIV-kans te reduceren en MSM die sekswerker zijn). In dit hoofdstuk hebben we
de testfrequentie en soa-positiviteit onderzocht bij MSM die een CSG in het oosten van
Nederland hebben bezocht, gedurende een studieperiode van 6 jaar. De testfrequentie

177
van deze MSM is vastgesteld op basis van een gemiddeld testinterval van meer of minder
dan 6 maanden. Vervolgens werden de MSM gecategoriseerd in respectievelijk laag
frequente en hoog frequente testers. Onze belangrijkste bevinding is dat HIV positieve
MSM vaker soa positief zijn bij testen, maar dat zij niet vaker testen op soa dan HIV
negatieve MSM. Onze studie toont aan dat het noodzakelijk is om HIV positieve MSM
te motiveren zich vaker te laten testen op soa.

Het bereiken van risicogroepen die het CSG mogelijk te

weinig bezoeken

Hoofdstuk 4: Cliënten met een migratieachtergrond

Cliënten met een migratieachtergrond zijn veelal afkomstig uit landen waar soa
endemisch zijn, hierdoor is de kans op soa bij deze cliënten groter dan bij cliënten
zonder een migratieachtergrond. Er is echter weinig bekend over hoe vaak mensen
met een migratieachtergrond een CSG bezoeken in vergelijking met Nederlandse
mensen. De resultaten van onze studie laten zien dat 7% van alle soa-consulten
tussen 2011 en 2013, is afgenomen door cliënten met een migratieachtergrond. Het
aantal soa-consulten van Nederlandse cliënten was 22,5 per 1000 persoonsjaren,
terwijl dit voor cliënten met een migratieachtergrond 8,5 per 1000 persoonsjaren
was. Daarnaast hebben Nederlandse cliënten een chlamydia-positiviteit van 15% en
werd de hoogste chlamydia-positiviteit vastgesteld onder Antilliaanse/Arubaanse
cliënten (27%). Bij het combineren van soa-consulten met chlamydia-positiviteit,
constateerden wij dat Oost- en Noord-Europese, Afrikaanse en Antilliaanse/
Arubaanse cliënten een hogere chlamydia-positiviteit hadden, maar een lager aantal
soa-consulten. Onze studie toont aan dat personen met een migratieachtergrond
ondervertegenwoordigd zijn bij de CSGs en dat er meer onderzoek gedaan moet
worden naar het beter bereiken van deze groep.

Hoofdstuk 5: Zelfstandig werkende sekswerkers

Zelfstandig werkende sekswerkers werken en verdienen hun geld onafhankelijk
van een derde partij. Door Nederlandse wetgeving en een minder gecentraliseerde
vindplaats van deze zelfstandig werkende sekswerkers blijft deze groep vermoedelijk
grotendeels verborgen voor de CSGs. Middels een internetvragenlijst hebben we
gekeken naar het seksueel risicogedrag en soa testgedrag van zelfstandig werkende
sekswerkers. De resultaten laten zien dat één derde van de mannelijke en vrouwelijke
sekswerkers niet altijd een condoom gebruikt tijdens vaginale seks bij cliëntcontacten.
Voor receptieve anale seks was het percentage inconsistent condoom gebruik hoger
(46% bij vrouwelijke sekswerkers en 36% bij mannelijke sekswerkers). Twee derde

178
van de sekswerkers rapporteerde dat ze een soa-test hadden gedaan in het afgelopen
jaar en 12% van de vrouwelijke sekswerkers en 8% van de mannelijke sekswerkers
rapporteerden dat ze een soa hadden gehad in het afgelopen jaar. Onze studie kende
echter een selectie van met name Nederlandse sekswerkers, sekswerkers met een
hoger opleidingsniveau en/of een heteroseksuele voorkeur tijdens werk, wat maakt
dat er meer onderzoek gedaan moet worden naar de tegenovergestelde groepen (niet-
Nederlands, lager opleidingsniveau en MSM sekswerkers).

Het beschouwen van groepen die niet meer zijn aangemerkt

als risicogroep

Hoofdstuk 6: Prostituanten
Door een lage soa-prevalentie worden ‘prostituanten’ (cliënten die seks hebben met
sekswerkers), als enige risico criterium, sinds 2015 niet meer gezien als een risicogroep.
Bij 8 CSGs die grenzen aan Duitsland kwamen signalen binnen van prostituanten die
vertelden voor seks naar Duitsland te gaan, omdat daar goedkopere en onveilige seks
verkrijgbaar is, wat kan leiden tot een verhoogd soa-risico. Met behulp van de data
van deze CSGs hebben wij onderzocht of seks in Duitsland met een sekswerker een
risicofactor is voor het oplopen van een soa. De resultaten laten zien dat de meeste
prostituanten een sekswerker in Nederland bezochten (82%), 10% bezocht een
sekswerker in een ander land (behalve Duitsland) en 8% bezocht een sekswerker in s
Duitsland. Analyses lieten vervolgens zien dat het bezoeken van een sekswerker in
Duitsland inderdaad een risicofactor is voor soa-positiviteit (OR=1.7). Gezien de lage
soa-positiviteit onder prostituanten in onze studie (10%) is een beleidswijziging voor
prostituanten niet nodig, wel moet er samengewerkt worden met Duitse partijen om
een mogelijke daling van soa onder prostituanten, en mogelijk ook onder sekswerkers,
te bewerkstelligen.

Hoofdstuk 7: Swingers
Swingers (heteroseksuele stellen die aan partnerruil of groepsseks doen met andere
stellen of heteroseksuele individuen) hadden tot 2015 toegang tot consulten bij
de CSGs, omdat zij dikwijls geschaard konden worden onder het risicocriterium "3
of meer partners gehad in het afgelopen half jaar". Vanaf 2015 was dit echter geen
risicocriterium meer. Om vast te stellen wat het risicogedrag en testgedrag van swingers
is voor en na deze beleidswijziging, hebben we een internetvragenlijst uitgezet in de
online swingers-gemeenschap in 2011 en 2018. We stelden vast dat het condoomgebruik
tussen 2011 en 2018 afgenomen was voor vaginale seks (van 73% naar 60%) en voor
anale seks (van 85% naar 75%). Hoewel het doen van een soa-test gelijk is gebleven

179
voor beide jaren (~65%), is het percentage swingers dat rapporteerde een soa te hebben
gehad toegenomen (van 23% naar 30%). Ook bij deze groep is een beleidswijziging niet
nodig, maar onderzoek blijven doen naar groepen die een beleidswijziging hebben
ondergaan verdient aandacht en inspanningen.

Discussie

Met onze studies naar verschillende groepen hebben we geprobeerd bij te dragen
aan het optimaliseren van de soa-zorg en bestrijding en aan soa-beleid vanuit het
perspectief van de CSGs. De uitkomsten van dit proefschrift kunnen gebruikt worden
door beleidsmakers en professionals die werken bij een CSG, voor het maken van
testbeleid en voor het ontwikkelen, selecteren en implementeren van interventies voor
specifieke groepen die een hoog risico op soa hebben en/of een lage test frequentie
hebben, waardoor de soa-zorg en bestrijding in het algemeen geoptimaliseerd kan
worden.
Gezien de toename van soa in Nederland, de gelimiteerde financiële middelen
van de CSGs en een toename van de testvraag, is continue monitoring en verdiepend
onderzoek naar risicogedrag, testgedrag, alsmede belemmerende en bevorderende
factoren voor testen in mogelijke risicogroepen met een suboptimale testfrequentie
erg belangrijk. Nationale instituten voeren veel van dit soort onderzoeken uit, maar
onderzoek vanuit professionals die in het veld van de seksuele gezondheid werken,
tezamen met de academische werkplaatsen, is minstens zo belangrijk, zoals ook
gepresenteerd is in dit proefschrift.

180
Dankwoord

Wat jammer dat het promotietraject erop zit! En wat mooi dat ik dit mee heb mogen
maken. Ik heb zoveel geleerd en enorm genoten. Vanaf het moment van brainstormen
over een onderzoeksopzet, de telefonische vergaderingen (ooit nog via een betaald inbel-
nummer), tot het weerleggen van soms wel heel veel commentaren van reviewers. Ik ben
dankbaar voor alles wat ik geleerd heb van alle mensen die een bijdrage hebben geleverd.

Jeannine, ik weet nog dat ons eerste onderzoek gepubliceerd was en ik je belde met de
vraag of promoveren iets voor mij zou zijn. Die vraag had ik nooit bij je neergelegd als
ik niet had gedacht dat het met jou wel moest lukken. Ik heb je altijd gewaardeerd om je
scherpe analytische opmerkingen, ondanks dat ‘soa’ niet direct je aandachtsgebied was.
Je wist altijd de vinger op de zere plek te leggen en je had bovendien ook oog voor mij
als persoon. Ik ben je nog steeds heel dankbaar voor een gesprek dat we hebben gevoerd
toen ik het even niet meer zag zitten op mijn werk, ik denk daar nog vaak aan terug.

Christian, wat een voorrecht om jou in ‘mijn’ team te hebben. Ik heb me er altijd over
verbaasd dat je ondanks je drukke agenda altijd zeer snel reageerde op weer een nieuwe
versie van een manuscript. Je wist altijd wel iets positiefs op te merken en van al je
feedback heb ik enorm veel geleerd. Ook heb ik je altijd bewonderd over je nuchtere
en integere kijk op het doen van onderzoek en je wist me altijd prikkelende vragen te
stellen tijdens onze overleggen, die naast nuttig ook erg leuk en gezellig waren.

Koos, ik kan me niet herinneren dat je ooit iets negatiefs hebt gezegd. Altijd zette je de
stip op de horizon voor me: ‘einde van het jaar ben je klaar’, zei je dan. Het was fijn om
d
jou in het team te hebben als aanjager, steun en voor de positieve noot. Ondanks dat je
al met pensioen bent, vind ik het fantastisch dat je mij nog wilde begeleiden.

Femke, toen je van het RIVM naar GGD Twente kwam was ik zo blij. Toen je ook nog
een heel erg leuk mens bleek te zijn, dacht ik ‘daar wil ik nog veel meer mee samen
werken’. Samen hebben we uren getalletjes door zitten nemen en zitten nadenken over
hoe we iets moesten aanpakken. Soms zei je; ‘Karlijn? Volgens mij gaat er hier iets fout’.
Neeeee! En dan deden we alles weer opnieuw. Ik had het gevoel dat je mijn vragen gelijk
begreep en ik deed erg mijn best om jouw statistische argumenten ook te begrijpen. Ik
ben heel blij dat je naast een fijne collega ook nog mijn vriendin bent.

Nelleke, toen Femke zei dat ze nog wel iemand wist als stagiair voor het onderzoek naar
mannen die seks hebben met mannen, dacht ik dat je met ‘een Koedijk’ niet zo snel fout
kon zitten. En dat bleek ook zo te zijn. Ik had geen werk aan je, jij deed alles zonder

183
hulp en met een intellect en nuchterheid waar ik enorm veel bewondering voor heb.
Aan het einde van de dag kwam je soms gewoon een praatje maken en daar heb ik van
genoten. Ik hoop dat we nog regelmatig met z’n drietjes afspreken en het nut bespreken
van het hebben van katten.

GGD Twente (Mieke Besselse, Erik Maarsingh, Anne-Marie Kok, Harry Rietman en alle
andere collega’s), toen ik vertelde over mijn plan om te promoveren werd dat gelijk goed
ontvangen. Ik heb alle ruimte en ook tijd gekregen om te werken aan onderzoek. Als
ik een scholing of een congres wilde volgen, kon dat vaak gewoon. Daarnaast waren er
verschillende collega’s die regelmatig informeerden naar mijn promotietraject en heel
veel belangstelling toonden, dat heb ik heel erg gewaardeerd.

Team seksuele gezondheid, alle onderzoeken in dit proefschrift heb ik te danken aan
jullie en dit proefschrift lag er niet zonder jullie. Telkens tijdens onze werkoverleggen
stelde ik dan weer een nieuw onderzoek voor om uit te voeren of aan mee te doen en
jullie zeiden nooit ‘nee’. Hoewel het soms best wel veel moeite kostte om deelnemers te
werven, ging de één nog fanatieker dan de ander aan de slag. Vooral bij het onderzoek
naar zelfstandig werkende sekswerkers was ik ontroerd over alle hulp die ik kreeg.
Iedereen hielp mee door telefoonnummers van sekswerkers te verzamelen door een
website af te struinen waar deze sekswerkers adverteerden. Ik ben altijd zo enorm trots
op jullie en besef me heel goed dat ik geluk heb gehad met zo’n goed team, jullie doen
enorm goed werk!

Lieve Barbara, dankjewel dat je altijd belangstelling toonde in mij en in mijn

proefschrift. Ik hoop dat we nog heel lang ‘hoe gaat het met je?’ aan elkaar vragen.
Ben, onze telefoongesprekken zijn nooit langer dan noodzakelijk, maar lang genoeg
om mijn ongenoegen of blijdschap aan je kwijt te kunnen of je advies in te winnen,
bedankt daarvoor. Triston, we zaten jaren tegenover elkaar op het werk. We hebben
serieuze gesprekken gehad, heel veel gelachen en soms gezongen. Cherelle van Stenus,
Daphne Reukers, Olga Visser en Inge Stortenbeker, bedankt dat ik jullie mocht bestoken
met al mijn vragen over promoveren en ook voor de geruststelling dat ik het wel kan.

Dear Amanda, my (step-)sister, I love you dearly and I thank you very much for helping
me with the English editing (during nightly hours). Joris, Bo en Luc, mijn drie broers, ik
hou heel veel van jullie en dat zeggen we te weinig tegen elkaar. Ik heb heel veel respect
voor hoe jullie zijn als mens. Alle drie een groot rechtvaardigheidsgevoel, intelligent en
veel humor. Ik kan niet goed uitdrukken hoe belangrijk jullie voor me zijn.

184
My ‘evil (maar niet echt!) stepmom’ Anneke, dankjewel dat je je hart openstelde voor
ons en dat je je altijd interesseert in onze levens. Lieve papa, ach mijn lieve wijze vader,
als jij geen dokter was geweest, was ik ook geen dokter geworden. Ik hou zoveel van je
en ik wil nog zoveel tijd met je doorbrengen. Ik vind het mooi dat ik mijn doctorstitel
hopelijk ga behalen op de universiteit waarop jij geneeskunde hebt gestudeerd. Lieve
mama, je bent al meer dan 25 jaar niet bij ons. Ik hoop dat je er ergens toch nog ‘bent’
om af en toe te kijken hoe het met ons gaat. Ik denk dat je trots op ons bent en we
dragen je altijd bij ons.

Lieve Fausto, er waren genoeg zondagen dat jij liever iets leuks samen wilde doen,
maar ik weer aan mijn proefschrift wilde werken. Je hebt er altijd begrip voor gehad
en je hebt altijd mijn rug in de meest ingewikkelde situaties. Je bent een hele rustige,
integere, slimme en knappe man en dat is een goede combinatie met de stuiterbal die
ik soms kan zijn. Soms zei je: ‘Ga maar even sporten’ en dat was dan ook precies wat ik
moest doen. We hebben samen het fijnste leven dat ik me kan wensen samen met onze
lieve katten Polly en Louis. Ik hou heel veel van jou!

185
About the author

Karlijn Kampman was born on August 19 th 1980 in

Almelo, The Netherlands. In 1998 she completed her
higher secondary education at Thijcollege in Oldenzaal
(Atheneum). That same year she began her study psychology
at the RijksUniversiteit Groningen. After 2 years she made
the switch to medicine, also at the RijksUniversiteit
Groningen. She did her internships at Deventer Ziekenhuis
in Deventer, where she participated in research in the field
of paedriatrics. She completed her medical training at
Rintveld in Zeist, with a master thesis on eating disorders.

After graduating from medical school in 2006, Karlijn became a resident in psychiatry
at Mediant in Enschede, and at Dimence in Deventer. In 2008, she changed direction,
to work for the Public Health Service in Enschede, first as a youth healthcare medical
doctor, and after a year, as a resident in infectious disease control. Here, she completed
her infectious disease residency in 2015 with research into chlamydia reinfections
among young heterosexual clients (presented in this thesis). In 2017, Karlijn began
combining her work in infectious disease control, with a PhD position at the Academic
Collaborative Centre AMPHI, Radboud university medical center in Nijmegen.

Karlijn sat on various committees, such as the committee of guidelines on sexually

transmitted infections, and the committee of Dutch doctors working in sexual
healthcare. She has provided education on STI for medical interns, general practitioners
(in training) and second-line medical doctors. She made educating a second job in 2018,
when she started work as a teacher at the nursing education at Saxion Hogescholen in a
Enschede. Karlijn is currently still employed as a medical doctor in infectious disease
control, alongside her job as a medical doctor in child abuse and domestic violence at
Veilig Thuis Twente in Enschede.

Karlijn lives with her partner Fausto, in Enschede.

187
List of publications

In this thesis

Kampman C, Koedijk F, Driessen-Hulshof H, Hautvast J, van den Broek I. Retesting

young STI clinic visitors with urogenital Chlamydia trachomatis infection in the
Netherlands; response to a text message reminder and reinfection rates: a prospective
study with historical controls. Sex Transm Infect. 2016 Mar;92(2):124-9
• Response to eLetter: Ahmed, N, Browne R. Retesting Chlamydia trachomatis in a
GUM clinic in London, UK. Sex Transm Infect. 2016. Available on: https://sti.bmj.
com/content/92/2/124.responses#re-retesting-chlamydia-trachomatis-in-a-gum-
clinic-in-london-uk

Kampman CJG, Heijne JCM, Kistemaker-Koedijk PHM, Koedijk FDH, Visser M,

Hautvast JLA. Determinants of frequent and infrequent STI testing and STI diagnosis
related to test frequency among men who have sex with men in the eastern part of the
Netherlands: a 6-year retrospective study. BMJ Open. 2018 May 31;8(5):e020495

Kampman CJG, Hoebe CJPA, Koene R, Kamp L, Jansen K, Koedijk FDH, Tostmann A,
Hautvast JLA. Sexually transmitted infections in male heterosexual Dutch clients who
visited German cross-border female sex workers; a 3 year retrospective study. BMC
Public Health. 2020 Jul 29;20(1):1182

Kampman CJG, Hautvast JLA, Koedijk FDH, Bijen MEM, Hoebe CJPA. Sexual behaviour
and STI testing among Dutch swingers: A cross-sectional internet based survey
performed in 2011 and 2018. PLoS One. 2020 Oct 1;15(10):e0239750

Ostendorf SB, Kampman CJG, Hoebe CJPA, van der Velden J, Hautvast JLA, van Jaarsveld
CHM. Consultation rate and chlamydia positivity among ethnic minority clients at STI p
clinics in the Netherlands. PLoS One. 2021 Feb 19;16(2):e0247130

Kampman CJG, Peters CMM, Koedijk FDH, Berkenbosch TS, Hautvast JLA, Hoebe CJPA.
Sexual risk and STI testing behaviour among Dutch female and male self-employed sex
workers; a cross-sectional study using an Internet based survey. BMC Public Health.
2022 Jun 9;22(1):1155

189
Other publications

Haitsma, A, Besselse, M, Kampman, K. Chlamydia en gonorroe in Twente 2007-2010.

Infectieziekten Bulletin, jaargang 23, nummer 1, januari 2012

Kampman, K. Kan een kind met een asymptomatische STEC-infectie naar het
kinderdagverblijf? Infectieziekten Bulletin, jaargang 24, nummer 2, februari 2013

Kampman CJG, Koedijk FDH, Hondelink I, Geeraedts F. Chlamydiatesten in Twente;

naar de huisarts of de GGD? Infectieziekten Bulletin, jaargang 27, nummer 3, maart 2016

Lanjouw, E., 2017. Chlamydia trachomatis: Clinical, bacterial, and host aspects of a
silent love bug. Thesis PhD. VU Amsterdam.
• Lanjouw E, de Waaij DJ, Ouburg S, Pleijster J, Bruisten SM, van der Sande MAB,
van Benthem BH, Kampman CJG, Variant Analyses Group, van der Zanden AGM,
Morré SA. The Dutch Chlamydia trachomatis Reference Laboratory 2010-2015:
identification and surveillance of clinical samples for plasmid free and other
Chlamydia trachomatis variants. In progress.

Visser M, van Aar F, Koedijk FDH, Kampman CJG, Heijne JCM. Repeat Chlamydia
trachomatis testing among heterosexual STI outpatient clinic visitors in the Netherlands:
a longitudinal study. BMC Infect Dis. 2017 Dec 20;17(1):782

Soons, A, Kampman, K. Een Canadese militair met het vermoeden op hand-voet-mond

ziekte die de Nijmeegse vierdaagse gaat lopen. Infectieziekten Bulletin, jaargang 29,
nummer 3, maart 2018

Manon T. M. Pelgrim, Karlijn J. G. Kampman, Henny Rexwinkel, Alma Tostmann,

Jeannine L. A. Hautvast. Overwegingen om te kiezen voor een soa-test bij de GGD. TSG
– Tijdschrift voor gezondheidswetenschappen, uitgave 2/2018

Soeteman, JH, Kampman CJG. Meningokokkenurethritis; soms ‘onder’ het hoofd

gezien… Infectieziekten Bulletin, jaargang 29, nummer 7, september 2018

Van Wees DA, Heijne JCM, Heijman T, Kampman KCJG, Westra K, de Vries A,
Kretzschmar MEE, den Daas C. Study protocol of the iMPaCT project: a longitudinal
cohort study assessing psychological determinants, sexual behaviour and chlamydia
(re)infections in heterosexual STI clinic visitors. BMC Infect Dis. 2018 Nov 13;18(1):559

190
Van Wees DA, Heijne JCM, Heijman T, Kampman KCJG, Westra K, de Vries A, de Wit J,
Kretzschmar MEE, den Daas C. A Multidimensional Approach to Assessing Infectious
Disease Risk: Identifying Risk Classes Based on Psychological Characteristics. Am J
Epidemiol. 2019 Sep 1;188(9):1705-1712

Kampman, CJG, Bos, H. De veranderende rol van de GGD in seksuele gezondheid.

Bijblijven. Uitgave 5/2019

Evers YJ, Dukers-Muijrers NHTM, Kampman CJG, van Liere GAFS, Hautvast JLA,
Koedijk FDH, Hoebe CJPA. Prevalence of drug use during sex among swingers and
perceived benefits and risks - a cross-sectional internet survey in the Netherlands. Sex
Transm Infect. 2020 Feb;96(1):40-46

Evers YJ, Hoebe CJPA, Dukers-Muijrers NHTM, Kampman CJG, Kuizenga-Wessel S,

Shilue D, Bakker NCM, Schamp SMAA, Van Buel H, Van Der Meijden WCJPM, Van Liere
GAFS. Sexual, addiction and mental health care needs among men who have sex with
men practicing chemsex - a cross-sectional study in the Netherlands. Prev Med Rep.
2020 Mar 6;18:101074

Slurink I, Groen K, Gotz HM, Meima A, Kroone MM, Hogewoning AA, Ott A, Niessen
W, Dukers-Muijers N, Hoebe C, Koedijk F, Kampman C, van Bergen J. Contribution
of general practitioners and sexual health centres to sexually transmitted infection
consultations in five Dutch regions using laboratory data of Chlamydia trachomatis
testing. Int J STD AIDS. 2020 May;31(6):517-525

Bogers SJ, Twisk DE, Beckers LM, Götz HM, Meima B, Kroone M, Hoornenborg E,
Ott A, Luning-Koster MN, Dukers-Muijrers NHTM, Hoebe CJPA, Kampman CJG,
Bosma F, Schim van der Loeff M, Geerlings S, van Bergen J. Who is providing HIV
diagnostic testing? Comparing HIV testing by general practitioners and sexual health p
centres in five regions in the Netherlands, 2011-2018. Sex Transm Infect. 2021 Jul
27:sextrans-2021-055109

Slurink I, van Aar F, Parkkali S, Heijman T, Götz H, Kampman K, van Weert Y, van
Benthem B, van de Laar T, Op de Coul E; RITA surveillance network of sexual health
centres. Recently acquired HIV infections and associated factors among men who
have sex with men diagnosed at Dutch sexual health centres. Int J STD AIDS. 2021
Sep;32(10):946-956

191
Research Data Management

This thesis is based on the results of human studies, which were conducted in
accordance with the principles of the Declaration of Helsinki. The medical and ethical
review board Committee on Research Involving Human Subjects Region Arnhem
Nijmegen, Nijmegen, the Netherlands has given approval to conduct these studies.

The data for analyses of five studies (the study in chapter 4 excluded) is stored on
the server of the department ‘General Health’ of the Public Health Service Twente
(T:/GGDTwente/Algemene gezondheidszorg/Poli seksuele gezondheid/Onderzoeken/
Promotieonderzoek Karlijn Kampman) and is only accessible for Karlijn Kampman
(PhD student and medical doctor) and Femke Koedijk (epidemiologist). The data for
analyses of the study in chapter 4 is stored on the server of the Public Health Service
Gelderland Midden and only accessible to Saskia Ostendorf (medical doctor).

For the study described in chapter 2 study participants filled in an informed consent
form on paper, which allowed us to send a text message reminder for a retest. These
consent forms were discarded one year after publication of the research article.

All participants in our studies described in chapter 2 to 4 and in chapter 6 were clients
of the (participating) STI clinics and their personal and health-related data, which
were collected as part of regular care, were registered in an online client registration
system. The records of clients, who were part of one of these studies were exported
into a de-identified dataset. Furthermore, in the studies described in chapter 3, 4 and
6, clients were not directly involved in any aspect of the study, so only their routinely
collected de-identified data was used. In chapter 2 to 4 and in chapter 6, multiple STI
clinics participated in these studies and agreed to provide the data used.

The study data in chapter 5 and 7 were obtained using the online survey tool
SurveyMonkey (San Mateo, California, USA), and were registered in a fully anonymized
and deidentified manner. Informed consent was obtained when a participant entered
the online survey. To enter the prize pool for random allotment of dinner cheques,
r
participants were directed to a separate survey where they could enter their email
address (only used for sending the incentive when applicable). After the prize winners
were emailed, the separate survey for entering email addresses was deleted. The
study data was exported from SurveyMonkey to an excel file, which was stored on the
department server, as described above. The studies and the data that were stored in
the online survey tool SurveyMonkey were deleted after export.

193
Data for chapter 4 can be found in the supplementary file of the original publication:
https://journals.plos.org/plosone/article/file?type=supplementary&id=10.1371/journal.
pone.0247130.s001

Data for chapter 7 can also be found in the supplementary files of the original
publication: https://doi.org/10.1371/journal.pone.0239750.s004

The data will be saved for 15 years after termination of each study. The datasets analyzed
during these studies are available from the corresponding author on reasonable request.

194
PhD portfolio of Karlijn Kampman

Department: Primary and community care

Graduate School: Radboud Institute for Health Sciences
PhD period: 1-11-2017 – 31-12-2022
Promotor(s): Prof. dr. J. van der Velden and Prof. dr. C.J.P.A. Hoebe
Copromotor(s): Dr. J.L.A. Hautvast

Training activities Hours

Courses
· Data analyses, EPID M (2017) 36
· Foodborne Outbreaks, a statistical approach, Tallin, Estonia (2017) 30
· Advanced Excel, Twentse Kracht (2018) 8
· Scientific integrity, Radboudumc (2018) 16
· Writing a scientific article, Taalcentrum VU (2019) 32
Seminars
· AMPHI tele-arena (every year), 2x oral presentation 4
· PhD trajectory for the AMPHI board, oral presentation (2019) 1
· PhD trajectory for Public Health Service Twente, oral presentation 1
(2021)
Conferences
· National annual Expert meeting on STI (every year), 2x oral 30
presentation 30
· National Congress STI/HIV/Sex (every year) 24
· Congress of the International Union against Sexually Transmitted
infections (IUSTI), Dublin, poster presentation (2018) 8
· National congress of sexual violence (2019) 18
· STI & HIV world congress (2021)
Other
Teaching activities
Lecturing
· Lecturing general practitioners in training on STI (every year) 12
· Lecturing general practitioners and specialists in second line care 20
in STI (every year) 12
· Lectures for medical students on STI (oral presentation), p
supervision of students in developing a workshop on STI or 8
infectious diseases (every year)
· Lecturing at career day for medical students at the University of
Groningen, oral presentation (2017,2019)

197
 Supervision of internships / other
· Supervision Bachelor student internship Psychology University 42
of Twente (2018)
· Supervision Master student internship Radboud University 8
(2020)
· Supervision Master student Nursing Sciences Utrecht 16
University (2021)
· Supervision of internship medical students of the University of 8
Groningen (every year)
Total 364

198