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The role of the complement system in HIV infection and preeclampsia

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Abstract

Background

The complement system is a key component of the innate immune system that plays a vital role in host defense, maintains homeostasis and acts as a mediator of the adaptive immune response. The complement system could possibly play a role in the pathogenesis of HIV infection and preeclampsia (PE), both of which represent major causes of maternal death in South Africa.

Recent findings

The relationship between PE and HIV infection is unclear as PE represents an exaggerated immune response, while HIV infection is associated with a decline in immune activity. Although the complement system works to clear and neutralize HIV, it could also enhance the infectivity of HIV by various other mechanisms. It has been suggested that the dysregulation of the complement system is associated with the development of PE.

Conclusion

There is currently a paucity of information on the combined effect of the complement system in HIV-associated PE. This review highlights the role of the complement system in the duality of HIV infection and PE and provides new insights into this relationship whilst also elucidating potential therapeutic targets.

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References

  1. Okoye AA, Picker LJ. CD4(+) T cell depletion in HIV infection: mechanisms of immunological failure. Immunol Rev. 2013;254:54–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Maartens G, Celum C, Lewin SR. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet. 2014;384:258–71.

    Article  PubMed  Google Scholar 

  3. UNAIDS. UNAIDS data. Geneva: UNAIDS; 2018.

    Google Scholar 

  4. UNAIDS. Ending AIDS: progress towards 90-90-90 targets. Geneva: UNAIDS; 2017.

    Google Scholar 

  5. Statistics South Africa. Statistical release P0302 mid-year population estimates 2018. Pretoria: Stats SA; 2018.

    Google Scholar 

  6. National Committee on Confidential Enquiries into Maternal Deaths. Saving mothers 2014–2016: seventh triennial report on confidential enquiries into maternal deaths in South Africa: short report. Pretoria: National Department of Health; 2018.

    Google Scholar 

  7. Moodley J, Onyangunga OA, Maharaj NR. Hypertensive disorders in primigravid black South African women: a one-year descriptive analysis. Hypertens Pregnancy. 2016;35:529–35.

    Article  CAS  PubMed  Google Scholar 

  8. Gilbert JS, Banek CT, Katz V, Babcock S, Regal JF. Complement activation in pregnancy: too much of a good thing? Hypertension. 2012;60:1114–6.

    Article  CAS  PubMed  Google Scholar 

  9. Brown MA, Magee LA, Kenny LC, Karumanchi SA, McCarthy FP, Saito S, et al. Hypertensive disorders of pregnancy: ISSHP classification, diagnosis, and management recommendations for international practice. Hypertension. 2018;72:24–43.

    Article  CAS  PubMed  Google Scholar 

  10. Silasi M, Cohen B, Karumanchi SA, Rana S. Abnormal placentation, angiogenic factors, and the pathogenesis of preeclampsia. Obstet Gynecol Clin N Am. 2010;37:239–53.

    Article  Google Scholar 

  11. Fisher SJ. Why is placentation abnormal in preeclampsia? Am J Obstet Gynecol. 2015;213:S115–22.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Williamson RD, McCarthy C, McCarthy FP, Kenny LC. Oxidative stress in pre-eclampsia; have we been looking in the wrong place? Pregnancy Hypertens. 2017;8:1–5.

    Article  PubMed  Google Scholar 

  13. Regal JF, Burwick RM, Fleming SD. The complement system and preeclampsia. Curr Hypertens Rep. 2017;19:87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hsu P, Nanan RKH. Innate and adaptive immune interactions at the fetal-maternal interface in healthy human pregnancy and pre-eclampsia. Front Immunol. 2014;5:125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Perez-Sepulveda A, Torres MJ, Khoury M, Illanes SE. Innate immune system and preeclampsia. Front Immunol. 2014;5:244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sebitloane HM, Moodley D. The impact of highly active antiretroviral therapy on obstetric conditions: a review. Eur J Obstet Gynecol Reprod Biol. 2017;210:126–31.

    Article  PubMed  Google Scholar 

  17. Alqudah MAY, Yaseen MMM, Yaseen MMS. HIV-1 strategies to overcome the immune system by evading and invading innate immune system. HIV AIDS Rev. 2016;15:1–12.

    Article  Google Scholar 

  18. Denny KJ, Woodruff TM, Taylor SM, Callaway LK. Complement in pregnancy: a delicate balance. Am J Reprod Immunol. 2013;69:3–11.

    Article  CAS  PubMed  Google Scholar 

  19. Yu Q, Yu R, Qin X. The good and evil of complement activation in HIV-1 infection. Cell Mol Immunol. 2010;7:334–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sarma JV, Ward PA. The complement system. Cell Tissue Res. 2011;343:227–35.

    Article  CAS  PubMed  Google Scholar 

  21. Merle NS, Church SE, Fremeaux-Bacchi V, Roumenina LT. Complement system part I—molecular mechanisms of activation and regulation. Front Immunol. 2015;6:262.

    PubMed  PubMed Central  Google Scholar 

  22. Noris M, Remuzzi G. Overview of complement activation and regulation. Semin Nephrol. 2013;33:479–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Lokki AI, Heikkinen-Eloranta J, Jarva H, Saisto T, Lokki M-L, Laivuori H, et al. Complement activation and regulation in preeclamptic placenta. Front Immunol. 2014;5:312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. McDonald CR, Tran V, Kain KC. Complement activation in placental malaria. Front Microbiol. 2015;6:1460.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Zhang S, Cui P. Complement system in zebrafish. Dev Comp Immunol. 2014;46:3–10.

    Article  CAS  PubMed  Google Scholar 

  26. Regal JF, Gilbert JS, Burwick RM. The complement system and adverse pregnancy outcomes. Mol Immunol. 2015;67:56–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Killick J, Morisse G, Sieger D, Astier AL. Complement as a regulator of adaptive immunity. Semin Immunopathol. 2018;40:37–48.

    Article  CAS  PubMed  Google Scholar 

  28. Derzsy Z, Prohaszka Z, Rigo J Jr, Fust G, Molvarec A. Activation of the complement system in normal pregnancy and preeclampsia. Mol Immunol. 2010;47:1500–6.

    Article  CAS  PubMed  Google Scholar 

  29. Schmidt CQ, Lambris JD, Ricklin D. Protection of host cells by complement regulators. Immunol Rev. 2016;274:152–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Alrahmani L, Willrich MAV. The complement alternative pathway and preeclampsia. Curr Hypertens Rep. 2018;20:40.

    Article  CAS  PubMed  Google Scholar 

  31. Lannaman K, Romero R, Chaiworapongsa T, Kim YM, Korzeniewski SJ, Maymon E, et al. Fetal death: an extreme manifestation of maternal anti-fetal rejection. J Perinat Med. 2017;45:851–68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Richani K, Soto E, Romero R, Espinoza J, Chaiworapongsa T, Nien JK, et al. Normal pregnancy is characterized by systemic activation of the complement system. J Matern Fetal Neonatal Med. 2005;17:239–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Albieri A, Kipnis T, Bevilacqua E. A possible role for activated complement component 3 in phagocytic activity exhibited by the mouse trophoblast. Am J Reprod Immunol. 1999;41:343–52.

    Article  CAS  PubMed  Google Scholar 

  34. Bulla R, Bossi F, Agostinis C, Radillo O, Colombo F, De Seta F, et al. Complement production by trophoblast cells at the feto-maternal interface. J Reprod Immunol. 2009;82:119–25.

    Article  CAS  PubMed  Google Scholar 

  35. Bulla R, Bossi F, Tedesco F. The complement system at the embryo implantation site: friend or foe? Front Immunol. 2012;3:55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Madhukaran SP, Alhamlan FS, Kale K, Vatish M, Madan T, Kishore U. Role of collectins and complement protein C1q in pregnancy and parturition. Immunobiology. 2016;221:1273–88.

    Article  CAS  PubMed  Google Scholar 

  37. Singh J, Ahmed A, Girardi G. Role of complement component C1q in the onset of preeclampsia in mice. Hypertension. 2011;58:716–24.

    Article  CAS  PubMed  Google Scholar 

  38. Chow FW-N, Lee Y-L, Wong P-C, Chung M-K, Lee K-F, Shu-Biu YW. Complement 3 deficiency impairs early pregnancy in mice. Mol Reprod Dev. 2009;76:647–55.

    Article  CAS  PubMed  Google Scholar 

  39. Lokki AI, Kaartokallio T, Holmberg V, Onkamo P, Koskinen LLE, Saavalainen P, et al. Analysis of complement C3 gene reveals susceptibility to severe preeclampsia. Front Immunol. 2017;8:589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lynch AM, Salmon JE. Dysregulated complement activation as a common pathway of injury in preeclampsia and other pregnancy complications. Placenta. 2010;31:561–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tomimatsu T, Mimura K, Endo M, Kumasawa K, Kimura T. Pathophysiology of preeclampsia: an angiogenic imbalance and long-lasting systemic vascular dysfunction. Hypertens Res. 2017;40:305–10.

    Article  CAS  PubMed  Google Scholar 

  42. Young BC, Levine RJ, Karumanchi SA. Pathogenesis of preeclampsia. Annu Rev Pathol. 2010;5:173–92.

    Article  CAS  PubMed  Google Scholar 

  43. Gelber SE, Brent E, Redecha P, Perino G, Tomlinson S, Davisson RL, et al. Prevention of defective placentation and pregnancy loss by blocking innate immune pathways in a syngeneic model of placental insufficiency. J Immunol. 2015;195:1129–38.

    Article  CAS  PubMed  Google Scholar 

  44. Lillegard KE, Johnson AC, Lojovich SJ, Bauer AJ, Marsh HC, Gilbert JS, et al. Complement activation is critical for placental ischemia-induced hypertension in the rat. Mol Immunol. 2013;56:91–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ma Y, Kong LR, Ge Q, Lu YY, Hong MN, Zhang Y, et al. Complement 5a-mediated trophoblasts dysfunction is involved in the development of pre-eclampsia. J Cell Mol Med. 2018;22:1034–46.

    CAS  PubMed  Google Scholar 

  46. Burwick RM, Feinberg BB. Eculizumab for the treatment of preeclampsia/HELLP syndrome. Placenta. 2013;34:201–3.

    Article  CAS  PubMed  Google Scholar 

  47. Wu W, Yang H, Feng Y, Zhang P, Li S, Wang X, et al. Polymorphisms in complement genes and risk of preeclampsia in Taiyuan, China. Inflamm Res. 2016;65:837–45.

    Article  CAS  PubMed  Google Scholar 

  48. Mohlin FC, Gros P, Mercier E, Gris JR, Blom AM. Analysis of C3 gene variants in patients with idiopathic recurrent spontaneous pregnancy loss. Front Immunol. 2018;9:1813.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Salmon JE, Heuser C, Triebwasser M, Liszewski MK, Kavanagh D, Roumenina L, et al. Mutations in complement regulatory proteins predispose to preeclampsia: a genetic analysis of the PROMISSE cohort. PLoS Med. 2011;8:e1001013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lokki AI, Aalto-Viljakainen T, Meri S, Laivuori H. Genetic analysis of membrane cofactor protein (CD46) of the complement system in women with and without preeclamptic pregnancies. PLoS One. 2015;10:e0117840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Chaiworapongsa T, Chaemsaithong P, Yeo L, Romero R. Pre-eclampsia part 1: current understanding of its pathophysiology. Nat Rev Nephrol. 2014;10:466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. He Y, Xu B, Song D, Yu F, Chen Q, Zhao M. Correlations between complement system’s activation factors and anti-angiogenesis factors in plasma of patients with early/late-onset severe preeclampsia. Hypertens Pregnancy. 2016;35:499–509.

    Article  CAS  PubMed  Google Scholar 

  53. Banadakoppa M, Balakrishnan M, Yallampalli C. Upregulation and release of soluble fms-like tyrosine kinase receptor 1 mediated by complement activation in human syncytiotrophoblast cells. Am J Reprod Immunol. 2018;80:e13033.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Guseh SH, Feinberg BB, Dawood HY, Yamamoto HS, Fichorova RN, Burwick RM. Urinary excretion of C5b-9 is associated with the anti-angiogenic state in severe preeclampsia. Am J Reprod Immunol. 2015;73:437–44.

    Article  CAS  PubMed  Google Scholar 

  55. Sones JL, Merriam AA, Seffens A, Brown-Grant DA, Butler SD, Zhao AM, et al. Angiogenic factor imbalance precedes complement deposition in placentae of the BPH/5 model of preeclampsia. FASEB J. 2018;32:2574–86.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Lynch AM, Wagner BD, Giclas PC, West NA, Gibbs RS, Holers VM. The relationship of longitudinal levels of complement bb during pregnancy with preeclampsia. Am J Reprod Immunol. 2016;75:104–11.

    Article  CAS  PubMed  Google Scholar 

  57. Velickovic I, Dalloul M, Wong KA, Bakare O, Schweis F, Garala M, et al. Complement factor B activation in patients with preeclampsia. J Reprod Immunol. 2015;109:94–100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hoffman MC, Rumer KK, Kramer A, Lynch AM, Winn VD. Maternal and fetal alternative complement pathway activation in early severe preeclampsia. Am J Reprod Immunol. 2014;71:55–60.

    Article  CAS  PubMed  Google Scholar 

  59. Banadakoppa M, Vidaeff AC, Yallampalli U, Ramin SM, Belfort MA, Yallampalli C. Complement split products in amniotic fluid in pregnancies subsequently developing early-onset preeclampsia. Dis Markers. 2015;2015:263109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Denny KJ, Coulthard LG, Finnell RH, Callaway LK, Taylor SM, Woodruff TM. Elevated complement factor C5a in maternal and umbilical cord plasma in preeclampsia. J Reprod Immunol. 2013;97:211–6.

    Article  CAS  PubMed  Google Scholar 

  61. Burwick RM, Fichorova RN, Dawood HY, Yamamoto HS, Feinberg BB. Urinary excretion of C5b-9 in severe preeclampsia: tipping the balance of complement activation in pregnancy. Hypertension. 2013;62:1040–5.

    Article  CAS  PubMed  Google Scholar 

  62. Eisen S, Dzwonek A, Klein NJ. Mannose-binding lectin in HIV infection. Future Virol. 2008;3:225–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Liu F, Dai S, Gordon J, Qin X. Complement and HIV-I infection/HIV-associated neurocognitive disorders. J Neurovirol. 2014;20:184–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Sheng A, Lan J, Wu H, Lu J, Wang Y, Chu Q, et al. A clinical case–control study on the association between mannose-binding lectin and susceptibility to HIV-1 infection among northern Han Chinese population. Int J Immunogenet. 2010;37:445–54.

    Article  CAS  PubMed  Google Scholar 

  65. Tan Y, Liu L, Luo P, Wang A, Jia T, Shen X, et al. Association between mannose-binding lectin and HIV infection and progression in a Chinese population. Mol Immunol. 2009;47:632–8.

    Article  CAS  PubMed  Google Scholar 

  66. Li H, Fu WP, Hong ZH. Replication study in Chinese Han population and meta-analysis supports association between the MBL2 gene polymorphism and HIV-1 infection. Infect Genet Evol. 2013;20:163–70.

    Article  CAS  PubMed  Google Scholar 

  67. Stoiber H, Kacani L, Speth C, Wurzner R, Dierich MP. The supportive role of complement in HIV pathogenesis. Immunol Rev. 2001;180:168–76.

    Article  CAS  PubMed  Google Scholar 

  68. Huber M, Trkola A. Humoral immunity to HIV-1: neutralization and beyond. J Intern Med. 2007;262:5–25.

    Article  CAS  PubMed  Google Scholar 

  69. Hu W, Yu Q, Hu N, Byrd D, Amet T, Shikuma C, et al. A high-affinity inhibitor of human CD59 enhances complement-mediated virolysis of HIV-1: implications for treatment of HIV-1/AIDS. J Immunol. 2010;184:359–68.

    Article  CAS  PubMed  Google Scholar 

  70. Ellegard R, Khalid M, Svanberg C, Holgersson H, Thoren Y, Wittgren MK, et al. Complement-opsonized HIV-1 alters cross talk between dendritic cells and natural killer (NK) cells to inhibit NK killing and to upregulate PD-1, CXCR70, and CCR70 on T cells. Front Immunol. 2018;9:899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Tjomsland V, Ellegard R, Burgener A, Mogk K, Che KF, Westmacott G, et al. Complement opsonization of HIV-1 results in a different intracellular processing pattern and enhanced MHC class I presentation by dendritic cells. Eur J Immunol. 2013;43:1470–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ellegard R, Crisci E, Burgener A, Sjowall C, Birse K, Westmacott G, et al. Complement opsonization of HIV-1 results in decreased antiviral and inflammatory responses in immature dendritic cells via CR3. J Immunol. 2014;193:4590–601.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Mishra N, Mohata M, Aggarwal H, Chaudhary O, Das BK, Sinha S, et al. Expression of complement receptor 3 (CR3) and regulatory protein CD46 on dendritic cells of antiretroviral naive and treated HIV-1 infected individuals: correlation with immune activation status. Mol Immunol. 2018;96:83–7.

    Article  CAS  PubMed  Google Scholar 

  74. Cornelius DC. Preeclampsia: from inflammation to immunoregulation. Clin Med Insights Blood Disord. 2018;11:1179545X17752325.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Harmon AC, Cornelius DC, Amaral LM, Faulkner JL, Cunningham MW Jr, Wallace K, et al. The role of inflammation in the pathology of preeclampsia. Clin Sci. 2016;130:409–19.

    Article  CAS  Google Scholar 

  76. Rossheim AEB, Cunningham TD, Hair PS, Shah T, Cunnion KM, Troy SB. Effects of well-controlled HIV infection on complement activation and function. J Acquir Immune Defic Syndr. 2016;73:20–6.

    Article  CAS  PubMed Central  Google Scholar 

  77. Ricklin D, Lambris JD. Complement in immune and inflammatory disorders: pathophysiological mechanisms. J Immunol. 2013;190:3831–8.

    Article  CAS  PubMed  Google Scholar 

  78. Kacani L, Banki Z, Zwirner J, Schennach H, Bajtay Z, Erdei A, et al. C5a and C5a(desArg) enhance the susceptibility of monocyte-derived macrophages to HIV infection. J Immunol. 2001;166:3410–5.

    Article  CAS  PubMed  Google Scholar 

  79. Popko K, Gorska E, Stelmaszczyk-Emmel A, Plywaczewski R, Stoklosa A, Gorecka D, et al. Proinflammatory cytokines Il-6 and TNF-alpha and the development of inflammation in obese subjects. Eur J Med Res. 2010;15(Suppl 2):120–2.

    PubMed  PubMed Central  Google Scholar 

  80. Huson MAM, Wouters D, van Mierlo G, Grobusch MP, Zeerleder SS, van der Poll T. HIV coinfection enhances complement activation during sepsis. J Infect Dis. 2015;212:474–83.

    Article  CAS  PubMed  Google Scholar 

  81. Khan R, Maduray K, Moodley J, Naicker T. Activation of CD35 and CD55 in HIV associated normal and pre-eclamptic pregnant women. Eur J Obstet Gynecol Reprod Biol. 2016;204:51–6.

    Article  CAS  PubMed  Google Scholar 

  82. Zhang W, Zhou Y, Ding Y. Lnc-DC mediates the over-maturation of decidual dendritic cells and induces the increase in Th1 cells in preeclampsia. Am J Reprod Immunol. 2017;77:e12647.

    Article  CAS  Google Scholar 

  83. Lutz MB, Schuler G. Immature, semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol. 2002;23:445–9.

    Article  CAS  PubMed  Google Scholar 

  84. Hsu P, Santner-Nanan B, Dahlstrom JE, Fadia M, Chandra A, Peek M, et al. Altered decidual DC-SIGN + antigen-presenting cells and impaired regulatory T-cell induction in preeclampsia. Am J Pathol. 2012;181:2149–60.

    Article  CAS  PubMed  Google Scholar 

  85. Bryant AK, Fazeli PL, Letendre SL, Ellis RJ, Potter M, Burdo TH, et al. Complement component 3 is associated with metabolic comorbidities in older HIV-positive adults. AIDS Res Hum Retrovir. 2016;32:271–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Kianpour M, Norozi S, Bahadoran P, Azadbakht L. The relationship between metabolic syndrome criteria and preeclampsia in primigravid women. Iran J Nurs Midwifery Res. 2015;20:263–8.

    PubMed  PubMed Central  Google Scholar 

  87. Siegfried N, van der Merwe L, Brocklehurst P, Sint TT. Antiretrovirals for reducing the risk of mother-to-child transmission of HIV infection. Cochrane Database Syst Rev. 2011;7:Cd003510.

    Google Scholar 

  88. Hall D, Gebhardt S, Theron G, Grove D. Pre-eclampsia and gestational hypertension are less common in HIV infected women. Pregnancy Hypertens. 2014;4:91–6.

    Article  PubMed  Google Scholar 

  89. Govender N, Naicker T, Moodley J. Maternal imbalance between pro-angiogenic and anti-angiogenic factors in HIV-infected women with pre-eclampsia. Cardiovasc J Afr. 2013;24(5):174–9.

    Article  PubMed  PubMed Central  Google Scholar 

  90. Wimalasundera RC, Larbalestier N, Smith JH, de Ruiter A, Mc GTSA, Hughes AD, et al. Pre-eclampsia, antiretroviral therapy, and immune reconstitution. Lancet. 2002;360:1152–4.

    Article  CAS  PubMed  Google Scholar 

  91. Suy A, Martinez E, Coll O, Lonca M, Palacio M, de Lazzari E, et al. Increased risk of pre-eclampsia and fetal death in HIV-infected pregnant women receiving highly active antiretroviral therapy. AIDS. 2006;20:59–66.

    Article  PubMed  Google Scholar 

  92. Sansone M, Sarno L, Saccone G, Berghella V, Maruotti GM, Migliucci A, et al. Risk of preeclampsia in human immunodeficiency virus-infected pregnant women. Obstet Gynecol. 2016;127:1027–32.

    Article  CAS  PubMed  Google Scholar 

  93. Landi B, Bezzeccheri V, Guerra B, Piemontese M, Cervi F, Cecchi L, et al. HIV infection in pregnancy and the risk of gestational hypertension and preeclampsia. World J Cardiovasc Dis. 2014;4:11.

    Article  Google Scholar 

  94. Kalumba VMS, Moodley J, Naidoo TD. Is the prevalence of pre-eclampsia affected by HIV/AIDS? A retrospective case–control study. Cardiovasc J Afr. 2013;24:24–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Boyajian T, Shah PS, Murphy KE. Risk of preeclampsia in HIV-positive pregnant women receiving HAART: a matched cohort study. J Obstet Gynaecol Can. 2012;34:136–41.

    Article  PubMed  Google Scholar 

  96. Adams JW, Watts DH, Phelps BR. A systematic review of the effect of HIV infection and antiretroviral therapy on the risk of pre-eclampsia. Int J Gynaecol Obstet. 2016;133:17–21.

    Article  PubMed  Google Scholar 

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Pillay, Y., Moodley, J. & Naicker, T. The role of the complement system in HIV infection and preeclampsia. Inflamm. Res. 68, 459–469 (2019). https://doi.org/10.1007/s00011-019-01240-0

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