Journal of Nephrology

, Volume 30, Issue 3, pp 307–317 | Cite as

A best practice position statement on the role of the nephrologist in the prevention and follow-up of preeclampsia: the Italian study group on kidney and pregnancy

  • Giorgina Barbara Piccoli
  • Gianfranca Cabiddu
  • Santina Castellino
  • Giuseppe Gernone
  • Domenico Santoro
  • Gabriella Moroni
  • Donatella Spotti
  • Franca Giacchino
  • Rossella Attini
  • Monica Limardo
  • Stefania Maxia
  • Antioco Fois
  • Linda Gammaro
  • Tullia Todros
  • on behalf of Kidney and Pregnancy Study Group of Italian Society of Nephrology
Position papers and Guidelines
Part of the following topical collections:
  1. Obstetric Nephrology


Preeclampsia (PE) is a protean syndrome causing a transitory kidney disease, characterised by hypertension and proteinuria, ultimately reversible after delivery. Its prevalence is variously estimated, from 3 to 5% to 10% if all the related disorders, including also pregnancy-induced hypertension (PIH) and HELLP syndrome (haemolysis, increase in liver enzyme, low platelets) are included. Both nephrologists and obstetricians are involved in the management of the disease, according to different protocols, and the clinical management, as well as the role for each specialty, differs worldwide. The increased awareness of the role of chronic kidney disease in pregnancy, complicating up to 3% of pregnancies, and the knowledge that PE is associated with an increased risk for development of CKD later in life have recently increased the interest and redesigned the role of the nephrologists in this context. However, while the heterogeneous definitions of PE, its recent reclassification, an emerging role for biochemical biomarkers, the growing body of epidemiological data and the new potential therapeutic interventions lead to counsel long-term follow-up, the lack of resources for chronic patients and the increasing costs of care limit the potential for preventive actions, and suggest tailoring specific interventional strategies. The aim of the present position statement of the Kidney and Pregnancy Study Group of the Italian Society of Nephrology is to review the literature and to try to identify theoretical and pragmatic bases for an agreed management of PE in the nephrological setting, with particular attention to the prevention of the syndrome (recurrent PE, presence of baseline CKD) and to the organization of the postpartum follow-up.


Chronic kidney disease Evidence based medicine Pregnancy Hypertension Proteinuria Preeclampsia Pre-term delivery 


Compliance with ethical standards

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Conflicts of interest

The authors declare they have no conflict of interest.


  1. 1.
    Phipps E, Prasanna D, Brima W, Jim B (2016) Preeclampsia: updates in pathogenesis, definitions, and guidelines. Clin J Am Soc Nephrol 11(6):1102–1113PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg P (2010) Pre-eclampsia. The Lancet 376:631–644CrossRefGoogle Scholar
  3. 3.
    Umans JG (2012) Obstetric nephrology: preeclampsia–the nephrologist’s perspective. Clin J Am Soc Nephrol 7:2107–2113PubMedCrossRefGoogle Scholar
  4. 4.
    Dekker GA (2014) Management of preeclampsia. Pregnancy Hypertens 4(3):246–247PubMedGoogle Scholar
  5. 5.
    Roberts JM, Mascalzoni D, Ness RB, Poston L, Global Pregnancy Collaboration (2016) Collaboration to understand complex diseases: preeclampsia and adverse pregnancy outcomes. Hypertension 67(4):681–687PubMedCrossRefGoogle Scholar
  6. 6.
    Fisher SJ (2015) Why is placentation abnormal in preeclampsia? Am J Obstet Gynecol 213(4 Suppl):115–122CrossRefGoogle Scholar
  7. 7.
    Redman C (2014) Pre-eclampsia: A complex and variable disease. Pregnancy Hypertens 4(3):241–242Google Scholar
  8. 8.
    Redman CW, Sargent IL, Staff AC (2014) IFPA Senior Award Lecture: making sense of pre-eclampsia—two placental causes of preeclampsia?. Placenta 35:S20–25PubMedCrossRefGoogle Scholar
  9. 9.
    Koual M, Abbou H, Carbonnel M, Picone O, Ayoubi JM (2013) Short-term outcome of patients with preeclampsia. Vasc Health Risk Manag 9:143–148PubMedPubMedCentralGoogle Scholar
  10. 10.
    Berks D, Steegers EA, Molas M, Visser W (2009) Resolution of hypertension and proteinuria after preeclampsia. Obstet Gynecol 114(6):1307–1314PubMedCrossRefGoogle Scholar
  11. 11.
    Ferrazzani S, De Carolis S, Pomini F, Testa AC, Mastromarino C, Caruso A (1994) The duration of hypertension in the puerperium of preeclamptic women: relationship with renal impairment and week of delivery. Am J Obstet Gynecol 171(2):506–512PubMedCrossRefGoogle Scholar
  12. 12. Accessed 28 Dec 2015
  13. 13.
    Mol BWJ, Roberts CT, Thangaratinam S, Magee LA, de Groot CJM, Hofmeyr GJ (2016) Pre-eclampsia. The Lancet 387:999–1011CrossRefGoogle Scholar
  14. 14.
    Redman C (2014) The six stages of pre-eclampsia. Pregnancy Hypertens 4(3):246PubMedGoogle Scholar
  15. 15.
    Henry CS, Biedermann SA, Campbell MF, Guntupalli JS (2004) Spectrum of hypertensive emergencies in pregnancy. Crit Care Clin 20(4):697–712 ixPubMedCrossRefGoogle Scholar
  16. 16.
    Remuzzi G, Ruggenenti P (1991) Prevention and treatment of pregnancy-associated hypertension: what have we learned in the last 10 years? Am J Kidney Dis 18(3):285–305PubMedCrossRefGoogle Scholar
  17. 17.
    Leeman L, Fontaine P (2008) Hypertensive disorders of pregnancy. Am Fam Physician 78(1):93–100PubMedGoogle Scholar
  18. 18.
    Myatt L, Roberts JM (2015) Preeclampsia: Syndrome or Disease? Curr Hypertens Rep 17(11):83PubMedCrossRefGoogle Scholar
  19. 19.
    Williams D, Davison J (2008) Chronic kidney disease in pregnancy. BMJ 336(7637):211–215PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Masuyama H, Nobumoto E, Okimoto N, Inoue S, Segawa T, Hiramatsu Y (2012) Superimposed preeclampsia in women with chronic kidney disease. Gynecol Obstet Invest 74(4):274–281PubMedCrossRefGoogle Scholar
  21. 21.
    Piccoli GB, Fassio F, Attini R, Parisi S, Biolcati M, Ferraresi M et al (2012) Pregnancy in CKD: whom should we follow and why? Nephrol Dial Transplant 27(Suppl 3):iii111–i8PubMedCrossRefGoogle Scholar
  22. 22.
    Piccoli GB, Attini R, Vasario E, Conijn A, Biolcati M, D’Amico F, Consiglio V, Bontempo S, Todros T (2010) Pregnancy and chronic kidney disease: a challenge in all CKD stages. Clin J Am Soc Nephrol 5:844–855PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    van der Graaf AM, Toering TJ, Faas MM, Lely AT (2012) From preeclampsia to renal disease: a role of angiogenic factors and the renin-angiotensin aldosterone system? Nephrol Dial Transplant 27(Suppl 3):iii51–i7PubMedGoogle Scholar
  24. 24.
    von Dadelszen P, Magee LA, Roberts JM (2003) Subclassification of preeclampsia. Hypertens Pregnancy 22:143–148CrossRefGoogle Scholar
  25. 25.
    Lisonkova S, Joseph KS (2013) Incidence of preeclampsia: risk factors and outcomes associated with early- versus late-onset disease. Am J Obstet Gynecol 209(6):544.e1-544.e12PubMedCrossRefGoogle Scholar
  26. 26.
    Ciantar E, Walker JJ (2011) Pre-eclampsia, severe pre-eclampsia and hemolysis, elevated liver enzymes and low platelets syndrome: what is new? Womens Health (Lond Engl) 7(5):555–569CrossRefGoogle Scholar
  27. 27.
    Arulkumaran N, Lightstone L (2013) Severe pre-eclampsia and hypertensive crises. Best Pract Res Clin Obstet Gynaecol 27(6):877–884PubMedCrossRefGoogle Scholar
  28. 28.
    Ness RB, Roberts JM (1996) Heterogeneous causes constituting the single syndrome of preeclampsia: A hypothesis and its implications. Am J Obstet Gynecol 175:1365–1370PubMedCrossRefGoogle Scholar
  29. 29.
    Brosens I (1964) A study of the spiral arteries of the decidua basalis in normotensive and hypertensive pregnancies. J Obstet Gynaecol Br Commonw 71:222–230PubMedCrossRefGoogle Scholar
  30. 30.
    Levine RJ, Maynard SE, Qian C et al (2004) Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350:672–683PubMedCrossRefGoogle Scholar
  31. 31.
    Masuyama H, Segawa T, Sumida Y, Masumoto A, Inoue S, Akahori Y, Hiramatsu Y (2010) Different profiles of circulating angiogenic factors and adipocytokines between early- and late-onset pre-eclampsia. BJOG 117:314–320PubMedCrossRefGoogle Scholar
  32. 32.
    Rana S, Schnettler WT, Powe C, Wenger J, Salahuddin S, Cerdeira AS, Verlohren S, Perschel FH, Arany Z, Lim KH, Thadhani R, Karumanchi SA (2013) Clinical characterization and outcomes of preeclampsia with normal angiogenic profile. Hypertens Pregnancy 32:189–201PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Roberts JM, Taylor RN, Musci TJ, Rodgers GM, Hubel CA, McLaughlin MK (1989) Preeclampsia: an endothelial cell disorder. Am J Obstet Gynecol 161:1200–1204PubMedCrossRefGoogle Scholar
  34. 34.
    Kaufmann P, Black S, Huppertz B (2003) Endovascular trophoblast invasion: Implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69:1–7PubMedCrossRefGoogle Scholar
  35. 35.
    Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111:649–658PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D’Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat Med 12:642–649PubMedCrossRefGoogle Scholar
  37. 37.
    Gilbert JS, Babcock SA, Granger JP (2007) Hypertension produced by reduced uterine perfusion in pregnant rats is associated with increased soluble fms-like tyrosine kinase-1 expression. Hypertension 50:1142–1147PubMedCrossRefGoogle Scholar
  38. 38.
    Makris A, Thornton C, Thompson J, Thomson S, Martin R, Ogle R, Waugh R, McKenzie P, Kirwan P, Hennessy A (2007) Uteroplacental ischemia results in proteinuric hypertension and elevated sFLT-1. Kidney Int 71:977–984PubMedCrossRefGoogle Scholar
  39. 39.
    Roberts JM, Hubel CA (2009) The two stage model of preeclampsia: Variations on the theme. Placenta 30(Suppl A):S32–S37PubMedCrossRefGoogle Scholar
  40. 40.
    Sircar M, Thadhani R, Karumanchi SA (2015) Pathogenesis of preeclampsia. Curr Opin Nephrol Hypertens 24(2):131–138PubMedCrossRefGoogle Scholar
  41. 41.
    Piccoli GB, Cabiddu G, Attini R, Vigotti FN, Maxia S, Lepori N et al (2015) Risk of Adverse pregnancy outcomes in women with CKD. J Am Soc Nephrol 26(8):2011–2022PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Grcevska L, Polenaković M (1992) Focal glomerular sclerosis (FGS)-like lesions are not rare in preeclampsia. Clin Nephrol 38(4):233–234PubMedGoogle Scholar
  43. 43.
    Nochy D, Hinglais N, Jacquot C, Gaudry C, Remy P, Bariety J (1986) De novo focal glomerular sclerosis in preeclampsia. Clin Nephrol 25(3):116–121PubMedGoogle Scholar
  44. 44.
    Shiiki H, Dohi K, Hanatani M et al (1990) Focal and segmental glomerulosclerosis in preeclamptic patients with nephrotic syndrome. Am J Nephrol 10(3):205–212PubMedCrossRefGoogle Scholar
  45. 45.
    Kincaid-Smith P (1991) The renal lesion of preeclampsia revisited. Am J Kidney Dis 17(2):144–148PubMedCrossRefGoogle Scholar
  46. 46.
    Piccoli GB, Daidola G, Attini R, et ql (2013) Kidney biopsy in pregnancy: evidence for counselling? A systematic narrative review. BJOG 120(4):412–427PubMedCrossRefGoogle Scholar
  47. 47.
    Rolfo A, Attini R, Tavassoli E et al (2015) Is it possible to differentiate chronic kidney disease and preeclampsia by means of new and old biomarkers? a prospective study. Dis Markers 2015:127083PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Rolfo A, Attini R, Nuzzo AM et al (2013) Chronic kidney disease may be differentially diagnosed from preeclampsia by serum biomarkers. Kidney Int 83(1):177–181PubMedCrossRefGoogle Scholar
  49. 49.
    Piccoli GB, Gaglioti P, Attini R et al (2013) Pre-eclampsia or chronic kidney disease? The flow hypothesis. Nephrol Dial Transplant 28(5):1199–1206PubMedCrossRefGoogle Scholar
  50. 50.
    Piccoli GB, Cabiddu G, Attini R et al (2015) Pregnancy in chronic kidney disease: questions and answers in a changing panorama. Best Pract Res Clin Obstet Gynaecol 29(5):625–642PubMedCrossRefGoogle Scholar
  51. 51.
    Nevis IF, Reitsma A, Dominic A et al (2011) Pregnancy outcomes in women with chronic kidney disease: a systematic review. Clin J Am Soc Nephrol 6(11):2587–2598PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Piccoli GB, Conijn A, Attini R et al (2011) Pregnancy in chronic kidney disease: need for a common language. J Nephrol 24(3):282–299PubMedCrossRefGoogle Scholar
  53. 53.
    Costa RA, Hoshida MS, Alves EA, Zugaib M, Francisco RP (2016) Preeclampsia and superimposed preeclampsia: The same disease? The role of angiogenic biomarkers. Hypertens Pregnancy 35(2):139–149PubMedCrossRefGoogle Scholar
  54. 54.
    Cabiddu G, Castellino S, Gernone G, et ql (2016) A best practice position statement on pregnancy in chronic kidney disease: the Italian Study Group on Kidney and Pregnancy. J Nephrol 29(3):277–303PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Zeisler H, Llurba E, Chantraine F et al (2016) Predictive value of the sFlt-1:PlGF ratio in women with suspected preeclampsia. N Engl J Med 374(1):13–22PubMedCrossRefGoogle Scholar
  56. 56.
    Hund M, Allegranza D, Schoedl M, Dilba P, Verhagen-Kamerbeek W, Stepan H (2014) Multicenter prospective clinical study to evaluate the prediction of short-term outcome in pregnant women with suspected preeclampsia (PROGNOSIS): study protocol. BMC Pregnancy Childbirth 14:324PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Park HJ, Kim SH, Jung YW et al (2014) Screening models using multiple markers for early detection of late-onset preeclampsia in low-risk pregnancy. BMC Pregnancy Childbirth 14:35PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Forest JC, Thériault S, Massé J, Bujold E, Giguère Y (2014) Soluble Fms-like tyrosine kinase-1 to placental growth factor ratio in mid-pregnancy as a predictor of preterm preeclampsia in asymptomatic pregnant women. Clin Chem Lab Med 52(8):1169–1178PubMedCrossRefGoogle Scholar
  59. 59.
    Doherty A, Carvalho JC, Drewlo S, El-Khuffash A, Downey K, Dodds M, Kingdom J (2014) Altered hemodynamics and hyperuricemia accompany an elevated sFlt-1/PlGF ratio before the onset of early severe preeclampsia. J Obstet Gynaecol Can 36(8):692–700PubMedCrossRefGoogle Scholar
  60. 60.
    Redman CW, Staff AC (2015) Preeclampsia, biomarkers, syncytiotrophoblast stress, and placental capacity. Am J Obstet Gynecol 213(4 Suppl):S9.e1–S9.11CrossRefGoogle Scholar
  61. 61.
    Kuc S, Wortelboer EJ, van Rijn BB, Franx A, Visser GH, Schielen PC (2011) Evaluation of 7 serum biomarkers and uterine artery Doppler ultrasound for first-trimester prediction of preeclampsia: a systematic review. Obstet Gynecol Surv 66(4):225–239PubMedCrossRefGoogle Scholar
  62. 62.
    Mooney SS, Lee RM, Tong S, Brownfoot FC (2016) Expectant management of severe preterm preeclampsia: a comparison of maternal and fetal indications for delivery. J Matern Fetal Neonatal Med 3:1–6Google Scholar
  63. 63.
    McKinney D, Boyd H, Langager A, Oswald M, Pfister A, Warshak CR (2016) The impact of fetal growth restriction on latency in the setting of expectant management of preeclampsia. Am J Obstet Gynecol 214(3):395.e1-7PubMedCrossRefGoogle Scholar
  64. 64.
    Bond DM, Gordon A, Hyett J, de Vries B, Carberry AE, Morris J (2015) Planned early delivery versus expectant management of the term suspected compromised baby for improving outcomes. Cochrane Database Syst Rev 11:CD009433Google Scholar
  65. 65.
    Costa ML (2015) Preeclampsia: reflections on how to counsel about preventing recurrence. J Obstet Gynaecol Can 37(10):887–893PubMedCrossRefGoogle Scholar
  66. 66.
    Barton JR, Sibai BM (2008) Prediction and prevention of recurrent preeclampsia. Obstet Gynecol 112(2 Pt 1):359–372PubMedCrossRefGoogle Scholar
  67. 67.
    van Oostwaard MF, Langenveld J, Schuit E et al (2015) Recurrence of hypertensive disorders of pregnancy: an individual patient data metaanalysis. Am J Obstet Gynecol 212(5):624. (Erratum in: Am J Obstet Gynecol 2015; 213(3):400)PubMedGoogle Scholar
  68. 68.
    Palatnik A, Grobman WA, Miller ES (2016) Is a history of preeclampsia associated with an increased risk of a small for gestational age infant in a future pregnancy? Am J Obstet Gynecol 215(3):355.e1-6PubMedCrossRefGoogle Scholar
  69. 69.
    Wise J (2016) Cardiac abnormalities may help identify women at risk of recurrent pre-eclampsia. BMJ 352:i1089. doi: 10.1136/bmj.i1089 PubMedCrossRefGoogle Scholar
  70. 70.
    Valensise H, Lo Presti D, Gagliardi G et al (2016) Persistent maternal cardiac dysfunction after preeclampsia identifies patients at risk for recurrent preeclampsia. Hypertension 67(4):748–753PubMedCrossRefGoogle Scholar
  71. 71.
    van Kuijk SM, Delahaije DH, Dirksen CD et al (2016) For the precare Study Group. Multicenter impact analysis of a model for predicting recurrent early-onset preeclampsia: a before-after study. Hypertens Pregnancy 35(1):42–54PubMedCrossRefGoogle Scholar
  72. 72.
    Stekkinger E, Scholten RR, Heidema WM, Spaanderman ME (2015) Recurrent pre-eclampsia in women with metabolic syndrome and low plasma volume: a retrospective cohort study. BJOG 122(13):1773–1780PubMedCrossRefGoogle Scholar
  73. 73.
    Spradley FT, Palei AC, Granger JP (2015) Increased risk for the development of preeclampsia in obese pregnancies: weighing in on the mechanisms. Am J Physiol Regul Integr Comp Physiol 309(11):R1326–R1343.&nbspPubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Williams PJ, Pipkin FB (2011) The genetics of pre-eclampsia and other hypertensive disorders of pregnancy. Best Pract Res Clin Obstet Gynaecol 25(4):405–417PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Skomsvoll JF, Baste V, Irgens LM, Østensen M (2002) The recurrence risk of adverse outcome in the second pregnancy in women with rheumatic disease. Obstet Gynecol 100(6):1196–1202PubMedGoogle Scholar
  76. 76.
    Skjaerven R, Wilcox AJ, Lie RT (2002) The interval between pregnancies and the risk of preeclampsia. N Engl J Med 346(1):33–38PubMedCrossRefGoogle Scholar
  77. 77.
    Tandberg A, Klungsoyr K, Romundstad LB, Skjærven R (2015) Pre-eclampsia and assisted reproductive technologies: consequences of advanced maternal age, interbirth intervals, new partner and smoking habits. BJOG 122(7):915–922PubMedCrossRefGoogle Scholar
  78. 78.
    England L1, Zhang J (2007) Smoking and risk of preeclampsia: a systematic review. Front Biosci 12:2471–2483PubMedCrossRefGoogle Scholar
  79. 79.
    Luque-Fernandez MA, Zoega H, Valdimarsdottir U, Williams MA (2016) Deconstructing the smoking-preeclampsia paradox through a counterfactual framework. Eur J Epidemiol 31(6):613–623PubMedCrossRefGoogle Scholar
  80. 80.
    Cheung KL, Lafayette RA (2013) Renal physiology of pregnancy. Adv Chronic Kidney Dis 20(3):209–214PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Odutayo A, Hladunewich M (2012) Obstetric nephrology: renal hemodynamic and metabolic physiology in normal pregnancy. Clin J Am Soc Nephrol 7(12):2073–2080PubMedCrossRefGoogle Scholar
  82. 82.
    Smyth A, Radovic M, Garovic VD (2013) Women, kidney disease, and pregnancy. Adv Chronic Kidney Dis 20(5):402–410PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Dean SV, Lassi ZS, Imam AM, Bhutta ZA (2014) Preconception care: nutritional risks and interventions. Reprod Health (London) 11(Suppl 3):S3CrossRefGoogle Scholar
  84. 84.
    Wilson RD; Genetics Committee (2015) Pre-conception folic acid and multivitamin supplementation for the primary and secondary prevention of neural tube defects and other folic acid-sensitive congenital anomalies. J Obstet Gynaecol Can 37(6):534–552Google Scholar
  85. 85.
    Wei SQ (2014) Vitamin D and pregnancy outcomes. Curr Opin Obstet Gynecol 26(6):438–447PubMedCrossRefGoogle Scholar
  86. 86.
    Harvey NC, Holroyd C, Ntani G et al (2014) Vitamin D supplementation in pregnancy: a systematic review. Health Technol Assess 18(45):1–190CrossRefGoogle Scholar
  87. 87.
    Agrawal S, Fledderjohann J, Vellakkal S, Stuckler D (2015) Adequately diversified dietary intake and iron and folic acid supplementation during pregnancy is associated with reduced occurrence of symptoms suggestive of pre-eclampsia or eclampsia in Indian women. PLoS One 10(3):e0119120PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Basu A, Yu JY, Jenkins AJ et al (2015) Trace elements as predictors of preeclampsia in type 1 diabetic pregnancy. Nutr Res 35(5):421–430PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kim J, Kim YJ, Lee R, Moon JH, Jo I (2012) Serum levels of zinc, calcium, and iron are associated with the risk of preeclampsia in pregnant women. Nutr Res 32(10):764–769PubMedCrossRefGoogle Scholar
  90. 90.
    Villa PM, Kajantie E, Räikkönen K et al PREDO Study group (2013) Aspirin in the prevention of pre-eclampsia in high-risk women: a randomised placebo-controlled PREDO Trial and a meta-analysis of randomised trials. BJOG 120(1):64–74PubMedCrossRefGoogle Scholar
  91. 91.
    LeFevre ML, US Preventive Services Task Force (2014) Low-dose aspirin use for the prevention of morbidity and mortality from preeclampsia: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 161(11):819–826PubMedCrossRefGoogle Scholar
  92. 92.
    Werner EF, Hauspurg AK, Rouse DJ (2015) A Cost-benefit analysis of low-dose aspirin prophylaxis for the prevention of preeclampsia in the United States. Obstet Gynecol 126(6):1242–1250PubMedCrossRefGoogle Scholar
  93. 93.
    Moore GS, Allshouse AA, Post AL, Galan HL, Heyborne KD (2015) Early initiation of low-dose aspirin for reduction in preeclampsia risk in high-risk women: a secondary analysis of the MFMU High-Risk aspirin study. J Perinatol 35(5):328–331PubMedCrossRefGoogle Scholar
  94. 94.
    Vikse BE, Irgens LM, Bostad L, Iversen BM (2006) Adverse perinatal outcome and later kidney biopsy in the mother. J Am Soc Nephrol 17(3):837–845PubMedCrossRefGoogle Scholar
  95. 95.
    Vikse BE, Irgens LM, Leivestad T, Skjaerven R, Iversen BM (2008) Preeclampsia and the risk of end-stage renal disease. N Engl J Med 359(8):800–809PubMedCrossRefGoogle Scholar
  96. 96.
    McDonald SD, Han Z, Walsh MW, Gerstein HC, Devereaux PJ (2010) Kidney disease after preeclampsia: a systematic review and meta-analysis. Am J Kidney Dis 55(6):1026–1039PubMedCrossRefGoogle Scholar
  97. 97.
    Sandvik MK, Hallan S, Svarstad E, Vikse BE (2013) Preeclampsia and prevalence of microalbuminuria 10 years later. Clin J Am Soc Nephrol 8(7):1126–1134PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Kessous R, Shoham-Vardi I, Pariente G, Sergienko R, Sheiner E (2015) Long-term maternal atherosclerotic morbidity in women with pre-eclampsia. Heart 101(6):442–446PubMedCrossRefGoogle Scholar
  99. 99.
    Lewandowski AJ, Leeson P (2014) Preeclampsia, prematurity and cardiovascular health in adult life. Early Hum Dev 90(11):725–729PubMedCrossRefGoogle Scholar
  100. 100.
    Charlton F, Tooher J, Rye KA, Hennessy A (2014) Cardiovascular risk, lipids and pregnancy: preeclampsia and the risk of later life cardiovascular disease. Heart Lung Circ 23(3):203–212PubMedCrossRefGoogle Scholar
  101. 101.
    Pauli JM, Repke JT (2015) Preeclampsia: Short-term and Long-term Implications. Obstet Gynecol Clin North Am 42(2):299–313PubMedCrossRefGoogle Scholar
  102. 102.
    Ahmed R, Dunford J, Mehran R, Robson S, Kunadian V (2014) Pre-eclampsia and future cardiovascular risk among women: a review. J Am Coll Cardiol 63(18):1815–1822PubMedCrossRefGoogle Scholar
  103. 103.
    Scantlebury DC, Hayes SN (2014) How does preeclampsia predispose to future cardiovascular disease? Curr Hypertens Rep 16(9):472PubMedCrossRefGoogle Scholar
  104. 104.
    Piccoli GB, Cabiddu G, Attini R et al (2016) Hypertension in CKD pregnancy: a question of cause and effect (cause or Effect? this is the question). Curr Hypertens Rep 18(5):35PubMedCrossRefGoogle Scholar
  105. 105.
    Wu CS, Nohr EA, Bech BH, Vestergaard M, Catov JM, Olsen J (2009) Health of children born to mothers who had preeclampsia: a population-based cohort study. Am J Obstet Gynecol 201(3):269.e1-269.e10PubMedCrossRefGoogle Scholar
  106. 106.
    Geelhoed JJ, Fraser A, Tilling K et al (2010) Preeclampsia and gestational hypertension are associated with childhood blood pressure independently of family adiposity measures: the Avon Longitudinal Study of Parents and Children. Circulation 122(12):1192–1199PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Staley JR, Bradley J, Silverwood RJ et al (2015) Associations of blood pressure in pregnancy with offspring blood pressure trajectories during childhood and adolescence: findings from a prospective study. J Am Heart Assoc 4(5):pii:e001422. doi: 10.1161/JAHA.114.001422
  108. 108.
    Fraser A, Nelson SM, Macdonald-Wallis C, Sattar N, Lawlor DA (2013) Hypertensive disorders of pregnancy and cardiometabolic health in adolescent offspring. Hypertension 62(3):614–620PubMedCrossRefGoogle Scholar
  109. 109.
    Sutherland M, Ryan D, Black MJ, Kent AL (2014) Long-term renal consequences of preterm birth. Clin Perinatol 41(3):561–573PubMedCrossRefGoogle Scholar
  110. 110.
    Bartnik P, Kosinska-Kaczynska K, Kacperczyk J et al (2016) Twin chorionicity and the risk of hypertensive disorders: gestational hypertension and pre-eclampsia. Twin Res Hum Genet 10:1–6Google Scholar
  111. 111.
    Bdolah Y, Lam C, Rajakumar A et al (2008) Twin pregnancy and the risk of preeclampsia: bigger placenta or relative ischemia? Am J Obstet Gynecol 198(4):428.e1-6PubMedCrossRefGoogle Scholar
  112. 112.
    Fox NS, Roman AS, Saltzman DH, Hourizadeh T, Hastings J, Rebarber A (2014) Risk factors for preeclampsia in twin pregnancies. Am J Perinatol 31(2):163–166PubMedGoogle Scholar
  113. 113.
    Mastrobattista JM, Skupski DW, Monga M, Blanco JD, August P (1997) The rate of severe preeclampsia is increased in triplet as compared to twin gestations. Am J Perinatol 14(5):263–265PubMedCrossRefGoogle Scholar
  114. 114.
    Skrablin S, Kuvacić I, Pavicić D, Kalafatić D, Goluza T (2000) Maternal neonatal outcome in quadruplet and quintuplet versus triplet gestations. Eur J Obstet Gynecol Reprod Biol 88(2):147–152PubMedCrossRefGoogle Scholar
  115. 115.
    Piccoli GB, Arduino S, Attini R et al (2013) Multiple pregnancies in CKD patients: an explosive mix. Clin J Am Soc Nephrol 8(1):41–50PubMedCrossRefGoogle Scholar
  116. 116.
    Licciardi F (2016) Toward a better understanding of the oocyte donation/pre-eclampsia connection. Fertil Steril 106(2):267PubMedCrossRefGoogle Scholar
  117. 117.
    Blázquez A, García D, Rodríguez A, Vassena R, Figueras F, Vernaeve V (2016) Is oocyte donation a risk factor for preeclampsia? A systematic review and meta-analysis. J Assist Reprod Genet 33(7):855–863PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Masoudian P, Nasr A, de Nanassy J, Fung-Kee-Fung K, Bainbridge SA, El Demellawy D (2016) Oocyte donation pregnancies and the risk of preeclampsia or gestational hypertension: a systematic review and metaanalysis. Am J Obstet Gynecol 214(3):328–339PubMedCrossRefGoogle Scholar

Copyright information

© Italian Society of Nephrology 2017

Authors and Affiliations

  • Giorgina Barbara Piccoli
    • 11
    • 12
  • Gianfranca Cabiddu
    • 1
  • Santina Castellino
    • 2
  • Giuseppe Gernone
    • 3
  • Domenico Santoro
    • 4
  • Gabriella Moroni
    • 5
  • Donatella Spotti
    • 6
  • Franca Giacchino
    • 7
  • Rossella Attini
    • 8
  • Monica Limardo
    • 9
  • Stefania Maxia
    • 1
  • Antioco Fois
    • 1
  • Linda Gammaro
    • 10
  • Tullia Todros
    • 8
  • on behalf of Kidney and Pregnancy Study Group of Italian Society of Nephrology
  1. 1.NephrologyAzienda Ospedaliera BrotzuCagliariItaly
  2. 2.Nephrology and DialysisTaormina HospitalTaorminaItaly
  3. 3.NephrologyS. Maria Degli Angeli HospitalPutignanoItaly
  4. 4.Nephrology and DialysisAOU “G. Martino”MessinaItaly
  5. 5.NephrologyFondazione Ca’ Granda Ospedale MaggioreMilanItaly
  6. 6.Nephrology and DialysisIRCCS Ospedale San RaffaeleMilanoItaly
  7. 7.NephrologyOspedale d’IvreaIvreaItaly
  8. 8.Obstetrics, Department of SurgeryUniversity of TorinoTurinItaly
  9. 9.NephrologyAzienda Ospedaliera della Provincia di LeccoLeccoItaly
  10. 10.Nephrology Ospedale Fracastoro San BonifacioSan BonifacioItaly
  11. 11.Department of Clinical and Biological SciencesUniversity of TorinoTurinItaly
  12. 12.NephrologieCentre Hospitalier Le MansLe MansFrance

Personalised recommendations