Original Article Journal of the International Association of Providers of AIDS Care HIV Retesting of HIV-Negative Pregnant Volume 18: 1-6ª The Author(s) 2019 Women in the Context of Prevention of Article reuse guidelines:sagepub.com/journals-permissions DOI: 10.1177/2325958218823530 Mother-to-Child Transmission of HIV in journals.sagepub.com/home/jia Primary Health Centers in Rural Zambia: What Did We Learn? Justin Mandala, MD, MPH1 , Prisca Kasonde, MD, MMed, MPH2, Titilope Badru, MSc3, Rebecca Dirks, MA, BA1, and Kwasi Torpey, MD, PhD, MPH, FGCP1,4 Abstract Background: This observational study describes implementation of HIV retesting of HIV-negative women in prevention of mother-to-child transmission (PMTCT) services in Zambia. Methods: Uptake of retesting and PMTCT services were compared across age, parity, and weeks of gestation at the time of the first HIV test, antiretrovirals regime, and HIV early diagnosis results from infants born to HIV-positive mothers. Results: A total of 19 090 pregnant women were tested for HIV at their first antenatal visit, 16 838 tested HIV-negative and were offered retesting 3 months later: 11 339 (67.3%) were retested; of those, 55 (0.5%) were HIV positive. Uptake of the PMTCT package by women HIV positive at retest was not different but HIV-exposed infants born to women who retested HIV positive were infected at a higher rate (11.1%) compared to those born to women who tested HIV positive at their initial test (3.2%). Conclusion: We suggest rigorously (1) measuring the proportion of MTCT attributable to women who seroconvert during pregnancy and possibly adjust PMTCT approaches and (2) addressing the substantial loss to follow-up of HIV-negative pregnant women before HIV retesting. Keywords prevention of mother-to-child transmission, HIV testing and counseling, Zambia Date received: 6 March 2018; revised: 21 November 2018; accepted: 10 December 2018. Background uptake and low retention on ART among pregnant and breast- feeding women.1 Another factor thought to hinder PMTCT Vertical transmission remains the principal route of new efforts is newly acquired HIV infection during pregnancy or pediatric HIV infections despite the availability of effective breastfeeding period.3-5 Literature suggests that pregnant interventions for the prevention of mother-to-child transmis- women have a higher risk of acquiring HIV infection than the sion (PMTCT) of HIV. In the last decade in Zambia, as in many other low- and middle-income countries, considerable improvements in PMTCT have been observed: Services are 1 increasingly available in primary health centers (PHCs) and a Global Health, Population and Nutrition, FHI 360, Washington, DC, USA2 ICAP at University of Columbia, Lusaka, Zambia growing proportion of HIV-positive pregnant women are 3 Strengthening Integrated Delivery of HIV/AIDS Services (SIDHAS) Project, accessing efficient combination antiretroviral treatment FHI 360, Washington, DC, USA (ART).1 The goal to eliminate new pediatric HIV infection 4 School of Public Health, University of Ghana, Accra, Ghana by 2015 was missed by most countries and very few countries 2 Corresponding Author:are on track toward elimination of new cases of pediatric HIV. Justin Mandala, Global Health, Population, and Nutrition, FHI 360, 1825 Progress toward elimination of new pediatric HIV infection Connecticut Ave NW, Washington, DC 20009, USA. is hindered by a number of factors including the suboptimal Email: jmandala@fhi360.org Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 Journal of the International Association of Providers of AIDS Care the same age group, HIV prevalence is higher among women What Do We Already Know about This Topic? (15.1%) than among men (11.3%). HIV is twice as prevalent in urban (18.2%) than in rural (9.1%) areas.11 According to the Joint Retesting of previously tested HIV-negative pregnant United Nations Programme on HIV and AIDS, in 2015 an esti- women is a recommended practice in many countries, mated 4700 children were newly infected with HIV in Zambia; one including Zambia, but its evaluation has been limited. of the highest national figures of new pediatric HIV infections.1 In response to the HIV epidemic threat, strong leadership How Does Your Research Contribute to the from the Government of Zambia and a partnership with United Field? States Agency for International Development (USAID) resulted in a decentralized HIV/AIDS program. In addition, This article contributes to the understanding of the extent there has been a visible integration of HIV-related interven- to which seroconverting pregnant women contribute to tions, particularly PMTCT, into routine maternal, neonatal and mother-to-child transmission of HIV. child health care (MNCH).12,13 The USAID support has been implemented through various What Are Your Research’s Implications toward initiatives, including the Zambia Prevention Care and Treat- Theory, Practice, or Policy? ment Partnership (ZPCT) project since 2005. This article reports on a study conducted in 10 MNCH clinics that have Our observations would inform the prevention of mother- to-child transmission strategy and policy in Zambia or in integrated PMTCT interventions. The interventions are based on the Zambian PMTCT guidelines, which recommend retest- countries with similar profiles; questions to consider might ing HIV-negative pregnant and breastfeeding women every 3 be “what should be the best approach to prevent mother- to 6 months.13 All HIV-positive pregnant women (at initial to-child transmission to minimize the risk of HIV vertical test or at retest) were offered a combination ART for the transmission from seroconverting women.” entire period of pregnancy and breastfeeding. The 10 MNCH clinics were rural PHCs that have been receiving technical support from the ZPCT project. They were selected because 6-8 they had the highest volume of clients among the PHCs sup-general population ; this risk is likely due to sexual behavior, ported by the ZPCT project. To shorten the recruitment time, pregnancy itself is the result of “unprotected” sex. Incident the authors decided to select health facilities that registered HIV infection during pregnancy is associated with higher risk 9 an average of 20 or more new pregnant women for firstof mother-to-child transmission of HIV (MTCT). Diagnosing antenatal visits per month. newly acquired HIV infections at the programmatic level is The study population consisted of all pregnant women and very challenging, and the realistic alternative is to repeat HIV their infants registered in antenatal clinics, labor and delivery testing among clients previously found to be HIV negative. The settings, and postnatal service points from 10 selected health Ministry of Health of Zambia recommends that pregnant facilities supported by ZPCT between February 2010 and Decem- women previously tested HIV negative be retested every 10 ber 2013 in 5 provinces. Four of the PHCs were in Copperbelt3 months after the initial test until delivery. province, 3 in Central province, 1 in Luapula province, 1 in North Despite the need for early diagnosis and initiation of treat- province, and 1 in North-Western province. All 10 health facili- ment for pregnant women, data are not systematically col- ties had PMTCT services integrated into MNCH services. lected, reported, and analyzed on the implementation of this recommendation. HIV Testing and Retesting Methodology Objective At their first antenatal care visit, all pregnant women were offered HIV testing and counseling (HTC) on an “opt out” The objective of this study was 4-fold: (1) determine to what extent basis, meaning all women were tested for HIV unless they women previously tested HIV negative are being retested, (2) explicitly refused. The HTC was performed by trained provi- determine the rate of HIV infection in the specific group of women ders: nurses or midwives or lay PMTCT counselors. As per the with a previous HIV-negative test who were retested, (3) describe national guidelines, the HIV testing algorithm is a serial rapid how HIV-incident pregnant women (and their infants) accessed HIV testing, and the description here refers to the active guide- PMTCT services, and (4) determine the MTCT rate among infants lines at the time of the study. The first-line test used was Deter- born to women who seroconverted during pregnancy. mine; if the Determine test result was negative, the HIV status was considered negative; when Determine result was positive, Methods the second-line test, Uni-Gold was used; if Uni-Gold test result, Trinity Biotech was also positive, the result was considered Study Context and Population positive; if Uni-Gold test result was negative (discordant with Zambia is an HIV hyperendemic country; in 2015, the estimated Determine test result), a third-line test, Bioline, was used as a HIV prevalence among adults (aged 15-49 years) was 13.3%; in tiebreaker.13 The retesting of previously tested HIV-negative Mandala et al 3 women was performed by the same providers and followed the was performed anonymously by a team that did not have con- same algorithm as the initial HIV testing. tact with the participants or with their identifiable information. Design Results This is a descriptive observational study of HIV testing and Study Population and Follow-up Overview retesting activities within MNCH settings. We analyzed all A total of 19 090 pregnant women were registered for the initial HIV test and retest results as well as age, parity, and gesta- antenatal clinic visit, ranging in age from 10 to 49 years with a tional age at the time of the first HIV tests; antiretrovirals median of 23 years (interquartile range [IQR]: 20-28). Their regime received by HIV-positive women; and feeding method parity ranged from 0 to 14 with a median of 1 (IQR: 0-3). The and HIV early diagnosis results from infants born to HIV- median gestational age at the time of the first antenatal clinical positive mothers. visit was 22 weeks (IQR: 18-26). The pregnant women who registered for the initial antenatal clinic visit (n ¼ 19 090) were offered HTC or screening for an Data Collection, Entry, and Analysis HIV-positive status; 16 838 (88.2%) of these tested HIV neg- The study used data routinely collected by PHC for integrated ative. The proportions of loss to follow-up (LTFU) and inde- PMTCT services—integrated antenatal register, delivery, and terminate results were negligible, 0.4% (n ¼ 77) and <0.1% postpartum registers as well as HIV-exposed infants registers. (n ¼ 10), respectively. A total of 2165 (11.3%) pregnant The specific data elements were entered into dedicated data women were determined to be HIV positive at that initial extraction article-based registers by health facility personnel antenatal screening (see Figure 1). at the selected health facilities; the personnel were trained on A total of 2220 infants born to HIV-positive mothers were the use of data extraction tools and were regularly supervised recorded: 2165 born to HIV-positive mothers from the initial by the ZPCT provincial technical officers to ensure good qual- HIV test and 55 to mothers who were HIV positive at the retest. ity data collection. The article-based register was double Throughout the cascade various degrees of LTFU were reg- entered into an Excel 2016 database by the data clerks and istered. The biggest LTFU (60.6%) was observed among checked for accuracy by the ZPCT provincial monitoring and infants born to mothers found HIV positive at the initial HIV evaluation (M&E) officer before being sent to the ZPCT cen- test between offer of early infant diagnosis and actual dried tral office in Lusaka. blood collection. See Figure 1 for further details. Frequencies and percentage distributions of key variables were generated. Differences in proportion were tested using Retesting and LTFU the w2 test. Continuous variables were described as mean or All HIV-negative women (16 838) were offered HIV retesting median depending on the distribution of the data. Incidence rate and counseling; the retest was to be conducted every 3 months was estimated from the number of seroconversions and total before delivery. A sizeable proportion of women—32.7% person-years of follow-up. For the incidence rate calculations, (n ¼ 5499)—was considered LTFU as they did not return for exposure time was calculated as the interval between time of subsequent antenatal clinic visits. Women LTFU (before enrollment until last HIV-negative test for non-seroconverters retesting) tended to be of older age (35), higher parity and until the time of HIV infection for seroconverters, which (4), and in late gestational age (28 week pregnancy; see was estimated as the midpoint between the last negative HIV Table 1). rapid test result and the first positive HIV rapid test result. Median gestational age at the time of retesting was P values below .05 were considered statistically significant. 34 weeks, ranging from 5 to 40 weeks. Very few (2.4%) Statistical analysis was performed with STATA, StataCorp were retested at the time of delivery. The median time (version 12). between the previous HIV-negative test and the HIV retest (regardless of the HIV retest results) was 93 days, ranging Ethical Approval and Informed Consent from 30 to 245 days. Authors could not explain the wide range of the lapse of time between the first HIV-negative Ethical approval was granted by the ethical review board and test and the retesting despite the recommendation to imple- the Ministry of Health of Zambia (reference: 2010-AUG-001) ment retesting every 3 months. and the FHI 360’s Protection of Human Subjects Committee (reference: OIRE/5/25/10). Incident HIV Infection The ethical review board and the Ministry of Health of Zambia as well as the FHI 360’s Protection of Human Subjects The study defined incident HIV as a positive HIV test in a Committee judged that informed consent was not needed. No woman who had a documented previous HIV negative test. A names or personal identifier of individual patients were col- total of 55 (0.49%) of 11 282 women (previously tested HIV lected. There was no participant ID or other means that could negative) retested HIV positive. Observation time was 5195.4 link data to participants on the electronic data set. Data analysis person-years. HIV incidence was estimated at 1.06 per 100 4 Journal of the International Association of Providers of AIDS Care Pregnant women who aended their 1st ANC visit and were offered HTC 19,090 LTFU 77 (0.4%) Indeterminate test 10 (<0.1%) HIV negave from the inial test, then offered retesng HIV posive from the inial test 16838 (88.2%) 2165 (11.3%) LTFU 5499 (32.7%) Indeterminate test 2 (<0.1%) Retest HIV negave Retest HIV posive 11282 (99.5%) 55 (0.5%) Infants born to HIV mothers offered EID Infants born to HIV mothers offered EID 55 2165 LTFU LTFU 19 (27.3%) 1312 (60.6%) PCR HIV negave HIV posive PCR HIV Posive PCR HIV negave 32 (89.9%) 4 (11.1%) 27 (3.2%) 826 (96.8%) Figure 1. Study population and follow-up overview. Table 1. Comparative Description of LTFU before Retest by Age, is the results of wide range of the lapse of time between the first Parity, and Gestational Age. HIV-negative test and the retesting. We observed that in Luapula Province, 2.1% of women Comparing key maternal variables between pregnant women that retested and those who were loss to follow-up (LTFU) before retest retested HIV positive, while 0.6%, 0.4%, and 0.4%, did so in (N ¼ 16 838) Central, Copperbelt, and North-Western Provinces, respec- tively. In Northern Province, none retested HIV positive. The Variables Retested (%) LTFU (%) P Value small proportion of those who retested HIV positive did not Age group (years) allow for any meaningful statistical analysis to compare inci- 24 (n ¼ 9622) 6444 (67.0) 3178 (33.0) dence between provinces. 25-34 (n ¼ 5922) 4094 (69.1) 1828 (30.9) <.001 35 (n ¼ 1294) 801 (61.9) 493 (38.1) Parity category Discussion 0 (n ¼ 5527) 3940 (71.3) 1587 (28.8) Published literature on retesting of previously tested HIV- 1-3 (n ¼ 8402) 5790 (68.9) 2612 (31.1) <.001  negative participants stressed the importance of retesting but4 (n ¼ 2909) 1609 (55.3) 1300 (44.7) to our knowledge, our analysis is the first to describe HIV Gestational categorya <28-week pregnancy 7256 (68.5) 3331 (31.5) <.001 retesting in the context of PMTCT programs and particularly ¼ in Zambia.4,5,14-16(n 10 587) Our findings reflect the landscape of MNCH 28-week pregnancy 866 (42.6) 1166 (57.4) and HIV programs in Zambia. (n ¼ 2032) We found that retesting, which is part of the integrated a PMTCT and MNCH interventions, is affected by the signifi-Data on weeks of gestation could not be reconstructed for 4219 pregnant women. cant dropout along the MNCH and PMTCT care cascade. Indeed, 32.7% of pregnant women were lost to follow-up after their first HIV-negative test, meaning they could not be person-years. The median time between the previous retested. According to the most recent Zambia Demographic HIV-negative test and the HIV-positive one was 97 days, rang- and Health Survey 2013-2014, approximately 45% of pregnant ing from 32 to 276 days. Authors believed that this wide range women are lost from the antenatal follow-up.11 Although the Mandala et al 5 Table 2. Key PMTCT Interventions Received by Categories of Women (“Retested” versus “Initially” Tested HIVþ). Among Women Who Were HIV Positive at Retest (n ¼ 55) Among Women Who Were HIV Positive at the Initial Test (n ¼ 2165) Access to ARVs for PMTCT; of the 55: Access to ARVs for PMTCT; of the 2165: 47 (85.5%) received any ARV regime 1981 (91.5%) received any ARV regime 44 (80.0%) received AZT þ NVPa 1764 (81.5%) received AZT þ NVPa 2 (3.6%) received triple ARV regimeb 192 (8.9%) received triple ARV regimeb 1 (1.8%) received sdNVPc 0 (0.0%) received sdNVPc 0 (0.0%) unspecified ARV regimen 25 (1.2%) unspecified ARV regimen 8 (14.5%) received no ARVs 184 (8.5%) received no ARVs A total of 24 (43.6%) women had a CD4 test performed and results A total of 1759 (81.2%) women had a CD4 test performed and results available; the median CD4 count was 571 cells/mm3 (IQR: 444-773). available; the median CD4 count was 395 cells/mm3 (IQR: 271-550). Of their HIV-exposed infants, 4 (7.3%) received ARV prophylaxis and 39 Of their HIV-exposed infants, 27 (1.3%) received ARV prophylaxis and (70.9%) were reportedly exclusively breastfed for the first 6 months 906 (41.8%) were reportedly exclusively breastfed for the first of life. 6 months of life. A total of 36 exposed infants accessed HIV “early infant diagnosis” A total of 853 exposed infants accessed EID and had their results (EID) and had their results available. The median age at the time of available. The median age at the time of the dried blood collection the dried blood collection for EID was 10 weeks rangingd from 2 to for EID was 7 weeks rangingd from 2 to 111 weeks; 27 (3.2%) were 58 weeks; 4 (11.1%) were HIV positive of the 36 EID results. HIV positive of the 853 EID results. Abbreviations: ARV, antiretrovirals; EID, early infant diagnosis; IQR, interquartile range; PMTCT, prevention of mother-to-child transmission; sdNVP, single-dose nevirapine. aThis consists of zidovudine (AZT) 300 mg þ nevirapine (NVP) twice a day. bThis is a highly active antiretroviral therapy comprised of AZT þ lamivudine (3TC) þ NVP. csdNVP is a single dose of NVP (200 mg) at the onset of labor. dAuthors believe that this huge range is the reflection of the known huge turnaround time between the blood sample collection and the availability of results to the health providers. magnitude of LTFU observed in the context of this study born to HIV-positive women at initial screening (60.6% or (32.7%) appears lower than the reported LTFU of pregnant 1312/2165) compared to LTFU of infants born to mothers women in the context of general antenatal care (ANC) identified HIV positive at retesting (27.3% of 19/55). (45%), the later mirrors and probably explains the first. Because such a large proportion of participants were From our analysis, the estimated HIV incidence was 1.06 per LTFU, we could not run meaningful statistical analysis to 100 person-years slightly higher than the previously reported compare MTCT rates between infants born to mothers tested HIV incidence in Zambia, which was reported as 0.80 per 100 HIV positive at their initial antenatal visit and those born to person-years in 2012.17 A systematic review and meta-analysis mothers retested HIV positive. Women who were 35 years of that did not find a significantly higher incidence among pregnant age or older, with a parity 4 or higher, and who came for ANC women as compared to the general population.3 A similar pro- at 28 weeks of gestation or later were less likely to be retested spective study in Uganda and Zimbabwe also concluded that for HIV during their pregnancy. We could not find a plausible neither pregnancy nor lactation placed women at increased risk explanation for that observation. The overall substantial of HIV-1 acquisition.5 Our study was not powered to measure LTFU is possibly the result of pregnant women not attending the HIV incidence; thus, we cannot compare our findings to the the number antenatal visits as recommended by the Zambian cited publications and draw a meaningful conclusion. norms and guidelines. We could not explain the higher proportion of pregnant Based on available data, we observed a higher proportion of women who retested HIV positive in Luapula (2.1%) compared MTCT among infants of mothers who retested HIV positive— to 0% to 0.6% in the 4 other provinces; the overall low pro- 11.1% (4/36)—than in infants born to mothers who had tested portion of women who retested HIV positive did not allow for HIV positive at their initial visit—3.2% (27/853; see Table 2). meaningful statistical analysis. We suggest that the difference in the MTCT rates is consistent Pregnant women who seroconverted were more than likely with other studies, which found higher MTCT rates when HIV cases of acute HIV infection. Indeed, the average CD4 count infection is acquired during pregnancy.3,9,18 was significantly higher among women who retested HIV pos- The major limitation of our study is the huge proportion of itive (median: 570 cells/mm3) than those who tested HIV pos- LTFU throughout the cascade of the integrated PMTCT and itive at the initial contact (median: 390 cells/mm3), a proxy MNCH. The small number of women that seroconverted (55) indicating that those who retested HIV positive were in an limited our capacity to assess the MTCT rates associated with earlier stage of HIV infection (see Table 2). incident HIV infection. We believe that this is a call to actively The overall proportion of HIV-exposed infants LTFU prior analyze the capacity of programs to implement HIV retesting to accessing early HIV diagnosis was remarkably high at 60% and (for those found HIV positive) linkage to care, as one of the (1331/2220). That proportion of LTFU was higher for infants criteria for performance of PMTCT services. 6 Journal of the International Association of Providers of AIDS Care Conclusion transmission in South Africa. J Infect Dis. 2011;203(9): 1231–1234. In rural Zambia, in the 10 health facilities studied, retesting 5. Morrison CS, Wang J, Van Der Pol B, Padian N, Salata RA, of previously HIV-negative women was offered but only 2 of Richardson BA. Pregnancy and the risk of HIV-1 acquisition 3 women received that service. Women who were 35 years of among women in Uganda and Zimbabwe. AIDS. 2007;21(8): age or older, with a parity 4 or higher, and who came for ANC 1027–1034. at 28 weeks of gestation or later were less likely to be retested 6. De Schacht C, Mabunda N, Ferreira OC, et al. High HIV inci- for HIV during their pregnancy. Incidence of HIV infection dence in the postpartum period sustains vertical transmission in observed was comparable to the known HIV incidence in settings with generalized epidemics: a cohort study in Southern Zambia (0.80 per 100 person-years). Mozambique. J Int AIDS Soc. 2014;17:18808. With observed vertical transmission rates of 11.1% and 7. Feldblum PJ, Enosse S, Dube K, et al. HIV prevalence and 3.2% from mothers with “incident” and “non-incident” HIV incidence in a cohort of women at higher risk for HIV acquisi- infection, respectively, we suggest that studies be conducted tion in Chókwè, southern Mozambique. PLoS One. 2014;9(5): to rigorously measure the proportion of MTCT attributable to e97547. women who seroconvert during pregnancy in program settings. 8. De Schacht C, Hoffman HJ, Mabunda N, et al. High rates of HIV We also suggest that PMTCT programs continue to offer retest- seroconversion in pregnant women and low reported levels of ing and thrive to improve its uptake. Efforts to reduce LTFU HIV testing among male partners in Southern Mozambique: along the cascade of MNCH and PMTCT should also be con- results from a mixed methods study. PLoS One. 2014;9(12): sidered to optimize PMTCT. e115014. Authors’ Note 9. Brenner BG, Roger M, Routy JP, et al. High rates of forward Data can be made available upon request but is not included in the transmission events after acute/early HIV-1 infection. J Infect submission at this time. Per FHI 360 policy, it would require permis- Dis. 2007;195(7):951–959. sion from the country office and the Zambia Prevention, Care and 10. Ministry of Health Z. Zambia Consolidated Guidelines for Treat- Treatment Partnership, which includes the Ministry of Health and the ment and Prevention of HIV. Lusaka, Zambia: Ministry of Health Ministry of Community Development and Mother and Child Health. Z; 2016. 11. Central Statistical Office Lusaka Zambia MoHLZ, University of Acknowledgements Zambia Teaching Hospital Virology Laboratory Lusaka Zambia, The authors would like to acknowledge Shelly Amieva and Paige University of Zambia Department of Population Studies Lusaka Zaitlin for proof-reading and editing the manuscript. Zambia, Tropical Diseases Research Centre Ndola Zambia, The DHS Program ICF International. Zambia Demographic and Declaration of Conflicting Interests Health Survey 2013-14. Rockville, MD; 2015. The author(s) declared no potential conflicts of interest with respect to 12. Ministry of Health Z. National Protocol Guidelines: Integrated the research, authorship, and/or publication of this article. Prevention of Mother to Child Transmission of HIV. Lusaka, Funding Zambia: Ministry of Health Z; 2007. 13. Ministry of Health Z. Zambia Consolidated Guidelines for Treat- The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This ment and Prevention of HIV Infection. Lusaka, Zambia: Ministry research was made possible thanks to funding from FHI 360. of Health Z; 2013. 14. Kinuthia J, Drake AL, Matemo D, et al. HIV acquisition during ORCID iD pregnancy and postpartum is associated with genital infections Justin Mandala https://orcid.org/0000-0002-3878-0693 and partnership characteristics. AIDS. 2015;29(15):2025–2033. 15. Moodley D, Esterhuizen TM, Pather T, Chetty V, Ngaleka L. References High HIV incidence during pregnancy: compelling reason for 1. United Nations International Children’s Emergency Fund. For repeat HIV testing. AIDS. 2009;23(10):1255–1259. Every Child, End AIDS—Seventh Stocktaking Report. 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