Vertical transmission of HIV among pregnant women who initially had false–negative rapid HIV tests in four South African antenatal clinics

Autoři: Simnikiwe H. Mayaphi aff001;  Desmond J. Martin aff001;  Thomas C. Quinn aff004;  Anton C. Stoltz aff006
Působiště autorů: Department of Medical Virology, University of Pretoria, City of Tshwane, South Africa aff001;  National Health Laboratory Service–Tshwane Academic Division (NHLS–TAD), City of Tshwane, South Africa aff002;  Toga Laboratories, Johannesburg, South Africa aff003;  Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America aff004;  Johns Hopkins University School of Medicine, Baltimore, Maryland, United States of America aff005;  Division of Infectious Diseases, Department of Internal Medicine, University of Pretoria, City of Tshwane, South Africa aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article



There is a risk of mother-to-child transmission of HIV (MTCT) during pregnancy and breastfeeding. The aim of this study was to assess vertical transmission of HIV among pregnant women who initially had false–negative rapid HIV tests in South African antenatal care (ANC) clinics.


Pregnant participants were enrolled in a diagnostic study that used nucleic acid amplification testing (NAAT) to screen for early HIV infection among individuals who tested negative on rapid HIV tests used at the point-of-care (POC) facilities. Participants were enrolled from four ANC clinics in the Tshwane district of South Africa. All NAAT-positive participants were recalled to the clinics for further management. Vertical transmission was assessed among exposed infants whose HIV polymerase chain reaction (PCR) results were available.


This study enrolled 8208 pregnant participants who tested negative on rapid HIV tests between 2013 and 2016. Their median age was 26 years (interquartile range [IQR]: 23–30). NAAT detected HIV infections in 0.6% (n = 49; 95% confidence interval {CI}: 0.5–0.8) of all study participants. The distribution of these infections among the four clinics ranged from 0.3%– 1.1%, but this was not statistically significant (p = 0.07). Forty-seven participants (95.9%) were successfully recalled and referred for antiretroviral treatment initiation as part of prevention of MTCT (PMTCT). Most women with newly diagnosed HIV infection presented for the first ANC visit in the second (61.9%, n = 26) and third (31.0%, n = 13) trimesters. HIV PCR results were available for thirty-two infants, three of whom tested positive (9.4%; 95% CI: 1.98–25.02).


This study showed that supplemental HIV testing for pregnant women led to earlier linkage to the PMTCT programme. Inaccurate diagnosis of HIV infection at ANC clinics is likely to undermine the efforts of eliminating MTCT particularly in HIV-endemic settings.

Klíčová slova:

Antenatal care – Enzyme-linked immunoassays – HIV diagnosis and management – HIV infections – Infants – Polymerase chain reaction – Pregnancy


1. Luzuriaga K, Mofenson LM. Challenges in the Elimination of Pediatric HIV-1 Infection N Engl J Med. 2016;374:761–70. doi: 10.1056/NEJMra1505256 26933850

2. Fasawe O, Avila C, Shaffer N, Schouten E, Chimbwandira F, Hoos D, et al. Cost-effectiveness analysis of Option B+ for HIV prevention and treatment of mothers and children in Malawi. PLoS One. 2013;8:e57778. doi: 10.1371/journal.pone.0057778 23554867

3. WHO. WHO validates elimination of mother-to-child transmission of HIV and syphilis in Thailand, Armenia, Belarus and the Republic of Moldova. 2016. Available from: Accessed on August 17, 2018.

4. WHO. Antiretroviral drugs for treating pregnant women and preventing HIV infection in infants: towards universal access: recommendations for a public health approach. 2006. Available from: Accessed on April 01, 2008.

5. WHO. Antiretroviral drugs for treating pregnant women and preventing HIV infection in infants: towards universal access: recommendations for a public health approach. 2010. Available from: Accessed on October 14, 2011.

6. WHO. Consolidated guidelines on the use of antiretroviral drugs for treating and preventing HIV infection: recommendations for a public health approach– 2nd ed. 2016. Available from: Accessed on June 28, 2016.

7. South African National Department of Health. PMTCT guidelines. 2013. Available from: Accessed on March 19, 2013.

8. Horwood C, Vermaak K, Butler L, Haskins L, Phakathi S, Rollins N. Elimination of paediatric HIV in KwaZulu-Natal, South Africa: large-scale assessment of interventions for the prevention of mother-to-child transmission. Bull World Health Organ. 2012;90:168–75. doi: 10.2471/BLT.11.092056 22461711

9. Barron P, Pillay Y, Doherty T, Sherman G, Jackson D, Bhardwaj S, et al. Eliminating mother-to-child HIV transmission in South Africa. Bull World Health Organ. 2013;91:70–4. doi: 10.2471/BLT.12.106807 23397353

10. Goga AE, Dinh T, Jackson DJ, Lombard C, Delaney KP, Puren A, et al. First population-level effectiveness evaluation of a national programme to prevent HIV transmission from mother to child, South Africa. J Epidemiol Community Health. 2015;69:240–8. doi: 10.1136/jech-2014-204535 25371480

11. Goga A, Chirinda W, Ngandu NK, Ngoma K, Bhardwaj S, Feucht U, et al. Closing the gaps to eliminate mother-to-child transmission of HIV (MTCT) in South Africa: Understanding MTCT case rates, factors that hinder the monitoring and attainment of targets, and potential game changers. S Afr Med J. 2018;108:17. doi: 10.7196/SAMJ.2018.v108i8b.13495

12. Black V, von Mollendorf CE, Moyes JA, Scott LE, Puren A, Stevens WS. Poor sensitivity of field rapid HIV testing: implications for mother-to-child transmission programme. BJOG. 2009;116:1805–8. doi: 10.1111/j.1471-0528.2009.02357.x 19781042

13. Kharsany ABM, Hancock N, Frohlich JA, Humphries HR, Abdool Karim SS, Abdool Karim Q. Screening for ‘window-period’ acute HIV infection among pregnant women in rural South Africa. HIV Med. 2010;11:661–5. doi: 10.1111/j.1468-1293.2010.00838.x 20497252

14. Mayaphi SH, Martin DJ, Quinn TC, Laeyendecker O, Olorunju SAS, Tintinger GR, et al. Detection of Acute and Early HIV-1 Infections in an HIV Hyper-Endemic Area with Limited Resources. PLoS One. 2016;11:e0164943. doi: 10.1371/journal.pone.0164943 27764165

15. Moodley D, Esterhuizen TM, Pather T, Chetty V, Ngaleka L. High HIV incidence during pregnancy: compelling reason for repeat HIV testing. AIDS. 2009;23:1255–9. doi: 10.1097/QAD.0b013e32832a5934 19455017

16. Moodley D, Esterhuizen T, Reddy L, Moodley P, Singh B, Ngaleka L, et al. Incident HIV Infection in Pregnant and Lactating Women and Its Effect on Mother-to-Child Transmission in South Africa. J Infect Dis. 2011; 203:1231–4. doi: 10.1093/infdis/jir017 21398393

17. Taha TE, James MM, Hoover DR, Sun J, Laeyendecker O, Mullis CE, et al. Association of recent HIV infection and in-utero HIV-1 transmission. AIDS. 2011;25:1357–64. doi: 10.1097/QAD.0b013e3283489d45 21572305

18. South African National Department of Health. National HIV Testing Services Policy. Department of Health, Republic of South African. 2016. Available from: Accessed on September 20, 2017.

19. Cohen MS, Shaw GM, McMichael AJ, Haynes BF. Acute HIV-1 Infection. N Engl J Med. 2011;364:1943–54. doi: 10.1056/NEJMra1011874 21591946

20. Delaney KP, Hanson DL, Masciotra S, Ethridge SF, Wesolowski L, Owen SM. Time Until Emergence of HIV Test Reactivity Following Infection With HIV-1: Implications for Interpreting Test Results and Retesting After Exposure. Clin Infect Dis. 2017;64:53–9. doi: 10.1093/cid/ciw666 27737954

21. South African National Department of Health. National consolidated guidelines for the prevention of mother-to-child transmission of HIV (PMTCT) and management of HIV in children, adolescents and adults. 2015. Available from: Accessed on June 01, 2015.

22. Strode A, Slack C, Essack Z. Child consent in South African law: Implications for researchers, service providers and policy-makers. S Afr Med J. 2010;100:249.

23. South African National Department of Health. The South African Antiretroviral Treatment Guidelines. 2013. Available from: Accessed on April 02, 2013.

24. Shisana O, Rehle T, Simbayi LC, Zuma K, Jooste S, Zungu N, et al. South African National HIV Prevalence, Incidence and Behaviour Survey, 2012. Cape Town, HSRC Press. 2014.

25. Drake AL, Richardson B, John-Stewart G, Wagner A. Incident HIV during Pregnancy and Postpartum and Risk of Mother-to-Child HIV Transmission: A Systematic Review and Meta-Analysis. PLoS Med. 2014; 11: e1001608. doi: 10.1371/journal.pmed.1001608 24586123

26. Fiscus SA, Adimora AA, Schoenbach VJ, McKinney R, Lim W, Rupar D, et al. Trends in Human Immunodeficiency Virus (HIV) Counseling, Testing, and Antiretroviral Treatment of HIV-Infected Women and Perinatal Transmission in North Carolina. J Infect Dis. 1999;180:99–105. doi: 10.1086/314840 10353867

27. Joshi S, Kulkarni V, Gangakhedkar R, Mahajan U, Sharma S, Shirole D, et al. Cost-effectiveness of a repeat HIV test in pregnancy in India. BMJ Open. 2015;5:e006718. doi: 10.1136/bmjopen-2014-006718 26068507

28. Woldesenbet S, Jackson D, Lombard C, Dinh TH, Puren A, Sherman G, et al. Missed Opportunities along the Prevention of Mother-to-Child Transmission Services Cascade in South Africa: Uptake, Determinants, and Attributable Risk (the SAPMTCTE). PLoS One. 2015;10:e0132425. doi: 10.1371/journal.pone.0132425 26147598

29. WHO. HIV assays: laboratory performance and other operational characteristics: rapid diagnostic tests (combined detection of HIV-1/2 antibodies and discriminatory detection of HIV-1 and HIV-2 antibodies): report 18. 2015. Available from: Accessed on July 21, 2018.

30. Bassett IV, Chetty S, Giddy J, Reddy S, Bishop K, Lu Z, et al. Screening for acute HIV infection in South Africa: finding acute and chronic disease. HIV Med. 2011;12:46–53. doi: 10.1111/j.1468-1293.2010.00850.x 20553336

31. WHO. Consolidated guidelines on HIV testing services 2015. Available from: Accessed on September 03, 2015.

32. Pavie J, Rachline A, Loze B, Niedbalski L, Delaugerre C, Laforgerie E, et al. Sensitivity of Five Rapid HIV Tests on Oral Fluid or Finger-Stick Whole Blood: A RealTime Comparison in a Healthcare Setting. PLoS One. 2010;5:e11581. doi: 10.1371/journal.pone.0011581 20657834

33. Kestens L, Hoofd G, Gigase PL, Deleys R, van der Groen G. HIV antigen detection in circulating immune complexes. J Virol Methods. 1991;31:67–76. doi: 10.1016/0166-0934(91)90145-p 2016394

34. Stanojevic M, Zerjav S, Jevtovic D, Markovic L. Antigen/antibody content of circulating immune complexes in HIV-infected patients. Biomed Pharmacother. 1996;50:488–93. doi: 10.1016/s0753-3322(97)89279-7 9091062

35. Wolpaw BJ, Mathews C, Chopra M, Hardie D, Lurie MN, Jennings K. Diagnosis and counselling of patients with acute HIV infection in South Africa. Sex Transm Infect. 2011;87:71–2. doi: 10.1136/sti.2009.041475 20643659

36. Mayaphi SH, Martin DJ, Olorunju SAS, Williams BG, Quinn TC, Stoltz AC. High risk exposure to HIV among sexually active individuals who tested negative on rapid HIV Tests in the Tshwane District of South Africa-The importance of behavioural prevention measures. PLoS One. 2018;13:e0192357. doi: 10.1371/journal.pone.0192357 29394288

37. Bull L, Khan AW, Barton S. Management of HIV infection in pregnancy. Obstet Gynaecol Reprod Med. 2015;25:273–8.

38. Ijeoma S, Vivian B. “They Told Me to Come Back”: Women’s Antenatal Care Booking Experience in Inner-City Johannesburg. Matern Child Health J. 2013; 17:359–67. doi: 10.1007/s10995-012-1019-6 22527767

39. Gumede S, Black V, Naidoo N, Chersich MF. Attendance at antenatal clinics in inner-city Johannesburg, South Africa and its associations with birth outcomes: analysis of data from birth registers at three facilities. BMC Public Health. 2017;17:443. doi: 10.1186/s12889-017-4347-z 28832284

40. Ebonwu J, Mumbauer A, Uys M, Wainberg ML, Medina-Marino A. Determinants of late antenatal care presentation in rural and peri-urban communities in South Africa: A cross-sectional study. PLoS One. 2018;13:e0191903. doi: 10.1371/journal.pone.0191903 29518082

41. Peltier CA, Ndayisaba GF, Lepage P, van Griensven J, Leroy V, Pharm CO, et al. Breastfeeding with maternal antiretroviral therapy or formula feeding to prevent HIV postnatal mother-to-child transmission in Rwanda. AIDS. 2009;23:2415–23. doi: 10.1097/QAD.0b013e32832ec20d 19730349

42. Shapiro RL, Hughes MD, Ogwu A, Kitch D, Lockman S, Moffat C, et al. Antiretroviral regimens in pregnancy and breast-feeding in Botswana. N Engl J Med. 2010;362:2282–94. doi: 10.1056/NEJMoa0907736 20554983

43. van Lettow M, Landes M, van Oosterhout JJ, Schouten E, Phiri H, Nkhoma E, et al. Prevention of mother-to-child transmission of HIV: a cross-sectional study in Malawi. Bull World Health Organ. 2018;96:256–65. doi: 10.2471/BLT.17.203265 29695882

44. Mauk M, Song J, Bau HH, Gross R, Bushman FD, Collman RG, et al. Miniaturized devices for point of care molecular detection of HIV. Lab on a chip. 2017;17:382–94. doi: 10.1039/c6lc01239f 28092381

45. Ondiek J, Omuomu K, Ndiege K, Namukaya Z, Mtapuri-Zinyowera S, Ncube P, et al. Multicountry Validation of SAMBA—A Novel Molecular Point-of-Care Test for HIV-1 Detection in Resource-Limited Setting. J Acquir Immune Defic Syndr. 2017;76:e52–e7. doi: 10.1097/QAI.0000000000001476 28902680

46. South African National Department of Health. Guidelines for maternity care in South Africa. 2015. Available from: Accessed on August 29, 2018.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden