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Provision of Sexually Transmitted Infection Services in a Mobile Clinic Reveals High Unmet Need in Remote Areas of South Africa

A Cross-sectional Study

Hoffman, Charlotte M. BSc*†; Mbambazela, Nontembeko BSc*; Sithole, Phumzile BA*; Morré, Servaas A. PhD; Dubbink, Jan Henk PhD*; Railton, Jean Fam Med*; McIntyre, James A. FRCOG; Kock, Marleen M. PhD¶∥; Peters, Remco P.H. PhD*†∥

Sexually Transmitted Diseases: March 2019 - Volume 46 - Issue 3 - p 206–212
doi: 10.1097/OLQ.0000000000000931
The Real World of STD Prevention

Background The burden of sexually transmitted infections (STIs) in areas of sub-Saharan Africa with poor access to health care services is not well documented. In remote areas of South Africa, we investigated the prevalence of STIs and approaches to providing STI services through a mobile clinic.

Methods We recruited 251 adult women visiting a mobile clinic that normally provides general health education and screening services, but not STI care. Clinical and sexual history was obtained and vaginal specimens were tested for Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium infection and for Candida albicans and bacterial vaginosis.

Results Laboratory test was positive for 133 (53%) of 251 women for at least 1 STI: C. trachomatis was observed in 52 (21%) women, N. gonorrhoeae in 39 (16%) women, T. vaginalis in 81 (32%) women and M. genitalium in 21 (8%) women. Eighty-one (32%) women met the criteria for vaginal discharge syndrome, of which 58% (47/81) would have been treated accurately. Among asymptomatic women 84 (49%) of 170 were diagnosed with an STI but untreated under the syndromic approach. We could not identify factors associated with asymptomatic STI infection.

Conclusions There is a high unmet need for STI care in rural South African settings with poor access to health care services. Provision of STI services in a mobile clinic using the syndromic management approach provides a useful approach, but would have to be enhanced by targeted diagnostics to successfully address the burden of infection.

Provision of sexually transmitted infection services through a mobile clinic provides a successful approach to address the high unmet need for sexually transmitted infection care in remote areas of South Africa.

From the *Anova Health Institute, Johannesburg, South Africa;

Department of Medical Microbiology, School of Public Health & Primary Care (CAPHRI), Maastricht University Medical Centre, Maastricht;

VU University Medical Center, Department of Medical Microbiology, Laboratory of Immunogenetics, Amsterdam, The Netherlands;

§School of Public Health & Family Medicine, University of Cape Town, Cape Town;

Tshwane Academic Division, National Health Laboratory Service, Pretoria; and

Department of Medical Microbiology, University of Pretoria, Pretoria, South Africa

Acknowledgments: The authors thank the patients for participating in this study as well as the staff at Anova Health Institute in Tzaneen and at the laboratory of Medical Microbiology at the University of Pretoria for their support.

Conflicts of Interest: None declared.

Sources of Funding: The authors declare that there is no conflict of interest. This work was supported by a grant (DHKF15/D27) from the Netherlands Enterprise Agency (Rijksdienst voor Ondernemend Nederland) to provide diagnostic tests. Anova Health Institute's Mobile Clinic is funded by Orange Babies (The Netherlands), Stichting Opstap (The Netherlands) and Sala Kuchi Kuchi (The Netherlands).

Correspondence: Remco P.H. Peters, PhD, ANOVA Health Institute, 12 Sherborne Road, Parktown, PostNet Suite 242, Private Bag X30500, Houghton, South Africa. E-mail:

Received for publication June 18, 2018, and accepted October 9, 2018.

The sexually transmitted infections (STIs) Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis, and Mycoplasma genitalium are common worldwide. The African region is particularly affected by these curable diseases, with an estimated incidence of respectively 12.0 million, 11.4 million and 37.4 million new infections per year.1,2 There is currently no accurate estimate available of incidence of M. genitalium infection in Africa, but prevalence has been reported in the range of 6% to 11% among women.3,4 South Africa is known for one of the highest prevalence rates of human immunodeficiency virus (HIV) worldwide.5 Also, it is one of the countries most affected by STIs, with prevalence and incidence rates higher than in other African countries.6 Incidence rates of 14% for C. trachomatis, 4% for N. gonorrhoeae and 7% for T. vaginalis per person-years at risk have been reported in community settings7; prevalence of STIs among pregnant women is even higher.8 Despite counseling and condom provision to reduce risk, incidence rates remain high.7

South Africa has implemented syndromic guidelines for management of STIs, meaning that symptomatic individuals are treated with a combination of empirical antibiotics.9 Several studies have demonstrated that a large proportion of cases receives under- or overtreatment result of using a syndromic instead of etiological approach.10–12 In the long term, untreated STIs can lead to severe complications, such as pelvic inflammatory disease, infertility, a predisposition to ectopic pregnancy and an increased risk of transmitting and acquiring HIV when exposed.13,14

Most studies addressing STIs in sub-Saharan Africa have been conducted among individuals visiting health care facilities or in specific key populations such as sex workers and men who have sex with men. However, there are limited data about the need for STI care and treatment in deep rural areas with high levels of poverty and poor access to health care facilities. Access to health care for people living in these remote areas can be challenging due to long distances and often impassable roads to the nearest primary health care clinic (PHC) as well as lack of personal funds to afford transportation fees.15 In some of these areas, basic health care is provided through mobile clinics. The health care package provided in mobile clinics generally consists of testing for HIV and screening for tuberculosis, diabetes mellitus, hypertension and cervical cancer. The effectiveness of delivering STI services through a mobile clinic has, to our best knowledge, never been investigated or reported on. In this study, we explored the need for provision of STI services in a mobile clinic in the deep rural parts of Mopani district, South Africa. In particular, we investigated the effectiveness of offering STI services using a syndromic and an etiological approach through this mobile clinic to inform the best strategy for providing STI care in remote rural African settings.

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Study Design and Population

This cross-sectional study was conducted in 2016 using a nongovernmental organization–deployed mobile clinic that visits deep rural parts of Mopani district, Limpopo Province, South Africa. This mobile clinic is operated by an experienced nurse practitioner and counselor, and has been operational in the region for more than four years. It provides health information and screening services for HIV, tuberculosis, noncommunicable diseases and cervical cancer. The clinic is stationed in a particular rural area from one up to several days following agreement with the traditional leader of that area. In this evaluation, we only included areas that were at least 20 km away from the nearest health care facility. All adult women (≥18 years) who attended the mobile clinic for any of the health services were eligible for this project, regardless of the presence of STI-associated symptoms. Women that were having menses at the time of recruitment were excluded. This study was approved by the Faculty of Health Sciences Research Ethics Committee of the University of Pretoria and by the Limpopo Provincial Health Research Committee of the Department of Health (Reference number: 498/2016).

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Study Procedures

After obtaining written informed consent, a short questionnaire was administered by the nurse including questions related to demographics, sexual behavior, and symptoms. Physical examination was conducted. Clinician-collected vaginal smear was obtained for microscopy to detect Candida infection and bacterial vaginosis (BV), and a clinician-collected standard flocked vaginal swab (Copan diagnostics, Italy) was obtained for diagnostic testing.

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Laboratory Analysis

All specimens were transported to and processed at the Department of Medical Microbiology of the University of Pretoria. After Gram staining, microscopic assessment of smears was performed to detect BV by Nugent Score and Candida albicans infection based on typical morphological appearance. The High Pure PCR Template Preparation Kit (Roche Molecular Diagnostics, Mannheim, Germany) was used to extract DNA from the swabs followed by real-time polymerase chain reaction on the LightCycler 480 (Roche Molecular Diagnostics, Mannheim, Germany) using the Presto C. trachomatis/N. gonorrhoeae assay for detection of C. trachomatis and N. gonorrhoeae.16 The presence of T. vaginalis was assessed by using the Prestoplus assay and the presence of M. genitalium by using an in-house multiplex PCR assay as described elsewhere.17–19

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Clinical Definitions and Management

Women were considered symptomatic if they met the criteria of the national guideline for management of the vaginal discharge syndrome (VDS)9: self-report of (altered) vaginal discharge, dysuria, and vaginal itch which is then confirmed through clinical examination. Following the national guidelines for VDS, women that were younger than 35 years and had no lower abdominal pain or pain on moving the cervix were empirically treated for STIs with a combination of azithromycin (oral, 1 mg), ceftriaxone (intramuscular, 250 mg), and metronidazole (oral, 2 mg). Women older than 35 years were treated with a combination of clotrimazole (pessary, 500 mg) and metronidazole (oral, 2 mg). For this analysis, women with a positive molecular test for at least 1 of the 4 STIs were classified as having an STI; these could be symptomatic or asymptomatic. Symptomatic women with BV or C. albicans infection on vaginal smear were classified as having a nonsexually transmitted reproductive tract infection (RTI). Symptomatic women with both STI and BV or C. albicans were classified as STI and analyzed separately when appropriate. Human immunodeficiency virus status was classified as positive based on self-reported positive status, negative based on result of rapid HIV test, and unknown in case HIV testing was declined. Symptomatic women were treated syndromically upon recruitment. All participants were contacted to discuss the results of STI testing; in case of asymptomatic STI or inadequate empirical treatment for the STI diagnosed, women were requested to visit the nearest health care facility and to meet with a member of the study team to receive appropriate treatment.

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Data Analysis

The results were analyzed using IBM SPSS Statistics Version 24 (SPSS Inc., Chicago, IL). Data are presented as numbers with proportion (%) and median with range. Comparative statistics were done using χ2 test, with Fisher's exact test if appropriate, for dichotomous and Mann-Whitney Test for continuous variables. A P-value less than 0.05 was considered statistically significant. Odds ratios (ORs) with 95% confidence intervals (CIs) are provided. Univariate analysis was performed to examine factors associated with STIs. Age and other relevant variables with a P value less than 0.01 through univariate analysis, were analyzed with multivariate analysis through logistic regression.

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Participant Characteristics

We recruited 251 women, with a median age of 34 years (range, 18–75 years), who visited the mobile clinic for any of the offered services (Table 1). Three quarters (75%) of the women were literate, 61 (25%) were employed. Three (1%) women were pregnant. Three-quarters (75%) of the participants were HIV-negative; 11% were HIV-infected and 8% had unknown HIV status and refused HIV testing. Almost all women (95%) reported practicing vaginal sex in the past 6 months; only 6% reported having oral sex and 2% anal intercourse. Only 44 (18%) of the women reported condom use during their last sex act. Forty-seven (19%) participants reported an experience of sexual coercion in the past 6 months. Eighty-one (32%) of the women met the criteria for VDS. Abnormal or altered discharge was reported in 36 (14%) women, 20 (8%) reported dysuria and 48 (19%) genital itch. Other genital symptoms that were reported, but are not included as entry point in the VDS algorithm, include lower abdominal pain (29%), pain during sexual intercourse (9%), and blood loss related to sexual intercourse (5%).



More than half of the women (53%; n = 133) tested positive for at least 1 STI: C. trachomatis was observed in 52 (21%) women, N. gonorrhoeae in 39 (16%) women, T. vaginalis in 81 (32%) women and M. genitalium in 21 (8%) women (Table 2). Thirty-four women were infected with 2 STIs, of which the combination C. trachomatis and T. vaginalis was the most common (n = 15). Thirteen women were infected with three STIs, most commonly the combination of C. trachomatis, N. gonorrhoeae and T. vaginalis (n = 6). Forty-nine (37%) of all STI-infected women were symptomatic. Thirty-eight (15%) women were diagnosed with another nonsexually transmitted RTI: BV in 34 (14%) women and C. albicans in six (2%). In twenty-five women with BV and three with C. albicans-infection, concurrent STI was diagnosed.



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Effectiveness of the Syndromic Approach for STI Screening and Management

Vaginal discharge syndrome was present in 81 (32%) women. Adequate empirical treatment (covering the microbiological etiology) based on the VDS algorithm was provided to 47 (58%) of these symptomatic women (Fig. 1): this was in 37 (79%) women with 1 or more STI and 29 (62%) women with 1 or more RTI. Of the 49 women with symptomatic STI, 37 (76%) would have been treated accurately; this is 29 (76%) of 38 women infected with 1 or more RTI. Twenty (25%) women without diagnosed STI or RTI, were treated unnecessarily for either STI or RTI. In addition, 84 (49%) of 170 asymptomatic women were diagnosed with an STI but remained untreated under the syndromic approach. Fewer women with a positive VDS screening (11%) had a sexual partner older than 10 years (P = 0.038) than women who did not meet the criteria for VDS (22%). Also, a trend for alcohol use and positive VDS screening was observed (P = 0.063), but no other demographic or behavioral factors were associated. Other symptoms related to reproductive tract infections, but not included in the VDS algorithm, such as blood loss during sexual intercourse (P = 0.031) and lower abdominal pain (P = 0.002) were positively associated with the presence of VDS. We did not observe an association between individual STIs and presence of symptoms, although a tendency was observed for M. genitalium infection with presence of VDS symptoms (OR, 2.5; 95% CI, 1.0–6.2 and P = 0.051). Three of 11 symptomatic women with M. genitalium infection had a concurrent T. vaginalis infection.

Figure 1

Figure 1

Adequately treated symptomatic women had a median age of 29 years (range, 18–61 years), compared with a median age of 43 years (range: 19–68) of inadequately treated women (Table 3). Adequate treatment was significantly associated with clinical presentation with vaginal discharge (OR, 2.7; 95% CI, 1.1–7.0 and P = 0.037) and inadequate treatment with dysuria (OR, 7.4; 95% CI, 2.3–24 and P = <0.001). Vaginal discharge was more often health care worker observed in adequately treated women (OR, 4.4; 95% CI, 1.6–12 and P = 0.005) compared to women that were inadequately treated. Furthermore, we found a significant association for lack of condom use (OR, 0.5; 95% CI, 0.4–0.7 and P = 0.001) in inadequately treated women.



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Effectiveness of the Etiological Approach for STI Screening and Management

STIs were detected in 133 (53%) women; only 49 (37%) of these women were symptomatic. Factors associated with STI were: age < 35 years (OR, 2.5; 95% CI, 1.5–4.2 and P = <0.001), literacy (OR, 2.0; 95% CI, 1.1–3.5 and P = 0.022), occasional sexual partner (OR, 1.9; 95% CI, 1.1–3.4 and P = 0.037), intravaginal cleansing (OR, 1.7; 95% CI, 1.1–2.8 and P = 0.040) and the use of alcohol (OR, 2.9; 95% CI, 1.2–6.7 and P = 0.016) (Table 4). C. trachomatis infection was more often seen in younger women (OR, 4.3; 95% CI, 2.1–8.8), women that had an history of STI treatment (OR, 2.8; 95% CI, 1.1–6.8) and those who reported the use of alcohol (OR, 2.4; 95% CI, 1.1–5.4). Factors associated with infection with N. gonorrhoeae were as follows: age, <35 years (OR, 2.6; 95% CI, 1.2–5.4), pregnancy (OR, 11; 95% CI, 1.1–128), practicing anal sex (OR, 0.8; 95% CI, 0.8–0.9) and intravaginal cleansing (OR, 2.6; 95% CI, 1.3–5.3). Women infected with M. genitalium more often reported fellatio (OR, 8.8; 95% CI, 2.8–27), the use of alcohol (OR, 3.3; 95% CI, 1.2–9.2), and experienced sexual coercion (OR, 3.8; 95% CI, 1.5–9.6). Vaginal discharge was significantly associated with M. genitalium (OR, 3.5; 95% CI, 1.3–9.3) and T. vaginalis (OR, 2.8; 95% CI, 1.3–5.7). Also, T. vaginalis infection was significantly associated with having an occasional sexual partner (OR, 2.2; 95% CI, 1.2–4.0).



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In this study, we show that there is a large burden of untreated symptomatic and asymptomatic STIs in a remote area of South Africa with poor access to health care services. We demonstrate that both syndromic and etiological screening and management can contribute to STI control in this setting, but with variable efficiency. To our knowledge, this is one of the first studies showing the importance of out-of-facility STI services through a mobile clinic in a rural area in Africa.

The high proportion (53%) of women infected with at least 1 STI is of concern; the observed prevalence in our study is relatively high, even for South Africa. A recently published structured review showed a prevalence of 7% to 8% of C. trachomatis for studies conducted in community settings and 2% to 28% at PHC facilities; prevalence for N. gonorrhoeae was 1% and 8% to 23%, respectively.6 In addition, recent STI Spectrum model estimates of C. trachomatis and N. gonorrhoeae infection in women of reproductive age are 7% and 15%, respectively.20 The prevalence of C. trachomatis (21%) and especially T. vaginalis (32%) was higher in this study than reported for a similar study of women visiting PHC facilities in the same district several years ago, whereas the prevalence of N. gonorrhoeae (16%) and M. genitalium (8%) was similar.3,21–23 Women in our study reported less often condom use during last sex act (18%) and previous STI treatment (9%) compared with women in the aforementioned facility-based study (36% respectively 22%).21 These findings suggest that lack of access to health care facilities may contribute considerably to the untreated burden of STIs in our region and that a concerning large number of symptomatic and asymptomatic women are left untreated in this area.

Our study confirms the limitations of the syndromic management approach for STI control due to high proportions of asymptomatic infections as reported by various others.10–12 Only 37% of all STI-infected women would have been adequately treated by using the South African syndromic management guidelines for VDS; two thirds of infected women would not have received adequate treatment. However, despite its limitations, the syndromic approach may be useful in a mobile setting with limited diagnostic resources, because 58% of symptomatic women would be treated adequately using this approach. However, as previously suggested, we would advocate for removing the age cutoff from the algorithm, because women 35 years or older with STI would not receive adequate treatment; this is the case in 48 (36%) of 133 women with STI in our study.10 We did not identify clear and useful factors associated with inadequate treatment that could be included in a potentially revised algorithm. Therefore, it should be considered to refer women with persistent or recurrent symptoms for diagnostic testing in case there is no clinical response to syndromic management.

The main limitation of the syndromic approach is that it leaves asymptomatic women with STI untreated. Therefore, systematic screening and diagnostic testing of high-risk asymptomatic women should be considered. Such introduction of etiological approach could be achieved by creating laboratory-based testing infrastructure or by inclusion of near-patient diagnostics in the mobile clinic. The latter has the advantage of same-day diagnosis and targeted treatment for the patient. The GeneXpert platform for near-patient testing for C. trachomatis, N. gonorrhoeae and T. vaginalis provides an opportunity to initiate etiological testing in mobile clinics and has recently been evaluated in 2 studies.8,24 The development of rapid point-of-care testing for M. genitalium is in the pipeline.25 This could be further augmented by building infrastructure for laboratory-based testing for other causes of VDS.

It is imperative to include remote areas in the public health response to the STI epidemic. Provision of STI services through a mobile clinic could address this unmet need. We did not include men in this study, but expect a similar unmet need for STI care. Mobile clinics are proven to be feasible and successful for providing health care in rural and hard-to-reach settings as shown by the implementation of a large infrastructure for mobile clinics in India.26 The first step would be to enhance the implementation of syndromic STI management guidelines across the health care sector and to include the mobile clinics. There is much progress to be made in the quality of provision of STI services in general in South Africa: a recent study that evaluated the quality of STI service delivery through standardized patient actors showed that the syndromic management according to guidelines was provided in only 61% of cases.27 Improvement of services would require deployment of specific resources (treatment) and training of the nurses on STI guidelines and identification of individuals at high risk for STIs. Moreover, a community awareness component would be essential to mobilize symptomatic individuals for STI care. Syndromic management for STIs in South Africa seems to have reached its use-by date and should be replaced by an etiological approach, which should be implemented in mobile clinics too.28 Further research is required to evaluate the full impact on the STI epidemic of delivering STI services through mobile clinics in resource-constraint remote settings and the potential effectiveness of implementing a combined symptomatic and etiological approach to STI control. A cost evaluation for delivering reproductive and primary health care services through a mobile clinic in South Africa, has shown that staffing costs are the largest component of providing mobile health services to rural communities; screening and treatment of STI had marginal cost.29

This study has several limitations. First, although the women in our study were invited for any of the health care services provided by the mobile clinic, we cannot rule out that some degree of selection of high-risk women occurred, resulting in an overestimation of prevalence. Second, we only recruited women in this study and the results cannot necessarily be translated to providing STI services in mobile clinics for men in general, and those with male urethritis syndrome in particular. Furthermore, the study was only conducted in 1 mobile clinic and operational factors may impact on generalizability of the implementation results. Finally, collection of sexual behavior data can be challenging and may have results in underreporting of sexual risk behavior by participants.

In conclusion, this study emphasizes the importance of providing STI services in remote areas with poor access to health care services to address the large STI epidemic in South Africa. In such areas, symptomatic STI screening and treatment through mobile clinics provides an important initial intervention that has to be enhanced by introduction of, preferably near-by patient, etiological testing and STI management.

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