Abstract
Chlamydia trachomatis (CT) infection has been a target for both selective and national screening programmes, and Sweden has an opportunistic approach. A national plan of action states that risk groups should be identified and offered risk reduction counselling. Patients attending a drop-in sexually transmitted infection (STI) clinic reception at the University Hospital, Umeå, Sweden, were invited to complete a questionnaire regarding sociodemographic characteristics, symptoms and sexual risk behaviour; all had a CT test taken. A total of 1305 patients were included, 58% men, mean age 27.8 years. CT prevalence was 11%; 51% of those with CT were ≥25 years old. Only 5% used a condom during the entire sexual intercourse with their last new/temporary partner. Sexually active inconsistent condom users comprised 62% of the study population and contributed to 81% of the chlamydia infections. Asking whether a condom was used could quickly triage patients into groups with a ‘higher risk’ (none or inconsistent use of condoms and at least one new/temporary partners), and ‘lower risk’ (with more consistent condom use, although not always accurate) allowing for individualized care and counselling when screening for chlamydia. Evaluating whether a condom was used throughout the sexual intercourse did not add any useful information.
INTRODUCTION
Chlamydia trachomatis (CT) is the most common sexually transmitted bacterial infection in Europe 1 with case rates up to 10% among the sexually active. 2,3 The infection is often asymptomatic but may be complicated by salpingitis and pelvic inflammatory disease with subsequent scarring resulting in chronic abdominal pain, ectopic pregnancies and infertility in women. 4 CT has also been associated with reduced fertility in men. 5 Persistent infection and chronic inflammation are discussed as possible cancer initiators/promoters in gynaecological tumours 6 and comorbid CT facilitates the transmission of HIV by two- to five-fold. 7 The costs to treat subfertility due to CT are high because it often requires in vitro fertilization. The highest rates of infection occur among young people and the European Centre for Disease Prevention and Control concludes that age <25 years and multiple partners are the only clear risk factors for CT. 1 In England, a national CT screening programme offers screening to young people <25 years annually or at change of partner. 8 In Sweden, there is no national screening programme but an opportunistic approach. CT tests and treatment are free of charge and CT has been incorporated into the legislation for the control of infectious diseases since 1988; partner notification including testing of partners is obligatory. 9 Because of the rising numbers of people with CT, the National Board of Health and Welfare in Sweden has concluded a national plan of action. It stated, among other things, that safe sex behaviour must increase among young people. It encourages research about identification of risk groups for sexually transmitted infections (STIs) so that they can be tested and offered interventions to prevent infection/re-infection. 10 STI clinic populations usually have a high prevalence of CT. While age <25 years is a good screening criterion in populations with low prevalence, there are indications that age has to be combined with other factors in populations with higher prevalence, to increase its performance. 11–13 Our goal was to investigate safe sex behaviour among people attending an STI clinic in Umeå, Sweden, and to identify factors indicating ‘higher’ and ‘lower’ risk for acquiring a CT infection so that they could be targeted for preventive interventions. One CT infection is a risk factor for reinfection 14 and repeated infections increase the risk of severe complications associated with CT. 15 Motivational interviewing has shown good results in changing sexual risk behaviour 16 but it is resource demanding and can often not be offered to all patients attending the clinic.
MATERIAL AND METHODS
The study took place at the STI clinic, Department of Dermatology and Venereology, University Hospital, Umeå, Sweden, from January 2008 to December 2009 and was approved by the Ethical Review Board at Umeå University. Patients were included after informed consent. The questionnaires and test results were saved with a code only and the identity of the patients is known only by the leader of the project. During November–December 2007, a pilot project was performed in order to test our method and validate our questionnaires. In January 2008, we started a regular ‘drop-in’ clinic. All patients attending were offered inclusion in the study. Exclusion criteria were: not understanding Swedish well enough to answer the questions; recent antibiotic treatment; previous participation in the study within the last six months. Participants were asked to answer questions regarding medication, demographic characteristics, marital status, symptoms, number of sexual partners, past STIs, sexual behaviour and condom use. Those reporting sexual activity within the last 12 months were asked to provide further information about their partners and condom use. On a time-axis they plotted sexual activity with each partner. Information about age, sexual preferences, contraceptive use and condom use at last intercourse with new/temporary partner was extracted from the medical records. The patients met a nurse or a physician and all patients with symptoms were examined by a physician experienced in venereology. All patients had a first-void urine test taken for CT; in women this was combined with an endocervical or self-taken vaginal swab. Nucleic acid amplification testing was used to detect CT DNA: at our laboratory this was performed with the BD ProbeTec strand displacement amplification assay (Becton, Dickinson & Company, Sparks, MD, USA). 17 If considered necessary, tests for other STIs were performed as well.
Statistical analysis
All data analysis was performed in SPSS 17.0 for Windows (IBM Corporation, Somers, NY, USA), with a significance level of P < 0.05. Chi-square (χ 2 test was used for categorical variables and Student's t-test for continuous variables. We used logistic regression to explore associations of CT infection with independent variables (age, marital status, highest completed education, employment and condom use). A confidence interval of 95% was chosen.
RESULTS
Response rates
During the study period (January 2008 to December 2009) 1855 visits were registered at the drop-in reception. One hundred and sixty persons (9%) were excluded due to participation in the study within the previous six months, 37 (2%) did not speak Swedish well enough to complete the questionnaires and 146 (9%) due to recent antibiotic treatment. Fifty-six patients (3%) who were homosexual or bisexual were also excluded, as this group was considered too small to allow for comparisons. One hundred and twelve persons (6%) were excluded because they declined to fill in a questionnaire or rejected an offer of CT testing and 39 (2%) patients did not receive a questionnaire due to administrative failure. The excluded patients did not differ significantly from the study population according to sex, age and CT infection status.
Characteristics of the studied population
Of the 1305 patients included in the study, 757 were men (58%). The mean age for men was 28.0 years (range 16–66) and for women 26.9 years (16–62). The overall prevalence of genital CT infection was 11.3%: men 12.4%, women 9.9% (P = 0.149) (see Table 1). The mean age of those infected was significantly lower than that of the uninfected (26.4 [SD 7.2] versus 27.7 [SD 7.3], P = 0.045). Fifty-one percent (76/148) of CT-infected individuals were ≥25 years old. When subdivided by gender, there was no significant difference regarding the mean age among men; CT-positive men 27.2 years (SD 8.0), CT-negative men 28.2 years (SD 7.3), P = 0.222. The mean age of CT-positive women was 25.1 years (SD 5.6) compared with CT-negative women (27.1 years [SD 7.1], P = 0.050). Seven hundred and sixty-nine patients underwent testing for other conditions in addition to CT, and 177 were diagnosed with other STIs (herpes genitalis 25; genital warts 81; Neisseria gonorrhoeae 2; Mycoplasma genitalium 13; non-specific urethritis/cervicitis 56). Five patients had co-infections with CT: one had herpes genitalis and four had genital warts.
Risk factors for Chlamydia trachomati s among patients attending an STI clinic in Umea, Sweden (n = 1305)
STI = sexually transmitted infection; CT+ = chlamydia infected; CuIUD = copper intra uterine device; CT = Chlamydia trachomatis
†Low education = highest completed education upper-secondary school; high education = highest completed education university
‡Information from patients' medical records
Behavioural factors associated with chlamydia infection
Nineteen percent (230/1209) stated that they always used a condom with a new/temporary partner and 67% (149/222) of them always used a condom throughout the intercourse. According to the medical records 24% (250/1041) had used a condom at the last intercourse with a new/temporary partner and 23% of them always used a condom throughout the intercourse.
Regarding the condom questions there were no differences according to sex (P = 0.564) but non-responders were significantly older (mean age 30.0, SD 9.9) compared with responders (mean age 27.0, SD 7.3), P < 0.001. Patients reporting many new/temporary partners within the past six months were less likely to use a condom; 4% (2/50) with ≥5 new/temporary partners stated always using condom, compared with 21% (91/428) of those with one new/temporary partner, P = 0.001. The inconsistent condom users accounted for 81% (979/1209) of all patients in the study and 91% (123/135) of all CT-positive participants; hazard ratio (HR) = 12.6. If patients with a new/temporary partner within the past six months and with inconsistent condom use were to be screened, this would require 62% (707/1137) of the population to be tested but would yield 81% (102/126) of all CT infection; HR = 14.4. Five percent (8/149) of those who stated they always used a condom throughout the intercourse with a new/temporary partner were CT-positive, compared with 2.7% (2/73) among those who always used a condom with a new/temporary partner, but not always throughout the intercourse. Thirteen percent (47/373) of those who did not always use a condom with new/temporary partners, but always used one throughout the intercourse when they did were infected with CT; compared with 12.7% (72/566) not always using a condom and not always using it throughout the intercourse. Having had at least one new/temporary partner was significantly associated with present CT infection in both sexes; men P = 0.011, women P = 0.013. Information about contraceptives was extracted from the women's medical records, and was missing for 26%. There was no significant age difference between responders and non-responders to the contraceptive question (mean age 27.3 [SD 7.0] versus 27.8 [SD 7.5], P = 0.205). The users of hormonal contraceptives were younger than the other responders (25.7 [SD 5.8] versus 27.9 [SD 7.7], P = 0.001), were more often inconsistent condom users (122/169 versus 157/191, P = 0.023), but did not have significantly more new/temporary partners (mean 1.4 versus 1.4, P = 0.818).
Multivariate analysis
Including all factors significantly associated with CT and possible confounders (age, marital status, highest completed education or employment and condom use), hormonal contraceptives remained significantly associated with CT among women, and symptoms among men (see Table 2). Three hundred and twenty-five women and 588 men were included in the analysis. Only 36% could answer the question about having a sexual partner with recent or current CT infection; due to this low response rate the question could not be included in the multivariate analysis, although the high-association indicates that this is a strong risk factor of CT infection.
Multivariate logistic regression with CT as the dependent variable
Including factors significantly associated with CT after bivariate analysis in each sex and possible confounders
CT = Chlamydia trachomatis; OR = odds ratio; CI = confidence interval; low education = highest completed education upper-secondary school; high education = highest completed education university
†Dysuria and/or discharge. As both highest completed education level and employment are measures of socioeconomic status, and highly correlated, only one factor was included in the analysis. The factor with the strongest association was chosen for each sex
DISCUSSION
Condoms protect effectively against STIs if they are used consistently and correctly. 18 In screening studies, questions about barrier contraception often focus on whether a condom was used at all and do not explore if the condom in fact was used throughout the intercourse. 19–21 Only 5% of patients attending our drop-in STI clinic reception used a condom throughout the intercourse with their last new/temporary contact and 30% who stated they always used a condom with a new/temporary partner did not consistently use a condom throughout the intercourse. Even if the number of consistent and correct users differs slightly depending on how the question was asked, and the number of non-responders contributes to uncertainty, inconsistent condom use (defined as not always using condom with a new/temporary partner) was associated with present CT infection. Additional information about whether the condom was used throughout the intercourse did not add any further risk of infection. To our knowledge, this is the first investigation evaluating this correlation. When screening for CT infection the important question seems to be if, and not how, a condom was used. Our belief is that most people not using a condom throughout the intercourse used it at the end of the intercourse as a method of contraceptive. Condoms protect against STIs, 18 but in the case of CT we could not find an increased risk of infection if the condom was used only during part of the intercourse.
Short counselling can enhance safe sex and reduce the risk of acquiring an STI. 16 Sexually active inconsistent condom users attending a drop-in STI clinic are at ‘higher risk’ of infection and seem to be a good target for preventive counselling. They constitute 62% of all visitors at the clinic but 81% of the patients with CT. Attendees with more consistent condom use or no new/temporary partners within the past six months belong to the ‘lower risk group’. Using the question as to whether a condom in fact was used and whether the patient had had any new/temporary partner could thus allow for quick risk stratification of the patients and enable individualized care depending on risk level. We cannot, however, comment on the reasons for inconsistent condom use. Others have found it to be attributed to alcohol use; key life stages; negative affective status; increased number of sexual partners; not considering oneself at risk of infection; and not wanting the partner to believe that they do not trust them/think they have CT. 21–23
Even if CT is more common among young people, sexual risk taking occurs among older patients as well. 12 Age would not be a sufficient criterion to select patients at higher risk of infection at this kind of clinic. If preventive counselling would have been offered to patients <25 years, 51% those with CT would have been missed. Since maternal age at first delivery now approaches 30 years in Sweden in combination with more liberal attitudes to casual sex, people continue to put themselves at risk of infection in higher age groups. 24 A prevalence study from France found increased rates of infections among 18–29 years old. 25
Different screening criteria should be used depending on the prevalence in the specific setting. 13
Socioeconomic factors were highly correlated with present CT infection among women, when adjusted for sexual behaviour factors; this is a known correlation. 19,26 Unemployment and being on sickness benefits are measures of lower socioeconomic status, which is correlated to many other health risks including smoking and hazardous drinking. These women might be more willing to take sexual risks as well. Depression and low self-esteem are also more common among those unemployed and on sickness benefits 24 and may also have a negative impact on sexual risk taking.
Individuals with symptoms are more likely to appear at a drop-in clinic. 27 Urogenital symptoms (discharge and dysuria) in men are strongly correlated with CT infection. 28 Self-reported abnormal discharge was more common among women with CT as well, compared with non-infected, but the correlation was not significant. The increased uncertainty in responses to this question by women may indicate that many women are not familiar with the normal variations of their discharge. It was more puzzling that many men were uncertain whether they had discharge or not; perhaps some men do not understand the full meaning of the term ‘discharge’ as it was used in this study. No significant correlation between women's self-reported symptoms of bleeding or dysuria and CT was shown in our study, in contrast to some other studies. 29,30
Knowing that one has had a partner with current/recent CT was a strong risk factor for having CT infection. An observation, however, is that the vast majority of the patients did not know the answer to this question. This association is supported by the fact that at least 65% of sexual partners of persons with CT are infected themselves. 31 This supports our current strategy of partner notification and preventive counselling for all patients with a recent CT-positive partner.
The use of hormonal contraceptives was also associated with current CT infection. Hormonal contraceptives have been associated with an increased affinity to STIs. 32 The users of hormonal contraceptives were younger and more often inconsistent condom users but did not have significantly more new/temporary partners. The correlation between hormonal contraceptives and current infection remained when adjusted for sexual behaviours and other possible confounders. There were a large number of non-responders to the contraceptive question; data for this question were extracted from the medical records and this information is supposed to be obtained from all women attending the STI clinic. There was no difference regarding age among responders and non-responders. If all non-responders were included in the chi-square analysis as not using hormonal contraceptives, the P-value changes to 0.05, but most likely at least some of the non-responders were users of hormonal contraceptives. We consider the correlation between hormonal contraceptives and CT infection strong irrespective of the low response rate.
Limitations
This is a cross-sectional survey and does not consider variations over time. Condom use and attitudes vary from day to day 21,22 and increased risk activity is also associated with key life stages, particularly in heterosexuals. 33 One possible reason for non-response in the questionnaires may be that not answering or not remembering is symptomatic of a high-risk lifestyle. Many non-responders had a high rate of infection. The study environment required participants to fill in a questionnaire including private questions in a crowded waiting room and this might also have had some influence. More women answered the question about lifetime STIs; non-responders to condom questions were older. The missing values from medical records seemed to occur randomly and were due to compliance by the medical staff seeing the patients.
CONCLUSIONS
A drop-in clinic allows for an opportunistic screening approach and our service attracts men and people aged ≥25 years, usually groups with a lower testing rate. 34 Despite this, we found a high rate of CT infection. A question about condom use and new partners could quickly classify patients into groups with a ‘higher risk’ and ‘lower risk’, enabling a degree of individualized care and counselling. Evaluation of whether a condom was used throughout the intercourse does not add any further information regarding the risk of CT infection. Hormonal contraceptives were independently correlated with current CT infection, even when controlled for possible confounders.
Footnotes
ACKNOWLEDGEMENTS
The contribution of the staff (nurses, counselor and secretaries) at our ‘drop-in’ STI clinic is greatly acknowledged. This work was supported by grants from The National Board of Health and Welfare, Sweden, and the counties of Västerbotten and Norrbotten.
