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Integrating Cervical Cancer Screening Into Safer Conception Services to Improve Women's Health Outcomes: A Pilot Study at a Primary Care Clinic in South Africa

Integrating Cervical Cancer Screening Into Safer Conception Services to Improve Women's Health... ORIGINAL STUDY Integrating Cervical Cancer Screening Into Safer Conception Services to Improve Women's Health Outcomes: A Pilot Study at a Primary Care Clinic in South Africa Natasha E.C.G. Davies, MPH,* Matthew Chersich, PhD,* Saiqa Mullick, PhD,* Nicolette Naidoo, MPH,* Nokuthula Makhoba, MPH,* Helen Rees, MRCGP, MRCOG,* and Sheree R. Schwartz, PhD*† of clients were eligible for cervical cancer screening and 85% (321 of Background: Sub-optimal cervical cancer screening in low- and middle- 376) of these completed screening. More than half had abnormal cervical income countries contributes to preventable cervical cancer deaths, partic- pathology (185 of 321) and 20% required colposcopy for possible high- ularly among human immunodeficiency virus (HIV)-positive women. We grade or persistently atypical lesions (64 of 321). Compared with HIV- assessed feasibility and outcomes of integrating cervical cancer screening negative women, abnormal pathology was more likely among HIV-positive into safer conception services for HIV-affected women. women, both those on ART <2 years (adjusted prevalence ratio, 2.5; 95% Methods: At a safer conception service in Johannesburg, South Africa, confidence interval, 1.2–5.0) and those on ART 2 years or longer (adjusted HIV-affected women desiring pregnancy received a standard package of care prevalence ratio, 2.1; 95% confidence interval, 1.0–4.2). designed to minimize HIV transmission risks while optimizing prepregnancy Conclusions: Integrating cervical cancer screening into safer conception health. All eligible women were offered Papanicolaou smear, and those with care was feasible with high coverage, including for HIV-positive women. significant pathology were referred for colposcopy before attempting pregnancy. Significant pathology, requiring colposcopy, was common, even among Multivariable analyses identified associations between patient characteristics and healthy women on ART. Safer conception services present an opportunity abnormal pathology. for integration of cervical cancer screening to avert preventable cancer- Results: In total, 454 women were enrolled between June 2015 and April related deaths among HIV-affected women planning pregnancy. 2017. At enrolment, 91% were HIV-positive, 92% were on antiretroviral ther- apy (ART) and 82% virally suppressed. Eighty-three percent (376 of 454) ach year over 250,000 women die of cervical cancer, a prevent- Eable condition. In high-income countries, population-level From the *Wits Reproductive Health and HIV Institute, Faculty of Health cervical cancer screening programs have effectively reduced cervi- Sciences, University of the Witwatersrand, Johannesburg, South Africa; and †Department of Epidemiology, Johns Hopkins School of cal cancer associated morbidity and mortality. Unfortunately, in Public Health, Baltimore, MD the most affected low- and middle-income countries (LMICs), Conflict of Interest: None declared. screening coverage remains low. In South Africa, for example, Sources of Funding: This work was partially supported through USAID, poor program coverage contributes to over 4000 cervical cancer Cooperative Agreement AID-674-A-12-00021 (Health System Strengthening deaths each year, making cervical cancer the leading cause of ABF 393). USAID funding provided support for the costs of safer cancer deaths in women of reproductive age. Integration of conception clinic staffing, training and development of job aides and cervical cancer screening into human immunodeficiency virus the creation of information, education and communication materials (HIV) programming in LMICs, such as South Africa, is particularly to advertise the new service. The implementation took place at a Gauteng important as this cancer disproportionately affects HIV-positive Department of Health (DOH) facility supported by DOH staff. The 5 6 authors' views expressed in this publication do not necessarily reflect women, even once they commence antiretroviral therapy (ART). the views of the United States Agency for International Development Screening opportunities for HIV-infected women are, however, or the United States Government. frequently missed due to low awareness and poorly integrated Correspondence: Natasha E.C.G. Davies, MPH, Wits RHI, Hillbrow Health 3,7 services. Considering the dual burden of HIV and cervical Precinct, 22 Esselen Street, Hillbrow, 2001, Johannesburg. South Africa. cancer seen in many LMICs, integrating cervical cancer E‐mail: ndavies@wrhi.ac.za. screening, and other sexual and reproductive health (SRH) services Acknowledgements: The authors are grateful to the study participants and into established HIV programs is clearly a priority. to the study team for their time and dedication to the work. The Built on a framework of reproductive rights, comprehen- authors thank the Hillbrow Community Health Centre, the City of sive safer conception services support HIV-affected couples to Johannesburg and the Department of Health for their support of the project. The authors thank USAID and the United States Government safely achieve their fertility goals while minimizing risks of hori- for providing funding support. zontal or vertical HIV transmission, and optimizing the couples' Received for publication June 20, 2018, and accepted September 9, 2018. overall health status before a pregnancy. In South Africa, over half DOI: 10.1097/OLQ.0000000000000914 of women accessing ART are of reproductive age and many express Copyright © 2018 The Author(s). Published by Wolters Kluwer Health, 10 adesireto havechildrennow or in thefuture. Recognizing this Inc. on behalf of the American Sexually Transmitted Diseases Associ- overlap between HIV and fertility desires, safer conception ation. This is an open-access article distributed under the terms of the services are recommended as part of the South African National Creative Commons Attribution-Non Commercial-No Derivatives License Contraceptive and Fertility Policy released in 2012. Such services 4.0 (CCBY-NC-ND), where it is permissible to download and share create a valuable opportunity for HIV and SRH integration, the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. including for cervical cancer screening. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 91 � Davies et al. This study aimed to investigate the feasibility of inte- model and integrate services into nine primary healthcare facilities grating cervical cancer screening into safer conception services in other parts of inner-city Johannesburg. as one component of a comprehensive package of care. The study, in Johannesburg, South Africa, was set within one of the first Study Population public sector safer conception services in the country. We also All women of reproductive age who were in an HIV-affected sought to assess the outcomes of cervical cancer screening. relationship (HIV seroconcordant, serodiscordant, or where one part- ner had unknown HIV status) who currently desired pregnancy were eligible to attend the service, with or without their partner. METHODS Men and women self-referred after hearing about the safer con- ception service during health talks presented in clinic waiting areas, from leaflets and posters within the facility, or by word of Study Context mouth. In addition, facility staff referred clients whom they In April 2015, a safer conception clinic was established in a screened as currently desiring pregnancy. busy, community health care center in inner-city Johannesburg. The facility offers general services and has an ART clinic, attended by over 21,000 HIV-positive clients. Although national policies Cervical Cancer Screening Process have supported the provision for safer conception services since Clients were provided with a standard package of safer con- 2012, no standardized, integrated approach or public sector ser- ception care with the aim of optimizing their health status before vice delivery model has been developed. In particular, prior to in- pregnancy and minimizing HIV transmission risks, including troducing the safer conception service at the facility, screening for cervical cancer screening in the form of a Pap smear which was fertility intentions was ad hoc, and the provision of SRH services, 14 conducted according to national guidelines. The HIV–positive including family planning and cervical cancer screening for HIV- women, regardless of age, were eligible for a Pap smear if they positive women, took place in a separate building from the ART had never been screened before, or they reported having been clinic, staffed by different providers. Patients requesting these ser- screened, but no result could be traced, their last abnormal vices were referred to the relevant providers. Pap smear was more than 12 months ago, or they had a normal Recognizing the lack of service integration, a safer concep- result more than 24 months previously. The HIV–negative tion clinic was introduced as a dedicated service which operated women were offered cervical cancer screening if they were older within the same building as the ART clinic. The service was than 30 years and had not had a normal Pap smear result in the past rendered by primary healthcare nurses who were supervised 10 years. Screening tests for human papillomavirus (HPV) were by a doctor and had received training in safer conception care. unavailable within public sector facilities at the time of this study. An integrated package of care was provided prepregnancy during Women who were eligible for a Pap smear were offered the the baseline visit and subsequent monthly to three monthly follow- service on the same day as their baseline visit, unless they were up visits. The package included risk reduction (safer conception) menstruating, in which case it was conducted at their next visit. counseling, support for HIV status disclosure, partner HIV testing, Most smears were performed by the safer conception service ART for women and their partners, preexposure prophylaxis for nurses in a one-stop shop approach, although some were done HIV-negative partners, screening and management of sexually by a postnatal clinic nurse situated in a nearby room during periods transmitted infections (STIs), care for comorbid opportunistic in- of high patient load. fections or noncommunicable diseases for both members of the Pap smear results, which have a reported sensitivity and couple, and cervical cancer screening for women with referral specificity of 75.8% and 83.4%, respectively, were available for further management where indicated. within 4 to 6 weeks. If required, women were referred to the onsite Services were delivered according to national guidelines. colposcopy service and advised to delay pregnancy attempts until In the case of cervical cancer screening, South Africa's recommen- their colposcopy results indicated no need for further manage- dations differ somewhat from international norms, with screening ment. This approach was taken given the risks of having untreated for HIV-negative women being conducted once in their third, abnormal cervical pathology during pregnancy including preg- fourth and fifth decades of life, and HIV-positive women being nancy loss and premature labor and delivery. The rationale for screened as soon as they are diagnosed with HIV infection and delaying pregnancy attempts was explained to each woman, and then every 1 to 3 years thereafter. her partner if present. Care was taken to minimize the anxiety Donor funding supported the safer conception clinic associated with receipt of abnormal Pap smear results while staffing, including clinical, administrative and research staff, job supporting the couple to delay pregnancy until any abnormal pa- aides and distribution of communication materials to inform pa- thology had been addressed. tients attending the clinic of this new service. Routine clinical pro- cedures, such as ART supply and Pap smears were funded through Data Collection and Analysis the Department of Health and the project was implemented at a Department of Health public sector facility. The only noninte- Data on patient demographics and health status were cap- grated component was medical male circumcision; male partners tured on case report forms, medical history was extracted from pa- who requested this intervention were referred to the medical male tient medical records and clinical data were collected during circumcision clinic within the same facility. Additionally, donor- procedures performed as part of the service. Results of Pap smears supported, colposcopy services, which had previously only been and colposcopy were obtained by reviewing women's clinical file available at a nearby tertiary hospital, had recently been estab- notes or searching the database of the National Health Laboratory lished at the study facility. No services for infertility were pro- Service, where all the samples were assessed. Data were entered vided at the clinic. If women did not conceive within 6 to into a REDCap database and analyzed in STATA 14 (College 9 months of trying they were offered referral to a low-cost fertility Station, TX). service in Pretoria, a city about 50 km away. Coverage (percentage of clients offered screening) and up- Enrolment into the demonstration project was completed in take (percentage of clients offered screening who had a Pap smear April 2017; however, efforts have been undertaken to adapt the done) were assessed. Characteristics of women who had a Pap 92 Sexually Transmitted Diseases Volume 46, Number 2, February 2019 � Integrating Safer Conception and Cervical Screening smear were compared with those who did not using χ tests or (M150146). The study was conducted according to good clinical nonparametric equality of medians tests, as appropriate. practice guidelines and all enrolled clients completed written, Analysis focused on 2 outcomes of interest: (1) women informed consent. with any abnormal Pap smear and (2) women with significant pa- thology requiring colposcopy. Significant pathology included: RESULTS high-grade squamous intraepithelial lesions (HSIL); persistent Overall, 454 women attended the safer conception service. low-grade squamous intraepithelial lesions (LSIL) or atypical Of these, 91% (n = 413 of 454) were HIV-positive, having had a squamous cells of unknown significance; or any smear in which positive HIV test a median of 5 years ago (interquartile range, HSIL or cervical intraepithelial neoplasia (CIN) I or II could not 3–9). The vast majority (92%, 382 of 413) were already on ART, be excluded. with 19% (n = 71 of 382) having initiated in the past year; 51% Pap smear results are presented and modified robust had a CD4 cell count 500 cells/mm or greater and only 7% had Poisson regression was used to separately assess correlates of a CD4 cell count 200 cells/mm or less. Overall, 75% (n = 311 having an abnormal Pap smear and having a result requiring col- of 413) of HIV-positive women had an undetectable viral load poscopy. Robust Poisson regression was used given that the prev- (<50 copies/mm ) at their baseline visit, and viral suppression alence of the outcome was greater than 10% and the log binomial was 82% among those taking ART (311 of 382). models failed to converge consistently. Bivariate analyses iden- Of all women, 83% (n = 376 of 454) were eligible for a Pap tified associations between demographic and clinical characteris- smear (Fig. 1). Of these, 18 were never offered a Pap smear by the tics and the two outcomes of interest (abnormal Pap smear and provider, representing missed screening opportunities due to pro- significant pathology requiring colposcopy). The final, multivari- vider oversight (n = 358 of 376 or 95% screening coverage). A able models included age, based on face validity and apriori hypotheses, and variables associated with the outcome in the bi- further 30 women were offered screening, but did not take it up variate analysis at P value less than 0.10. (92% uptake). No differences were detected in demographic or clinical characteristics between the 15% (n = 70 of 454, Fig. 1) of women who recently had a Pap smear and those who did not. Ethics Overall, a Pap smear was performed for 87% (n = 328 of 376) Ethical approval was secured from the Human Research of eligible women, 93% (n = 306) of whom were HIV-positive. Ethics Committee of the University of the Witwatersrand Women who were eligible for a Pap smear, but did not receive Figure 1. Flow diagram of females enrolled and accessing cervical cancer screening via safer conception service. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 93 � Davies et al. one, were more likely to be lost to follow-up after their baseline About three quarters of the 64 women who required colpos- safer conception visit, precluding an opportunity to conduct the copy had a traceable histology result (n = 47, 73%) (Table 2). None Pap smear during follow-up (31% compared with 8% among of these women had invasive malignancy. Twenty-five (53%) women who did receive a Pap smear, P <0.01). women had evidence of HSIL or CIN II/III, with 20 of these hav- Across all demographic and clinical variables, the only dif- ing incomplete resection at the biopsy margins. These women re- ference detected between those accessing Pap smears through the quired further follow-up, but no records of a repeat colposcopy safer conception service was HIV status, with those receiving a could be located. Among the 64 women, 9 had a confirmed preg- Pap smear being more likely to be HIV-positive (Table 1). nancy, 2 of whom conceived before colposcopy was performed. Of the 321 results available for analysis (7 results were un- No difference was detected in rates of retention in the safer con- traceable), 58% (n = 185 of 321) had abnormal cytology, equating ception service between women referred for colposcopy and to 41% (185 of 454) of all women attending the clinic (Table 2). In women not requiring colposcopy (95% vs. 91%, P =0.30). total, 20% of those who had an abnormal Pap smear result (n = 64 of 321) required colposcopy prior to beginning pregnancy attempts, DISCUSSION which translates into 14% (64 of 454) of all women attending the clinic. Among women requiring colposcopy, 31% (n = 20 of 64) Three key findings emerge from this study. First, integra- were younger than 30 years. Additionally, bacterial vaginosis was tion of cervical cancer screening into safer conception services is detected in 38% (n = 122 of 321) of Pap smears and Trichomonas feasible and is associated with high coverage and uptake. Most vaginalis (TV) in 3.4% (n = 11 of 321). women, despite accessing routine HIV services, had not previ- In the bivariate robust Poisson regression assessing corre- ously been screened for cervical cancer, illustrating the importance lates of having a Pap smear result of any abnormal cytology, only of integration initiatives, such as done in this study. Second, rou- HIV status was associated with having an abnormal Pap smear tine cervical cancer screening identifies high levels of significant (Table 3). These results were robust in the multivariable model, pathology, particularly among HIV-positive women. Of all women with only minor changes noted to point estimates. Being HIV- attending the clinic, around 40% had abnormal pathology and one positive increased the magnitude of risk for an abnormal Pap in seven required colposcopy. Third, significant pathology is com- smear about 2-fold, regardless of whether a woman had not begun mon despite a large proportion of these women being on ART for ART, or had received ART for under 24 months or for over several years. This reiterates the importance of cervical cancer 24 months. Relationships were similar in the models assessing cor- screening, regardless of ART status. relates of Pap smear results requiring colposcopy; the magnitude Overall, the study supports increasing calls to improve inte- of the association between HIV and duration of ART use was gration of SRH services—including cervical cancer screening and 8,19 stronger for the colposcopy outcome, though statistical signifi- family planning—with HIV services. The benefits of such in- cance was not reached. tegration have been demonstrated across numerous countries and TABLE 1. Demographics of Female Clients Attending a Safer Conception Service (N = 454) Women With Pap Smear Women With No Pap Smear Done While Attending Safer Done While Attending Safer Characteristics Conception Service (n = 328) Conception Service (n = 126)* P Age: n (%), y 0.86 18–24 19 (5.8%) 10 (7.9%) 25–29 70 (21.3%) 25 (19.9%) 30–34 117 (35.7%) 45 (35.7%) ≥35 122 (37.2%) 46 (36.5%) 306 (93%) 107 (85%) HIV-positive, n (%) 0.01 Years since HIV diagnosis, median (IQR) 5.5 (2.7–8.7) 5.1 (2.9–8.4) 0.82 On ART at enrolment, n (%) 281 (92%) 101 (94%) 0.39 Years on ART at enrolment, median (IQR) 3.2 (1.6–6.1) 2.9 (1.2–5.2) 0.26 Latest CD4 count at enrolment, median (IQR) 500 (364–631) 508 (351–689) 0.73 Viral load <50 copies/mL at enrolment, n (%) 230 (75%) 81 (76%) 0.80 Nationality, n (%) 0.78 South African 180 (55%) 71 (56%) Non-South African 148 (45%) 55 (44%) Highest educational level completed, n (%) 0.17 Primary school or less 21 (6%) 12 (10%) Some high school but not completed 127 (39%) 38 (30%) High school or higher completed 179 (55%) 76 (60%) 208 (63%) 73 (58%) Employed, n (%) 0.28 Monthly income in USD, median (IQR)† 222 (0–296) 200 (0–356) 0.92 Partner circumcised, n (%) 163 (51%) 65 (52%) 0.83 Smoker, n (%) 29 (9%) 11 (9%) 0.98 Totals vary due to missing data for some variables. * Pap smear not done for 126 women while they attended the safer conception service includes 78 women who were not eligible for a Pap smear and 48 women who were eligible, but did not access a Pap smear. † South African Rand to US Dollar (USD) exchange rate 13.5:1. IQR, interquartile range. 94 Sexually Transmitted Diseases Volume 46, Number 2, February 2019 � Integrating Safer Conception and Cervical Screening For example, at the nearby tertiary hospital, only 250 to 300 TABLE 2. Pap Smear and Colposcopy Outcomes for Safer 13 women access colposcopy annually. Thus, even if current efforts Conception Service Clients (N = 321)* to decentralize colposcopy services to district or primary level care Number Proportion are intensified, only a small portion of need would be met if rates Pap Smear Outcomes (N = 321) (%) [95% CI] of pathology were universally as high as seen in this study. This study therefore reinforces growing calls for South Africa to No action required 136 42% [37–48] 14,23 review their cervical cancer screening recommendations, NILM Repeat Pap smear required in 12 months 121 38% [33–43] particularly with a view to expanding the “see and treat” approaches LSIL 90 to bypass weak referral pathways and reduce demand for ASCUS 31 colposcopy. This would also avoid the need for, and associated Colposcopy referral required 64 20% [16–25] costs of, repeated follow-up visits by clients. HSIL 36 Ideally, such a shift in approach would be accompanied by LSIL or ASCUS 15 the introduction of HPV testing. This would improve the ability to cannot exclude HSIL or CIN I/II triage women at highest risk of cervical cancer, enabling them to Atypical cells/persistent atypia 13 be prioritized for further management. In an evaluation of HPV (LSIL or ASCUS) testing, Pap smear, and visual inspection with ascetic acid (VIA), Colposcopy Outcomes (N = 64) Firnhaber et al reported sensitivity/specificity rates of 92%/ No record of colposcopy result 11 17% 51.4% for HPV, 75.8/83.4% for Pap smear and 65.4/68.5% Repeat pap result traced, no 69% for VIA when used to screen HIV-infected women in South colposcopy result traced Africa. In light of the high sensitivity of HPV screening but lower No dysplasia reported 2 3% specificity, a combined approach, using both HPV screening and Total with LSIL 20 31% [20–44] VIA, or HPV screening, Pap smear, and colposcopy would help LSIL with complete resection 13 20% to optimize the potential benefits while reducing the potential at margins harm of unnecessary interventions, such as colposcopy. This LSIL with incomplete resection 711% combined approach would help to avoid exposing women to at margins Total with HSIL/CIN III 25 39% [27–52] unnecessary discomfort, significant anxiety and potential harm HSIL or CIN III with complete 58% associated with colposcopy or other treatment modalities. resection at margins Both bacterial vaginosis (BV) and TV are associated with HSIL or CIN III with incomplete 20 31% increased HIV transmission and acquisition risks, as well as nega- resection at margins tive birth outcomes, including miscarriage and preterm labor and delivery. Detecting BV and TV at the time of cervical cancer *N = 321 because 7 (2%) of 328 Pap smears had no traceable result. screening enabled us to manage these conditions effectively. Fur- NILM, negative for intraepithelial lesion or malignancy; ASCUS, atypical thermore, the relatively high rate of BVand TV seen in our cohort squamous cells of unknown significance; 95% CI, 95% confidence interval. may suggest that we saw the “tip of the iceberg” of underlying STIs, as gonorrhea, chlamydia, and herpes simplex virus are not 20,21 service delivery models. In this study, the levels of coverage detected on Pap smear. In settings like South Africa, where and uptake observed suggest a high level of client acceptability. clinicians rely on a syndromic approach to STI screening and In South Africa, almost all colposcopy services are provided in management, many asymptomatic infections are missed. tertiary-level facilities, with long waiting lists and limited capacity. Samples collected during cervical cancer screening could also be TABLE 3. Bivariate and Multivariable Correlates of Any Abnormal Pap Smear Result or Results Requiring Colposcopy (N = 321) Correlates of Having an Abnormal Correlates of Having a Pap Smear Pap Smear Result Requiring Colposcopy Crude Prevalence Adjusted Prevalence Crude Prevalence Adjusted Prevalence Characteristics Ratio (95% CI) Ratio (95% CI) Ratio (95% CI) Ratio (95% CI) Age, y <30 Reference Reference Reference Reference ≥30 0.86 (0.71–1.05) 0.86 (0.71–1.05) 0.84 (0.53–1.35) 0.87 (0.55–1.39) Employment status Unemployed Reference — Reference — Employed 1.06 (0.87–1.28) — 1.16 (0.74–1.81) — Income (above/below median) <219 USD/month Reference — Reference — ≥219 USD/month 0.94 (0.77–1.14) — 0.79 (0.50–1.24) — Completed high school No Reference — Reference — Yes, high 0.99 (0.82–1.19) — 1.21 (0.77–1.89) — school or beyond HIV and ART HIV-negative Reference Reference Reference Reference HIV-positive, not yet begun ART 2.05 (0.95–4.42) 2.01 (0.93–4.32) 2.64 (0.29–23.66) 2.58 (0.29–23.04) HIV-positive, ART <2 years 2.47 (1.23–4.97) 2.47 (1.22–4.96) 6.67 (0.96–46.61) 6.66 (0.95–46.66) HIV-positive, ART ≥2 years 2.08 (1.04–4.17) 2.14 (1.06–4.30) 3.92 (0.56–27.38) 4.02 (0.57–28.55) Models estimated using robust Poisson regression. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 95 � Davies et al. used to conduct increasingly affordable point-of-care diagnostic estimates. To address this limitation, we also assessed the predic- tests for STIs. There is clearly an opportunity, within integrated tors of having any abnormal Pap smear result and found the results services, to introduce molecular testing not only for HPV, but to be robust across the two models. Additionally, although we also for other common STIs. Assessment is needed of the costs of aimed for a fully integrated service with all Pap smears pro- this approach, weighed against the potential benefits of reducing vided within the safer conception clinic, this was not always cervical cancer, mitigating HIV transmission risks, reducing possible, perhaps contributing to missed opportunities. Going poor obstetric outcomes and minimizing infertility related to forward, complete service and provider-level integration would STIs. Enhanced screening services could also incorporate be recommended. screening and management of other conditions, such as The dual epidemic of HIVand cervical cancer continues to noncommunicable diseases including diabetes, hypertension take its toll on women across Africa. Even HIV-positive women and obesity. Comprehensive, streamlined protocols that address who are otherwise well on ART continue to experience higher cer- multiple competing priorities are needed to ensure that no vical cancer rates compared to their HIV-negative peers. Effective single intervention risks forcing other significant public health integration of cervical cancer screening into differentiated ART interventions off the providers' agenda. delivery models, including safer conception services, is critical The high rates of untreated pathology observed in this co- if cervical cancer screening uptake is to be effectively supported hort may indicate numerous previously missed opportunities to and expanded in the era of decentralization of ART care and in provide cervical cancer screening, especially considering the ma- the absence of large-scale national cervical cancer screening pro- jority of women had accessed routine HIV and ART care for sev- grams in LMICs. This project demonstrates that such integration eral years. Such missed opportunities contribute to persistently is feasible and detects high levels of significant pathology. Our high rates of preventable cervical cancer deaths in HIV-positive findings support others' calls for South Africa to update its 19,27 women across Africa. In light of increasing pressures to de- cervical cancer screening policies, to shift to HPV testing with congest overburdened health facilities and reduce clinic visits integrated STI screening via the use of point-of-care testing through the provision of decentralized, differentiated services for technologies, accompanied by an expansion of “see and treat” stable ART clients, it is essential that the need for regular cervi- services to relieve the pressure on limited and overstretched cal cancer screening among these women is not overlooked. Even colposcopy services. though data on whether cervical cancer risk declines after ARTare conflicting, a large number of women attending HIV care require 29–32 cervical cancer screening, regardless of ART use. 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PloS one 2015; 10:e0122169. squamous intraepithelial lesions in human immunodeficiency virus- 22. Blanckenberg ND, Oettle CA, Conradie HH, et al. Impact of introduc- positive women. J Infect Dis 2010; 201:681–690. tion of a colposcopy service in a rural South African sub-district on 33. Holme F, Kapambwe S, Nessa A, et al. Scaling up proven innovative uptake of colposcopy. South African Journal of Obstetrics and Gynaecol- cervical cancer screening strategies: Challenges and opportunities in ogy. 2013; 19:81–85. Available at: http://www.sajog.org.za/index.php/ implementation at the population level in low- and lower-middle- SAJOG/article/view/388/410. Accessed October 10, 2018. income countries. International journal of gynaecology and obstetrics: 23. Campos NG, Lince-Deroche N, Chibwesha CJ, et al. 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High prevalence of asymptomatic Gynaecol 2011; 25(5):653–665. sexually transmitted infections among human immunodeficiency 36. Bruinsma FJ, Quinn MA. The risk of preterm birth following treatment virus-infected pregnant women in a low-income South African com- for precancerous changes in the cervix: A systematic review and meta- munity. Int J STD AIDS 2017; 956462417724908. analysis. BJOG 2011; 118:1031–1041. 26. Low N, Broutet N, Adu-Sarkodie Y, et al. Global control of sexually transmitted infections. Lancet 2006; 368:2001–2016. 37. Rees H, Delany-Moretlwe S, Scorgie F, et al. At the Heart of the Prob- 27. Huchko MJ, Maloba M, Nakalembe M, et al. The time has come to lem: Health in Johannesburg's Inner-City. BMC Public Health 2017; make cervical cancer prevention an essential part of comprehensive 17(Suppl 3):554. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 97 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Sexually Transmitted Diseases Pubmed Central

Integrating Cervical Cancer Screening Into Safer Conception Services to Improve Women's Health Outcomes: A Pilot Study at a Primary Care Clinic in South Africa

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Copyright © 2018 The Author(s). Published by Wolters Kluwer Health, Inc. on behalf of the American Sexually Transmitted Diseases Association.
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Abstract

ORIGINAL STUDY Integrating Cervical Cancer Screening Into Safer Conception Services to Improve Women's Health Outcomes: A Pilot Study at a Primary Care Clinic in South Africa Natasha E.C.G. Davies, MPH,* Matthew Chersich, PhD,* Saiqa Mullick, PhD,* Nicolette Naidoo, MPH,* Nokuthula Makhoba, MPH,* Helen Rees, MRCGP, MRCOG,* and Sheree R. Schwartz, PhD*† of clients were eligible for cervical cancer screening and 85% (321 of Background: Sub-optimal cervical cancer screening in low- and middle- 376) of these completed screening. More than half had abnormal cervical income countries contributes to preventable cervical cancer deaths, partic- pathology (185 of 321) and 20% required colposcopy for possible high- ularly among human immunodeficiency virus (HIV)-positive women. We grade or persistently atypical lesions (64 of 321). Compared with HIV- assessed feasibility and outcomes of integrating cervical cancer screening negative women, abnormal pathology was more likely among HIV-positive into safer conception services for HIV-affected women. women, both those on ART <2 years (adjusted prevalence ratio, 2.5; 95% Methods: At a safer conception service in Johannesburg, South Africa, confidence interval, 1.2–5.0) and those on ART 2 years or longer (adjusted HIV-affected women desiring pregnancy received a standard package of care prevalence ratio, 2.1; 95% confidence interval, 1.0–4.2). designed to minimize HIV transmission risks while optimizing prepregnancy Conclusions: Integrating cervical cancer screening into safer conception health. All eligible women were offered Papanicolaou smear, and those with care was feasible with high coverage, including for HIV-positive women. significant pathology were referred for colposcopy before attempting pregnancy. Significant pathology, requiring colposcopy, was common, even among Multivariable analyses identified associations between patient characteristics and healthy women on ART. Safer conception services present an opportunity abnormal pathology. for integration of cervical cancer screening to avert preventable cancer- Results: In total, 454 women were enrolled between June 2015 and April related deaths among HIV-affected women planning pregnancy. 2017. At enrolment, 91% were HIV-positive, 92% were on antiretroviral ther- apy (ART) and 82% virally suppressed. Eighty-three percent (376 of 454) ach year over 250,000 women die of cervical cancer, a prevent- Eable condition. In high-income countries, population-level From the *Wits Reproductive Health and HIV Institute, Faculty of Health cervical cancer screening programs have effectively reduced cervi- Sciences, University of the Witwatersrand, Johannesburg, South Africa; and †Department of Epidemiology, Johns Hopkins School of cal cancer associated morbidity and mortality. Unfortunately, in Public Health, Baltimore, MD the most affected low- and middle-income countries (LMICs), Conflict of Interest: None declared. screening coverage remains low. In South Africa, for example, Sources of Funding: This work was partially supported through USAID, poor program coverage contributes to over 4000 cervical cancer Cooperative Agreement AID-674-A-12-00021 (Health System Strengthening deaths each year, making cervical cancer the leading cause of ABF 393). USAID funding provided support for the costs of safer cancer deaths in women of reproductive age. Integration of conception clinic staffing, training and development of job aides and cervical cancer screening into human immunodeficiency virus the creation of information, education and communication materials (HIV) programming in LMICs, such as South Africa, is particularly to advertise the new service. The implementation took place at a Gauteng important as this cancer disproportionately affects HIV-positive Department of Health (DOH) facility supported by DOH staff. The 5 6 authors' views expressed in this publication do not necessarily reflect women, even once they commence antiretroviral therapy (ART). the views of the United States Agency for International Development Screening opportunities for HIV-infected women are, however, or the United States Government. frequently missed due to low awareness and poorly integrated Correspondence: Natasha E.C.G. Davies, MPH, Wits RHI, Hillbrow Health 3,7 services. Considering the dual burden of HIV and cervical Precinct, 22 Esselen Street, Hillbrow, 2001, Johannesburg. South Africa. cancer seen in many LMICs, integrating cervical cancer E‐mail: ndavies@wrhi.ac.za. screening, and other sexual and reproductive health (SRH) services Acknowledgements: The authors are grateful to the study participants and into established HIV programs is clearly a priority. to the study team for their time and dedication to the work. The Built on a framework of reproductive rights, comprehen- authors thank the Hillbrow Community Health Centre, the City of sive safer conception services support HIV-affected couples to Johannesburg and the Department of Health for their support of the project. The authors thank USAID and the United States Government safely achieve their fertility goals while minimizing risks of hori- for providing funding support. zontal or vertical HIV transmission, and optimizing the couples' Received for publication June 20, 2018, and accepted September 9, 2018. overall health status before a pregnancy. In South Africa, over half DOI: 10.1097/OLQ.0000000000000914 of women accessing ART are of reproductive age and many express Copyright © 2018 The Author(s). Published by Wolters Kluwer Health, 10 adesireto havechildrennow or in thefuture. Recognizing this Inc. on behalf of the American Sexually Transmitted Diseases Associ- overlap between HIV and fertility desires, safer conception ation. This is an open-access article distributed under the terms of the services are recommended as part of the South African National Creative Commons Attribution-Non Commercial-No Derivatives License Contraceptive and Fertility Policy released in 2012. Such services 4.0 (CCBY-NC-ND), where it is permissible to download and share create a valuable opportunity for HIV and SRH integration, the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. including for cervical cancer screening. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 91 � Davies et al. This study aimed to investigate the feasibility of inte- model and integrate services into nine primary healthcare facilities grating cervical cancer screening into safer conception services in other parts of inner-city Johannesburg. as one component of a comprehensive package of care. The study, in Johannesburg, South Africa, was set within one of the first Study Population public sector safer conception services in the country. We also All women of reproductive age who were in an HIV-affected sought to assess the outcomes of cervical cancer screening. relationship (HIV seroconcordant, serodiscordant, or where one part- ner had unknown HIV status) who currently desired pregnancy were eligible to attend the service, with or without their partner. METHODS Men and women self-referred after hearing about the safer con- ception service during health talks presented in clinic waiting areas, from leaflets and posters within the facility, or by word of Study Context mouth. In addition, facility staff referred clients whom they In April 2015, a safer conception clinic was established in a screened as currently desiring pregnancy. busy, community health care center in inner-city Johannesburg. The facility offers general services and has an ART clinic, attended by over 21,000 HIV-positive clients. Although national policies Cervical Cancer Screening Process have supported the provision for safer conception services since Clients were provided with a standard package of safer con- 2012, no standardized, integrated approach or public sector ser- ception care with the aim of optimizing their health status before vice delivery model has been developed. In particular, prior to in- pregnancy and minimizing HIV transmission risks, including troducing the safer conception service at the facility, screening for cervical cancer screening in the form of a Pap smear which was fertility intentions was ad hoc, and the provision of SRH services, 14 conducted according to national guidelines. The HIV–positive including family planning and cervical cancer screening for HIV- women, regardless of age, were eligible for a Pap smear if they positive women, took place in a separate building from the ART had never been screened before, or they reported having been clinic, staffed by different providers. Patients requesting these ser- screened, but no result could be traced, their last abnormal vices were referred to the relevant providers. Pap smear was more than 12 months ago, or they had a normal Recognizing the lack of service integration, a safer concep- result more than 24 months previously. The HIV–negative tion clinic was introduced as a dedicated service which operated women were offered cervical cancer screening if they were older within the same building as the ART clinic. The service was than 30 years and had not had a normal Pap smear result in the past rendered by primary healthcare nurses who were supervised 10 years. Screening tests for human papillomavirus (HPV) were by a doctor and had received training in safer conception care. unavailable within public sector facilities at the time of this study. An integrated package of care was provided prepregnancy during Women who were eligible for a Pap smear were offered the the baseline visit and subsequent monthly to three monthly follow- service on the same day as their baseline visit, unless they were up visits. The package included risk reduction (safer conception) menstruating, in which case it was conducted at their next visit. counseling, support for HIV status disclosure, partner HIV testing, Most smears were performed by the safer conception service ART for women and their partners, preexposure prophylaxis for nurses in a one-stop shop approach, although some were done HIV-negative partners, screening and management of sexually by a postnatal clinic nurse situated in a nearby room during periods transmitted infections (STIs), care for comorbid opportunistic in- of high patient load. fections or noncommunicable diseases for both members of the Pap smear results, which have a reported sensitivity and couple, and cervical cancer screening for women with referral specificity of 75.8% and 83.4%, respectively, were available for further management where indicated. within 4 to 6 weeks. If required, women were referred to the onsite Services were delivered according to national guidelines. colposcopy service and advised to delay pregnancy attempts until In the case of cervical cancer screening, South Africa's recommen- their colposcopy results indicated no need for further manage- dations differ somewhat from international norms, with screening ment. This approach was taken given the risks of having untreated for HIV-negative women being conducted once in their third, abnormal cervical pathology during pregnancy including preg- fourth and fifth decades of life, and HIV-positive women being nancy loss and premature labor and delivery. The rationale for screened as soon as they are diagnosed with HIV infection and delaying pregnancy attempts was explained to each woman, and then every 1 to 3 years thereafter. her partner if present. Care was taken to minimize the anxiety Donor funding supported the safer conception clinic associated with receipt of abnormal Pap smear results while staffing, including clinical, administrative and research staff, job supporting the couple to delay pregnancy until any abnormal pa- aides and distribution of communication materials to inform pa- thology had been addressed. tients attending the clinic of this new service. Routine clinical pro- cedures, such as ART supply and Pap smears were funded through Data Collection and Analysis the Department of Health and the project was implemented at a Department of Health public sector facility. The only noninte- Data on patient demographics and health status were cap- grated component was medical male circumcision; male partners tured on case report forms, medical history was extracted from pa- who requested this intervention were referred to the medical male tient medical records and clinical data were collected during circumcision clinic within the same facility. Additionally, donor- procedures performed as part of the service. Results of Pap smears supported, colposcopy services, which had previously only been and colposcopy were obtained by reviewing women's clinical file available at a nearby tertiary hospital, had recently been estab- notes or searching the database of the National Health Laboratory lished at the study facility. No services for infertility were pro- Service, where all the samples were assessed. Data were entered vided at the clinic. If women did not conceive within 6 to into a REDCap database and analyzed in STATA 14 (College 9 months of trying they were offered referral to a low-cost fertility Station, TX). service in Pretoria, a city about 50 km away. Coverage (percentage of clients offered screening) and up- Enrolment into the demonstration project was completed in take (percentage of clients offered screening who had a Pap smear April 2017; however, efforts have been undertaken to adapt the done) were assessed. Characteristics of women who had a Pap 92 Sexually Transmitted Diseases Volume 46, Number 2, February 2019 � Integrating Safer Conception and Cervical Screening smear were compared with those who did not using χ tests or (M150146). The study was conducted according to good clinical nonparametric equality of medians tests, as appropriate. practice guidelines and all enrolled clients completed written, Analysis focused on 2 outcomes of interest: (1) women informed consent. with any abnormal Pap smear and (2) women with significant pa- thology requiring colposcopy. Significant pathology included: RESULTS high-grade squamous intraepithelial lesions (HSIL); persistent Overall, 454 women attended the safer conception service. low-grade squamous intraepithelial lesions (LSIL) or atypical Of these, 91% (n = 413 of 454) were HIV-positive, having had a squamous cells of unknown significance; or any smear in which positive HIV test a median of 5 years ago (interquartile range, HSIL or cervical intraepithelial neoplasia (CIN) I or II could not 3–9). The vast majority (92%, 382 of 413) were already on ART, be excluded. with 19% (n = 71 of 382) having initiated in the past year; 51% Pap smear results are presented and modified robust had a CD4 cell count 500 cells/mm or greater and only 7% had Poisson regression was used to separately assess correlates of a CD4 cell count 200 cells/mm or less. Overall, 75% (n = 311 having an abnormal Pap smear and having a result requiring col- of 413) of HIV-positive women had an undetectable viral load poscopy. Robust Poisson regression was used given that the prev- (<50 copies/mm ) at their baseline visit, and viral suppression alence of the outcome was greater than 10% and the log binomial was 82% among those taking ART (311 of 382). models failed to converge consistently. Bivariate analyses iden- Of all women, 83% (n = 376 of 454) were eligible for a Pap tified associations between demographic and clinical characteris- smear (Fig. 1). Of these, 18 were never offered a Pap smear by the tics and the two outcomes of interest (abnormal Pap smear and provider, representing missed screening opportunities due to pro- significant pathology requiring colposcopy). The final, multivari- vider oversight (n = 358 of 376 or 95% screening coverage). A able models included age, based on face validity and apriori hypotheses, and variables associated with the outcome in the bi- further 30 women were offered screening, but did not take it up variate analysis at P value less than 0.10. (92% uptake). No differences were detected in demographic or clinical characteristics between the 15% (n = 70 of 454, Fig. 1) of women who recently had a Pap smear and those who did not. Ethics Overall, a Pap smear was performed for 87% (n = 328 of 376) Ethical approval was secured from the Human Research of eligible women, 93% (n = 306) of whom were HIV-positive. Ethics Committee of the University of the Witwatersrand Women who were eligible for a Pap smear, but did not receive Figure 1. Flow diagram of females enrolled and accessing cervical cancer screening via safer conception service. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 93 � Davies et al. one, were more likely to be lost to follow-up after their baseline About three quarters of the 64 women who required colpos- safer conception visit, precluding an opportunity to conduct the copy had a traceable histology result (n = 47, 73%) (Table 2). None Pap smear during follow-up (31% compared with 8% among of these women had invasive malignancy. Twenty-five (53%) women who did receive a Pap smear, P <0.01). women had evidence of HSIL or CIN II/III, with 20 of these hav- Across all demographic and clinical variables, the only dif- ing incomplete resection at the biopsy margins. These women re- ference detected between those accessing Pap smears through the quired further follow-up, but no records of a repeat colposcopy safer conception service was HIV status, with those receiving a could be located. Among the 64 women, 9 had a confirmed preg- Pap smear being more likely to be HIV-positive (Table 1). nancy, 2 of whom conceived before colposcopy was performed. Of the 321 results available for analysis (7 results were un- No difference was detected in rates of retention in the safer con- traceable), 58% (n = 185 of 321) had abnormal cytology, equating ception service between women referred for colposcopy and to 41% (185 of 454) of all women attending the clinic (Table 2). In women not requiring colposcopy (95% vs. 91%, P =0.30). total, 20% of those who had an abnormal Pap smear result (n = 64 of 321) required colposcopy prior to beginning pregnancy attempts, DISCUSSION which translates into 14% (64 of 454) of all women attending the clinic. Among women requiring colposcopy, 31% (n = 20 of 64) Three key findings emerge from this study. First, integra- were younger than 30 years. Additionally, bacterial vaginosis was tion of cervical cancer screening into safer conception services is detected in 38% (n = 122 of 321) of Pap smears and Trichomonas feasible and is associated with high coverage and uptake. Most vaginalis (TV) in 3.4% (n = 11 of 321). women, despite accessing routine HIV services, had not previ- In the bivariate robust Poisson regression assessing corre- ously been screened for cervical cancer, illustrating the importance lates of having a Pap smear result of any abnormal cytology, only of integration initiatives, such as done in this study. Second, rou- HIV status was associated with having an abnormal Pap smear tine cervical cancer screening identifies high levels of significant (Table 3). These results were robust in the multivariable model, pathology, particularly among HIV-positive women. Of all women with only minor changes noted to point estimates. Being HIV- attending the clinic, around 40% had abnormal pathology and one positive increased the magnitude of risk for an abnormal Pap in seven required colposcopy. Third, significant pathology is com- smear about 2-fold, regardless of whether a woman had not begun mon despite a large proportion of these women being on ART for ART, or had received ART for under 24 months or for over several years. This reiterates the importance of cervical cancer 24 months. Relationships were similar in the models assessing cor- screening, regardless of ART status. relates of Pap smear results requiring colposcopy; the magnitude Overall, the study supports increasing calls to improve inte- of the association between HIV and duration of ART use was gration of SRH services—including cervical cancer screening and 8,19 stronger for the colposcopy outcome, though statistical signifi- family planning—with HIV services. The benefits of such in- cance was not reached. tegration have been demonstrated across numerous countries and TABLE 1. Demographics of Female Clients Attending a Safer Conception Service (N = 454) Women With Pap Smear Women With No Pap Smear Done While Attending Safer Done While Attending Safer Characteristics Conception Service (n = 328) Conception Service (n = 126)* P Age: n (%), y 0.86 18–24 19 (5.8%) 10 (7.9%) 25–29 70 (21.3%) 25 (19.9%) 30–34 117 (35.7%) 45 (35.7%) ≥35 122 (37.2%) 46 (36.5%) 306 (93%) 107 (85%) HIV-positive, n (%) 0.01 Years since HIV diagnosis, median (IQR) 5.5 (2.7–8.7) 5.1 (2.9–8.4) 0.82 On ART at enrolment, n (%) 281 (92%) 101 (94%) 0.39 Years on ART at enrolment, median (IQR) 3.2 (1.6–6.1) 2.9 (1.2–5.2) 0.26 Latest CD4 count at enrolment, median (IQR) 500 (364–631) 508 (351–689) 0.73 Viral load <50 copies/mL at enrolment, n (%) 230 (75%) 81 (76%) 0.80 Nationality, n (%) 0.78 South African 180 (55%) 71 (56%) Non-South African 148 (45%) 55 (44%) Highest educational level completed, n (%) 0.17 Primary school or less 21 (6%) 12 (10%) Some high school but not completed 127 (39%) 38 (30%) High school or higher completed 179 (55%) 76 (60%) 208 (63%) 73 (58%) Employed, n (%) 0.28 Monthly income in USD, median (IQR)† 222 (0–296) 200 (0–356) 0.92 Partner circumcised, n (%) 163 (51%) 65 (52%) 0.83 Smoker, n (%) 29 (9%) 11 (9%) 0.98 Totals vary due to missing data for some variables. * Pap smear not done for 126 women while they attended the safer conception service includes 78 women who were not eligible for a Pap smear and 48 women who were eligible, but did not access a Pap smear. † South African Rand to US Dollar (USD) exchange rate 13.5:1. IQR, interquartile range. 94 Sexually Transmitted Diseases Volume 46, Number 2, February 2019 � Integrating Safer Conception and Cervical Screening For example, at the nearby tertiary hospital, only 250 to 300 TABLE 2. Pap Smear and Colposcopy Outcomes for Safer 13 women access colposcopy annually. Thus, even if current efforts Conception Service Clients (N = 321)* to decentralize colposcopy services to district or primary level care Number Proportion are intensified, only a small portion of need would be met if rates Pap Smear Outcomes (N = 321) (%) [95% CI] of pathology were universally as high as seen in this study. This study therefore reinforces growing calls for South Africa to No action required 136 42% [37–48] 14,23 review their cervical cancer screening recommendations, NILM Repeat Pap smear required in 12 months 121 38% [33–43] particularly with a view to expanding the “see and treat” approaches LSIL 90 to bypass weak referral pathways and reduce demand for ASCUS 31 colposcopy. This would also avoid the need for, and associated Colposcopy referral required 64 20% [16–25] costs of, repeated follow-up visits by clients. HSIL 36 Ideally, such a shift in approach would be accompanied by LSIL or ASCUS 15 the introduction of HPV testing. This would improve the ability to cannot exclude HSIL or CIN I/II triage women at highest risk of cervical cancer, enabling them to Atypical cells/persistent atypia 13 be prioritized for further management. In an evaluation of HPV (LSIL or ASCUS) testing, Pap smear, and visual inspection with ascetic acid (VIA), Colposcopy Outcomes (N = 64) Firnhaber et al reported sensitivity/specificity rates of 92%/ No record of colposcopy result 11 17% 51.4% for HPV, 75.8/83.4% for Pap smear and 65.4/68.5% Repeat pap result traced, no 69% for VIA when used to screen HIV-infected women in South colposcopy result traced Africa. In light of the high sensitivity of HPV screening but lower No dysplasia reported 2 3% specificity, a combined approach, using both HPV screening and Total with LSIL 20 31% [20–44] VIA, or HPV screening, Pap smear, and colposcopy would help LSIL with complete resection 13 20% to optimize the potential benefits while reducing the potential at margins harm of unnecessary interventions, such as colposcopy. This LSIL with incomplete resection 711% combined approach would help to avoid exposing women to at margins Total with HSIL/CIN III 25 39% [27–52] unnecessary discomfort, significant anxiety and potential harm HSIL or CIN III with complete 58% associated with colposcopy or other treatment modalities. resection at margins Both bacterial vaginosis (BV) and TV are associated with HSIL or CIN III with incomplete 20 31% increased HIV transmission and acquisition risks, as well as nega- resection at margins tive birth outcomes, including miscarriage and preterm labor and delivery. Detecting BV and TV at the time of cervical cancer *N = 321 because 7 (2%) of 328 Pap smears had no traceable result. screening enabled us to manage these conditions effectively. Fur- NILM, negative for intraepithelial lesion or malignancy; ASCUS, atypical thermore, the relatively high rate of BVand TV seen in our cohort squamous cells of unknown significance; 95% CI, 95% confidence interval. may suggest that we saw the “tip of the iceberg” of underlying STIs, as gonorrhea, chlamydia, and herpes simplex virus are not 20,21 service delivery models. In this study, the levels of coverage detected on Pap smear. In settings like South Africa, where and uptake observed suggest a high level of client acceptability. clinicians rely on a syndromic approach to STI screening and In South Africa, almost all colposcopy services are provided in management, many asymptomatic infections are missed. tertiary-level facilities, with long waiting lists and limited capacity. Samples collected during cervical cancer screening could also be TABLE 3. Bivariate and Multivariable Correlates of Any Abnormal Pap Smear Result or Results Requiring Colposcopy (N = 321) Correlates of Having an Abnormal Correlates of Having a Pap Smear Pap Smear Result Requiring Colposcopy Crude Prevalence Adjusted Prevalence Crude Prevalence Adjusted Prevalence Characteristics Ratio (95% CI) Ratio (95% CI) Ratio (95% CI) Ratio (95% CI) Age, y <30 Reference Reference Reference Reference ≥30 0.86 (0.71–1.05) 0.86 (0.71–1.05) 0.84 (0.53–1.35) 0.87 (0.55–1.39) Employment status Unemployed Reference — Reference — Employed 1.06 (0.87–1.28) — 1.16 (0.74–1.81) — Income (above/below median) <219 USD/month Reference — Reference — ≥219 USD/month 0.94 (0.77–1.14) — 0.79 (0.50–1.24) — Completed high school No Reference — Reference — Yes, high 0.99 (0.82–1.19) — 1.21 (0.77–1.89) — school or beyond HIV and ART HIV-negative Reference Reference Reference Reference HIV-positive, not yet begun ART 2.05 (0.95–4.42) 2.01 (0.93–4.32) 2.64 (0.29–23.66) 2.58 (0.29–23.04) HIV-positive, ART <2 years 2.47 (1.23–4.97) 2.47 (1.22–4.96) 6.67 (0.96–46.61) 6.66 (0.95–46.66) HIV-positive, ART ≥2 years 2.08 (1.04–4.17) 2.14 (1.06–4.30) 3.92 (0.56–27.38) 4.02 (0.57–28.55) Models estimated using robust Poisson regression. Sexually Transmitted Diseases Volume 46, Number 2, February 2019 95 � Davies et al. used to conduct increasingly affordable point-of-care diagnostic estimates. To address this limitation, we also assessed the predic- tests for STIs. There is clearly an opportunity, within integrated tors of having any abnormal Pap smear result and found the results services, to introduce molecular testing not only for HPV, but to be robust across the two models. Additionally, although we also for other common STIs. Assessment is needed of the costs of aimed for a fully integrated service with all Pap smears pro- this approach, weighed against the potential benefits of reducing vided within the safer conception clinic, this was not always cervical cancer, mitigating HIV transmission risks, reducing possible, perhaps contributing to missed opportunities. Going poor obstetric outcomes and minimizing infertility related to forward, complete service and provider-level integration would STIs. Enhanced screening services could also incorporate be recommended. screening and management of other conditions, such as The dual epidemic of HIVand cervical cancer continues to noncommunicable diseases including diabetes, hypertension take its toll on women across Africa. Even HIV-positive women and obesity. Comprehensive, streamlined protocols that address who are otherwise well on ART continue to experience higher cer- multiple competing priorities are needed to ensure that no vical cancer rates compared to their HIV-negative peers. Effective single intervention risks forcing other significant public health integration of cervical cancer screening into differentiated ART interventions off the providers' agenda. delivery models, including safer conception services, is critical The high rates of untreated pathology observed in this co- if cervical cancer screening uptake is to be effectively supported hort may indicate numerous previously missed opportunities to and expanded in the era of decentralization of ART care and in provide cervical cancer screening, especially considering the ma- the absence of large-scale national cervical cancer screening pro- jority of women had accessed routine HIV and ART care for sev- grams in LMICs. This project demonstrates that such integration eral years. Such missed opportunities contribute to persistently is feasible and detects high levels of significant pathology. Our high rates of preventable cervical cancer deaths in HIV-positive findings support others' calls for South Africa to update its 19,27 women across Africa. In light of increasing pressures to de- cervical cancer screening policies, to shift to HPV testing with congest overburdened health facilities and reduce clinic visits integrated STI screening via the use of point-of-care testing through the provision of decentralized, differentiated services for technologies, accompanied by an expansion of “see and treat” stable ART clients, it is essential that the need for regular cervi- services to relieve the pressure on limited and overstretched cal cancer screening among these women is not overlooked. Even colposcopy services. though data on whether cervical cancer risk declines after ARTare conflicting, a large number of women attending HIV care require 29–32 cervical cancer screening, regardless of ART use. 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Sexually Transmitted DiseasesPubmed Central

Published: Oct 10, 2018

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