Coinfection rates of HIV and sexually transmitted infections (STIs) are not widely reported in Zimbabwe and no local guidelines regarding the screening of STIs in people living with HIV exist.
This cross-sectional study was conducted to determine the prevalence and associated risk factors for STI coinfection in a cohort of HIV-infected women.
Between January and June 2016, 385 HIV-infected women presenting for routine cervical cancer screening were tested for five STIs:
Two hundred and thirty-three participants (60.5%) had a confirmed positive result for at least one STI: HSV 2 prevalence 52.5%, TV 8.1%, CT 2.1%, NG 1.8% and TP 11.4%. Eighty-seven per cent of the women were asymptomatic for any STI; 62.3% of women with a non-viral STI were asymptomatic. Women who had attended tertiary education were 90% less likely to have a non-viral STI (adjusted odds ratio [aOR]: 0.10, 95% confidence interval [CI]: 0.03–0.39,
A high prevalence of predominantly asymptomatic STIs is reported in a cohort of HIV-infected women. Syndromic management results in underdiagnosis of asymptomatic patients. More than three lifetime sexual partners and less formal education are risk factors for coinfection with non-viral STI. High-risk women should be screened using aetiological methods.
Sexually transmitted infections (STIs) and their many sequelae are among the top five reasons that adults seek healthcare in low-income settings.
HIV and STIs share a complex bidirectional relationship. STIs increase HIV viral shedding in the genital tract, resulting in significant increases in HIV transmission risk. Local inflammation activates HIV replication in the genital compartment independent of HIV in peripheral blood. An individual may have an undetectable plasma HIV viral load (VL), while the genital tract VL is elevated.
The prevalence of STIs varies according to region, gender and risk group. A number of key populations with high prevalence of STIs have been reported. These include sex workers, their clients and other partners; men who have sex with men; transgender people; people who inject drugs; and people living with HIV (PLWH). Enhanced STI screening is recommended in these key populations.
This analytic cross-sectional study was conducted in HIV-infected adult women at Newlands Clinic (NC), Harare, Zimbabwe. NC provides comprehensive HIV care and treatment services to approximately 6000 individuals in the greater Harare urban area. The clinic operates in a public-private partnership with the Ministry of Health and Child Care, Zimbabwe. Funding for the clinic is provided by the Ruedi Luethy Foundation and other partners.
A questionnaire was verbally administered by a trained study nurse, which collected sociodemographic, medical, gynaecological and sexual history data. Current CD4+ count, HIV VL and antiretroviral therapy (ART) history were documented in the medical history. Current CD4+ count and VL were defined as results which had been obtained within the preceding month. The sexual history included questions regarding age of sexual debut, number of sexual partners, type of sexual activity, STI symptoms, previous STI diagnoses, condom use, family planning, sexual orientation and past history of sexual abuse.
On completion of the questionnaire, a complete abdominal and gynaecological examination including the collection of endocervical swabs was conducted. Findings were recorded on a participant’s respective case report forms. On completion of endocervical swab collection, the nurse proceeded with an examination of the cervix using the visual inspection with acetic acid and cervicography (VIAC) methodology. The swabs were used for
A 4 mL blood sample was collected into a clot activating tube and processed for onsite testing. Processing involved centrifuging of the sample after clotting and harvesting the serum for subsequent tests. Herpes simplex virus type 2 infection was tested in serum using PreCheck HSV 2 IgG test kits. The seroprevalence of syphilis was defined as having a positive treponemal-specific antibody test using the SD Bioline Rapid Antibody Test with or without a positive non-treponemal RPR carbon assay. All participants with confirmed STI diagnoses were managed using an aetiological approach, and respective antibiotic treatment was administered as recommended in the national guidelines.
VL measurements were performed on EDTA plasma using the Roche COBAS Ampliprep and TaqMan version 2.0, while CD4+ counts were measured in whole blood using a Partec Cyflow Counter II.
Data were entered into a Microsoft Access 2016 database and then exported to Microsoft Excel for cleaning. Cleaned data were exported to Stata 12.1 for analysis. Medians and interquartile ranges (IQR) were used to describe continuous data. A maximum
The study was approved by the NC Research Unit and the Medical Research Council of Zimbabwe (approval number MRCZ/A/1980). All participants provided written informed consent before enrolling in the study.
Between 01 January and 30 June 2016, 385 women were enrolled in the study, 356 (93.0%) being on ART. The median age of the participants was 41 years (IQR: 35–47). A total of 171 (44.0%) participants were married and 103 (27.0%) were widows; 86 (22.0%) had seven years or less of education and 57 (15.0%) had reached tertiary education.
Participant characteristics (
Characteristic | Frequency |
||
---|---|---|---|
% | IQR | ||
41 | - | 35–47 | |
Married | 171 | 44.4 | - |
Widowed | 103 | 26.8 | - |
Divorced/separated | 62 | 16.1 | - |
Single | 49 | 12.7 | - |
503 | - | 347–655 | |
< 1000 copies/mL | 347 | 97.5 | |
< 50 copies/mL | 324 | 91.0 | |
6.2 | - | 3.2–9.0 | |
Age at sexual debut, years, median (IQR) | 19 | - | 17–21 |
Condoms use for last sex | 242 | 62.9 | |
Positive | 196 | 50.0 | - |
Negative | 66 | 17.1 | - |
Unknown | 123 | 32.0 | - |
166 | 43.1 | - | |
47 | 12.2 | - | |
26 | 6.8 | - | |
32 | 8.3 | - |
IQR, interquartile range; ART, antiretroviral therapy; STI, sexually transmitted infections.
Of the 356 (93.0%) participants who were taking ART, 324 (91.0%) were virologically suppressed with VLs of < 50 copies/mL. Twelve (3.0%) were severely immunocompromised (CD4+ cell count < 100 cells/μL), but the majority were immunocompetent with the median CD4+ cell count being 503 (IQR: 347–655) cells/μL. Among those receiving ART, the median duration on ART was 6.2 years (IQR: 3.2–9.0) and 323 women (84.0%) were taking a first-line ART regimen.
Forty-three percent of the women reported having a previous STI, diagnosed using the syndromic management approach. The majority of patients (
Of the 385 participants screened, 233 (61.0%) women had at least one confirmed result for an STI (HSV-2, TV, NG, CT, syphilis). Seventy-nine (21.0%) women had at least one non-viral STI (TV, NG, CT, syphilis). Eleven (3.0%) women were coinfected with two non-viral STIs: six were positive for syphilis and TV, three for TV and NG and two for TV and CT.
Prevalence of sexually transmitted infections (
Women who had attended tertiary education were 90% less likely to have a non-viral STI compared with those without any education (adjusted odds ratio [aOR]: 0.10, 95% CI: 0.03–0.39,
Patient characteristics as risk factors for non-viral sexually transmitted infections.
Risk factor | All women |
Non-viral STI positive |
OR (95% CI, |
aOR (95% CI, |
||
---|---|---|---|---|---|---|
% | % | |||||
≤ 25 | 20 | 5.2 | 7 | 35.0 | - | - |
26–35 | 80 | 21.9 | 22 | 27.5 | 0.51 (0.25–1.99, 0.51) | - |
> 35 | 285 | 78.1 | 50 | 17.5 | 0.39 (0.09–1.04, 0.06) | - |
None | 24 | 6.2 | 9 | 37.5 | - | - |
Primary | 62 | 16.1 | 19 | 30.7 | 0.73 (0.27–1.98, 0.54) | 0.79 (0.28–2.24, 0.65) |
Secondary | 242 | 62.9 | 47 | 19.4 | 0.39 (0.15–1.00, 0.05) | |
Tertiary | 57 | 14.8 | 4 | 7.0 | ||
1 | 91 | 23.6 | 9 | 9.9 | - | - |
2 | 88 | 22.9 | 13 | 14.8 | 1.57 (0.64–3.90, 0.32) | 1.55 (0.60–3.99, 0.37) |
≥ 3 | 206 | 53.5 | 57 | 27.7 | ||
Casual | 12 | 3.1 | 0 | - | - | - |
Regular | 373 | 96.9 | 79 | 21.2 | - | - |
Yes | 246 | 63.9 | 53 | 21.5 | - | - |
No | 139 | 36.1 | 26 | 18.7 | 0.83 (0.50–1.41, 0.51) | - |
No | 312 | 81.0 | 54 | 17.3 | - | |
Yes | 73 | 19.0 | 25 | 34.3 | ||
No | 219 | 56.9 | 39 | 17.8 | - | - |
Yes | 166 | 43.1 | 40 | 24.1 | 1.46 (0.89–2.40, 0.13) | - |
< 16 | 25 | 6.5 | 7 | 28.0 | - | - |
16–20 | 237 | 61.6 | 59 | 24.9 | 0.85 (0.34–2.14, 0.73) | 1.30 (0.49–3.51, 0.60) |
123 | 31.9 | 13 | 10.6 | 0.60 (0.19–1.86, 0.37) | ||
No | 333 | 86.5 | 68 | (86.1 | - | - |
Yes | 52 | 13.5 | 11 | 13.9 | 1.05 (0.51–2.14, 0.90) | - |
OR, odds ratio; CI, confidence interval; STI, sexually transmitted infection.
Note: Bold values indicate statistically significant,
Our study reports a high prevalence of STIs in a cohort of HIV-infected women in Zimbabwe. Sixty-one per cent of women had a positive confirmatory test for any STI and approximately one in five women was diagnosed with a treatable non-viral STI. The majority of the women in this study (62.0%) were asymptomatic at the time of diagnosis of non-viral STIs and would therefore not have received treatment using the current syndromic management guidelines. A wide variation in STI prevalence data collected mostly through antenatal programmes has been presented across different low- and middle-income countries.
Reported syphilis prevalence in this study is significantly higher (11.0%) than what has been previously described in Zimbabwean cohorts. Gwanzura et al. reported a prevalence of 2.3% in male factory workers. The prevalence of active syphilis in HIV-infected women and all antenatal clinic attendees has been previously reported at 4.0% and 1.2%, respectively.
The second most prevalent non-viral STI in this study was TV, which was confirmed in 8.0% of the participants. Similar to other STIs, it is increasingly recognised that TV plays an important role in increasing the risk of both acquisition and onward transmission of HIV. Using mathematical models, Quinlivan et al. estimated that 22.0% of projected HIV transmissions from women in the United States are attributable to TV infections and up to 2.0% of all HIV transmissions in the United States may be related to TV infection.
The prevalence of infection with chlamydia varies significantly between regions, countries and risk groups. The prevalence of NG and CT in our study was 1.8% and 2.1%, respectively. Studies conducted in Kenya, Zimbabwe, Nigeria and South Africa have shown that the prevalence of CT varied between 6.0% and 20.0% in these countries.
An HSV 2 seropositivity rate of 52.0% is in keeping with global published rates in PLWH of 50.0% – 90.0%.
Analysis from this study suggests that women with less formal education were more likely to be diagnosed with an STI; this is consistent with findings from other similar studies. Quinlivan et al. found a five-fold increase in risk of infection with TV in women living with HIV with low reported education status.
Multivariate analysis revealed that women reporting more than three lifetime sexual partners were three times as likely to be diagnosed with a non-viral STI. Taking a thorough sexual history is an important tool in risk profiling of patients, and in countries where resources are limited, it can enable healthcare professionals to target high-risk patients for targeted screening. Participants in this study were not recruited based on symptoms. However, on completion of a detailed sexual history, 13.0% of women reported ongoing symptoms consistent with an STI diagnosis. Possible reasons for participants delaying in seeking treatment include stigma associated with an STI diagnosis.
The prevalence of previous or current sexual abuse and/or intimate partner violence (IPV) was reported in this study. Our results are consistent with published data reporting a strong association between IPV and HIV infection.
This study highlights an unrecognised burden of STIs and defines an at-risk population of HIV-infected women. An important limitation of the study is, however, the lack of generalisability of our results to all HIV-infected women, as participants were recruited from one urban site. The cohort also did not include key populations such as sex workers or adolescents and young adults. The investigators did not survey any additional anatomical sites; consequently, the results for this study focus on vaginal and cervical STIs (except for syphilis). Women were asked to report historical events which may introduce recall bias particularly relating to number of sexual partners and condom use.
In conclusion, we have reported a high prevalence of non-viral STIs in a cohort of largely asymptomatic HIV-infected women. Those reporting more than three lifetime partners and with less formal education were at higher risk of STI acquisition. The major strategy in most resource-poor settings for STI control is focused on syndromic management of genitourinary infections. Although we recognise this is an important public health measure, this hidden epidemic may be associated with significant morbidity and drives onward HIV transmission. STI control remains an important aspect of HIV prevention. These results emphasise the need for identification of high-risk women through routine sexual history checking and targeted aetiological screening of high-risk individuals for asymptomatic STIs. There is an increased role for diagnostic technology which can be used for surveillance and STI screening of at-risk women. Polymerase chain reaction and point-of-care diagnostic technology need to be included as part of rapid STI treatment modalities.
The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.
S.L. was responsible for the conception of the study and its design, drafting of the manuscript and analysis of data. P.M. was responsible for data collection. M.P. supervised the research process and contributed to the analysis of the data and write-up. A.M. was responsible for managing the study data, follow-up of patients and assisted with the write-up. T.M., T.S., R.L. and C.C. assisted with study conception, data analysis and write-up. All the authors revised the draft critically and gave fnal approval of the version to be published. All authors read and approved the fnal manuscript.