Revista Brasileira de Ginecologia e Obstetrícia

Pré-eclâmpsia: mecanismo vascular na fisiopatologia e implicações para diagnóstico precoce e tratamento

DOI: 10.1055/s-0036-1592294 - volume 38 - Agosto 2016

Jose Augusto Duran Chávez, Ricardo de Carvalho Cavalli

Abstract


Full Text

Hypertensive disease of pregnancy, postpartum hemorrhage and infectious syndromes in pregnancy and puerperium are the leading causes of morbidity and mortality for pregnant women around the world.1 Their frequency varies according to the country and accessibility to health care.1 Hypertensive diseases, including preeclampsia, complicate 2–10% of all pregnancies.1 2 3 In Latin America and the Caribbean, hypertensive disorders are responsible for at least 26% of maternal deaths.3

 

Preeclampsia is a multifactorial disease caused by environmental factors that act over a genetic base, permitting the occurrence of this disorder.4 5 6 7 8 9 10 11 12 Based on this premise, the risk factors considered for the development of this disease are: overweightness; obesity; nulliparity and multiparity; being at the extremes of reproductive life; vascular diseases, such as chronic hypertension; metabolic diseases, such as diabetes mellitus; collagen diseases, such as systemic lupus erythematosus; multiple pregnancies; maternal and paternal family history12 13 14 (paternal imprinting expressed in the mother); pregnancy by assisted reproductive techniques;12 micropolycystic ovary syndrome with insulin resistance;15 severe anemia;16 antiphospholipid syndrome;17 and low-calcium diets consumed by people living at high altitudes.18 19

 

The interaction of risk factors and multiple polymorphic genes induces the synthesis of several proteins with effects differing from their original function, leading to the impairment of placental perfusion and the consequent production of mediators that damage the endothelium. The main proteins and others factors involved are listed below.7 8 20

 

Group I – vasoactive and vascular remodeling proteins: nitric oxide synthase; renin; type I and II angiotensin receptors; angiotensin converting enzyme; polycarboxypeptidase; endothelin-1; alpha and beta estrogen receptors; endoglin; tyrosine-kinase fms-like receptor-1; placental growth factor; and vascular endothelial growth factor.20

 

Group II – thrombophilia and hypofibrinolysis: methyltetrahydrofolate reductase; Leiden Factor V; prothrombin; fetal thrombophilia; plasminogen activator inhibitor-1; B3 integrin; and glycoprotein IIIA.20

 

Group III – oxidative stress, lipid metabolism, endothelial injury: epoxide hydrolase; glutathione transferase; superoxide dismutase; cytochrome P450 1A1; lipoprotein lipase; apolipoprotein E; and long-chain 3-hydroxyacyl-CoA dehydrogenase.20

 

Group IV – immunogenetic: human leukocyte antigen; interleukins 1 and 10; and tumor necrosis factor.20

 

Physiologically, in order to promote vascular remodeling, the changes of the decidua also occur in the inner area of the myometrium.21 An interaction of trophoblastic human leukocyte antigen (HLA) C, HLA-E, HLA-G with natural killer cells or dendritic cells or both is necessary for this event to occur. The presence of certain combinations of HLA-C and isoform types of immunoglobulin receptors bound to natural killer cells predispose to preeclampsia.22 23 24 25

 

The intervillous blood flow seems to begin by the 7th to 8th week of pregnancy, by connections between spiral arteries and lakes formed in the wall of the implanted blastocyst.26 A tamponade is formed early by the trophoblast that protects the embryo from high oxygen concentrations. These blockades are then replaced by the intravascular migration of the trophoblast.26 27 The onset of the circulation is normally a progressive periphery-center phenomenon, and high levels of oxidative stress in the periphery may induce the formation of the chorion laeve.26 27 Thus, from the beginning of the implantation, this process will determine the absence or a decrease in the replacement of the muscle layer of the myometrial spiral arteries, causing a low flow and high resistance in these vessels instead of what is expected in a normal pregnancy. This determines placental hypoperfusion, hypoxia and the release of pro-inflammatory cytokines that favor the formation of free radicals.7 8 28 29

 

Superoxide ion, hydroxyls and hydrogen peroxide damage the lipid bilayer through peroxidation, destroying endothelial cells and exposing the subendothelium28 29 to which platelets adhere and release thromboxane A2, causing vasoconstriction and platelet aggregation. Endothelial destruction and decreased prostacyclin production will then occur, with a vasodilating and antiaggregant effect.28 29

 

Placental hypoxia generates the production of soluble fms-like tyrosine kinase receptor-1 (sFlt-1), which binds to the vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) that are responsible for the maintenance of endothelial integrity.7 8 Therefore, the clinical expression of this process will involve elevated blood pressure powered by the decrease of nitric oxide and increased endothelin7 8 28 29 and the presence of urinary protein.30

 

The pathophysiology of other signs and symptoms, such as headache, tinnitus, scotoma, vomiting, nausea, epigastric and right upper quadrant pain, oliguria, hyperreflexia, and convulsions31 32 involves an imbalance between thromboxane and prostacyclin and the consequences of subsequent hypoxia and ischemia resulting from the obstruction of blood flow.4 5 7 31 32 Blood concentration is further increased by volume changes due to loss of protein in the urine because of the presence of glomerular endotheliosis.31 32

 

It is important to note that in the brain there is a significant increase in the production of excitatory amino acids such as glutamate, which binds to the N-methyl D-aspartate (NMDA) receptor, allowing the opening of calcium channels in the cell membrane, with calcium entry into hypoxic cells triggering the typical tonic-clonic convulsions of eclampsia.33

 

The classification of hypertensive diseases has been changing, currently comprising preeclampsia-eclampsia, gestational hypertension, chronic hypertension and chronic hypertension plus superimposed preeclampsia, as well as the complication represented by the HELLP (H: hemolysis, EL: elevated liver enzymes, LP: low platelet count) syndrome.2 34

 

We use the term preeclampsia when systolic blood pressure and/or diastolic blood pressure are higher than 140/90 mmHg after 20 weeks of gestation and 300 mg or more of protein in a 24-hour urine collection, or when there is a + random protein strip or higher, or 24-hour protein levels higher than 300 mg/dL, and a protein/creatinine ratio greater than or equal to 0.3. The severity of the condition is based on the presence of arterial blood pressure higher than 160/110 mmHg, creatinine higher than 1.1 mg/dL, brain and visual disturbances, platelet count lower than 100.000/µL, and a 2-fold increase in liver enzymes. It should be remembered that the absence of urinary protein does not exclude the diagnosis because the diagnosis is made according to the severity of signs and symptoms even in the absence of proteinuria.2 34

 

Once the diagnosis is made and based on the proposed vascular pathophysiological mechanisms, the therapeutic approach can be focused on four objectives: to prevent and treat seizures;35 to treat increased blood pressure; to determine the gestational age at which to end pregnancy; and to diagnose maternal and fetal complications.

 

Regarding the first objective, the drug of choice is magnesium sulfate,33 which has been used since the early 1900's, although its effectiveness was demonstrated only one century later.33 Its mechanism of action is central (blocking NMDA receptors) and peripheral, decreasing cytosolic calcium by blocking the calcium channels on the neuromotor plate and increasing intracellular magnesium and acetylcholine in the synaptic gap.

 

Despite the risk of cardiorespiratory arrest, we can avoid magnesium intoxication with optimal clinical control of respiratory rate, osteotendinous reflexes, and diuresis. A laboratory test is not necessary for the measurements of serum magnesium.33 34 36 If cardiorespiratory arrest should occur, it may be corrected with intravenous calcium gluconate. Magnesium sulfate is administered up to 24 hours after delivery. Vasomotor symptoms should be checked before withdrawal of the drug, since their presence would be an indication to extend its administration.34

 

Unlike the first objective, the second one involves some concerns. Three drugs are available for the treatment of hypertensive crises: hydralazine, labetalol and nifedipine. The last two are superior, since hydralazine involves a higher risk of lowering the Apgar score at the first minute and inducing arterial hypotension and oliguria.34 37 In contrast, nifedipine improves diuresis by inducing afferent arteriolar vasodilation. However, according to a Cochrane review,38 medical experience is the determinant factor in choosing the ideal drug for each patient. The objective of the treatment is to maintain a diastolic pressure around 90 mmHg and a systolic pressure not exceeding 160 mmHg.34 39 For this purpose, we could use fast or osmotic release nifedipine for maintenance or perform expectant management. Alpha-metyldopa is another option which is chosen by many clinicians with a broad experience with its use.34 39 40

 

The determination of the gestational age at which to end pregnancy depends on the presence of complications such as HELLP syndrome, eclampsia and uncontrolled arterial pressure. In any case, the patient should be first stabilized before ending the pregnancy.41 42 43 44

 

Between 24 and 34 weeks of gestation, two options are available for the management of severe preeclampsia:

 

 

  1. interventionist management consisting of lung maturation with steroids and the termination of pregnancy;

  2. expectant management consisting of lung maturation with steroids, determining whether platelet counts are above 100,000 µL, checking for the presence of vasomotor symptoms, determining if systolic blood pressure is below 160 mmHg and diastolic blood pressure is about 90 mmHg with or without drugs, and checking for adequate diuresis with or without fluids, in order to give the fetus more days in the uterus.41 42 43 44

 

 

An important factor to consider in the management of preeclampsia is fluid therapy. Although there is this false idea not supported by scientific evidence that enhancing the entry of fluids will improve the prognosis, intravascular volume expansion carries a serious risk of volume overload, which could lead to pulmonary or cerebral edemas. Physicians should be careful because of the risk of acute lung edema with the excessive use of fluids.45 46

 

Finally, in order to fulfill the objective of diagnosing maternal and fetal complications, we should determine perinatal comorbidities such as oligohydramnios, intrauterine growth restriction and abruption. For this purpose, we may use fetal biometry, umbilical artery, middle cerebral artery and venous duct flowmetry, and cardiotocography.47

 

Checking fetal movements daily, using a non-stressful test twice a week, determining fluid volume weekly and fetal growth every two weeks are helpful for the assessment of fetal wellbeing.2 48

 

In addition to the immediate risks and complications for both mother and fetus, gestations that include fetal exposure to preeclampsia appear to elevate the risk of cerebrovascular and neuroanatomical changes during development. Such changes during fetal life may explain the postnatal findings of elevated risks for stroke and specific deviations of cognitive functioning, including visual spatial processing and memory, as shown in an initial pilot study by a group of researchers at Queen's University, published in this issue.49

 

Although we have presented a review of the epidemiology, physiopathology, clinical features, diagnosis and treatment of hypertensive disease of pregnancy, we believe that the main goal should be to identify patients without a previous history of preeclampsia but with potential risk factors. In this situation, we should apply predictive tests to these patients in order to determine the risk and to administer low doses of calcium and aspirin if necessary.2 43 44

 

However, the available predictive tests are useless. Furthermore, many biomarkers have been suggested,50 but none has been demonstrated to be sufficiently predictive. The combination of three interventions, that is, risk factors questionnaire, uterine artery flowmetry and some biomarkers, such as serum pregnancy-associated plasma protein-Av (PAPP-A), sFlt-1 and PlGF,50 performed during the first or second trimester may allow us to predict the possibility of the disease and to reduce the risk preeclampsia complications.2 7 51 52

 

Calcium administered at a daily dose of 1.5 to 2 g has proved to decrease the risk of preeclampsia in patients with low calcium intake34 or with risk factors or positive predictive tests for the disease. At these doses, calcium reduces the release of the parathyroid hormone, thus reducing cytosolic calcium and vascular hyperresponsiveness.43 Low aspirin doses of 80 to 150 mg have produced a modest drop of the disease in patients with risk factors.53 54 The mechanism of the drug is mediated by the irreversible blocking of platelet cyclooxygenase 1 and 2, inhibiting the aggregation and the release of thromboxane.43 44 Other drugs, such as low molecular weight heparins added to aspirin, have been suggested, but their efficacy still needs to be demonstrated.55

 

In view of the aforementioned considerations, we can see that progress is being made in the understanding of the pathophysiology of preeclampsia that allows us to explore new fields of scientific research, seeking therapeutic interventions to achieve success in the management of the disease.49 Additionally, the advance of knowledge about the disease prediction should substantially contribute to the better understanding of the prevention of preeclampsia and consequently the reduction of maternal and perinatal morbidity and mortality.


References

1 Duley L. The global impact of pre-eclampsia and eclampsia. Semin Perinatol. 2009;33(3):130-137


2 . Hypertension in pregnancy Report of the American College of Obstetricians and Gynecologists' Task Force on Hypertension in Pregnancy. Obstet Gynecol. 2013;122(5):1122-1131


3 Khan KS, Wojdyla D, Say L, Gülmezoglu AM, Van Look PFA. WHO analysis of causes of maternal death a systematic review. Lancet. 2006;367(9516):1066-1074


4 Brosens I, Robertson WB, Dixon HG. The role of spiral arteries in the pathogenesis of preeclampsia In: Obstetrics and Gynecology Annual, edWynn RM. New York: Appleton-Century-Crofts;. 1972;:177-191


5 Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy facts and controversies. Placenta. 2006;27(9-10):939-958


6 Founds SA, Dorman JS, Conley YP. Microarray technology applied to the complex disorder of preeclampsia. J Obstet Gynecol Neonatal Nurs. 2008;37(2):146-157


7 Baumann MU, Bersinger NA, Surbek DV. Serum markers for predicting pre-eclampsia. Mol Aspects Med. 2007;28(2):227-244


8 Sibai BM. Hypertensive disorders of pregnancy the United States perspective. Curr Opin Obstet Gynecol. 2008;20(2):102-106


9 Chappell S, Morgan L. Searching for genetic clues to the causes of pre-eclampsia. Clin Sci (Lond). 2006;110(4):443-458


10 Nejatizadeh A, Stobdan T, Malhotra N, Pasha MA. The genetic aspects of pre-eclampsia achievements and limitations. Biochem Genet. 2008;46(7-8):451-479


11 Wright D, Akolekar R, Syngelaki A, Poon LC, Nicolaides KH. A competing risks model in early screening for preeclampsia. Fetal Diagn Ther. 2012;32(3):171-178


12 Paré E, Parry S, McElrath TF, Pucci D, Newton A, Lim KH. Clinical risk factors for preeclampsia in the 21st century. Obstet Gynecol. 2014;124(4):763-770


13 Duckitt K, Harrington D. Risk factors for pre-eclampsia at antenatal booking systematic review of controlled studies. BMJ. 2005;330(7491):565-565


14 Lie RT, Rasmussen S, Brunborg H, Gjessing HK, Lie-Nielsen E, Irgens LM. Fetal and maternal contributions to risk of preeclampsia population based study. BMJ. 1998;316(7141):1343-1347


15 Martinez Abundis E, Gonzalez Ortiz M, Quiñones Galvan A, Ferrannini E. Hyperinsulinemia in glucose-tolerant women with preeclampsia A controlled study. Am J Hypertens. 1996;9(6):610-614


16 Bilano VL, Ota E, Ganchimeg T, Mori R, Souza JP. Risk factors of preeclampsia/ eclampsia and its adverse outcomes in low- and middle- income countries a WHO secondary analysis. PLoS ONE. 2014;9(3):-


17 . Clinical risk factors for pre-eclampsia determined in early pregnancy systematic review and meta-analysis of large cohort studies. BMJ. 2016;353:i1753-i1753


18 Hofmeyr GJ, Lawrie TA, Atallah AN, Duley L. Calcium supplementation during pregnancy for preventing hypertensive disorders and related problems. Cochrane Database Syst Rev. 2010;8(8):CD001059-CD001059


19 Herrera-Suárez CC, Vásquez-Garibay EM, Romero-Velarde E, Romo-Huerta HP, García De Alba García JE, Troyo-Sanromán R. Food habits and culture factors in pregnant adolescents. Arch Latinoam Nutr. 2008;58(1):19-26


20 Mütze S, Rudnik-Schöneborn S, Zerres K, Rath W. Genes and the preeclampsia syndrome. J Perinat Med. 2008;36(1):38-58


21 Ng EH, Chan CC, Tang OS, Yeung WS, Ho PC. The role of endometrial and subendometrial vascularity measured by three-dimensional power Doppler ultrasound in the prediction of pregnancy during frozen-thawed embryo transfer cycles. HumReprod. 2006;21(6):1612-1617


22 Hanna J, Goldman-Wohl D, Hamani Y. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med. 2006;12(9):1065-1074


23 Goldman-Wohl DS, Ariel I, Greenfield C. Lack of human leukocyte antigen-G expression in extravillous trophoblasts is associated with pre-eclampsia. Mol Hum Reprod. 2000;6(1):88-95


24 Le Bouteiller P, Pizzato N, Barakonyi A, Solier C. HLA-G, preeclampsia, immunity and vascular events. J Reprod Immunol. 2003;59(2):219-234


25 Moffett A, Hiby SE. How Does the maternal immune system contribute to the development of pre-eclampsia. Placenta. 2007;28(Suppl A):S51-S56


26 Burton GJ, Jauniaux E, Watson AL. Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy the Boyd collection revisited. Am J Obstet Gynecol. 1999;181(3):718-724


27 Burton GJ, Jauniaux E. Placental oxidative stress frommiscarriage to preeclampsia. J Soc Gynecol Investig. 2004;11(6):342-352


28 Pijnenborg R, Brosens I. Deep trophoblast invasion and spiral artery remodelling In: Pijnenborg R, Brosens I, Romero R, eds. Placental bed disorders: basic science and its translation to obstetrics. Cambridge: Cambridge University Press;. 2010;:97-107


29 Plasencia W, Maiz N, Bonino S, Kaihura C, Nicolaides KH. Uterine artery Doppler at 11 þ 0 to 13 þ 6 weeks in the prediction of preeclampsia. Ultrasound Obstet Gynecol. 2007;30(5):742-749


30 Craici IM, Wagner SJ, Bailey KR. Podocyturia predates proteinuria and clinical features of preeclampsia longitudinal prospective study. Hypertension. 2013;61(6):1289-1296


31 Sibai BM. Diagnosis, controversies, and management of the syndrome of hemolysis, elevated liver enzymes, and low platelet count. Obstet Gynecol. 2004;103(5):981-991


32 Cavkaytar S, Ugurlu EN, Karaer A, Tapisiz OL, Danisman N. Are clinical symptoms more predictive than laboratory parameters for adverse maternal outcome in HELLP syndrome. Acta Obstet Gynecol Scand. 2007;86(6):648-651


33 . Do women with pre-eclampsia, and their babies, benefit from magnesium sulphate The Magpie Trial: a randomised placebo-controlled trial. Lancet. 2002;359(9321):1877-1890


34 . Am J Obstet. Gynecol. 2000;183(1):S1-S22


35 Witlin AG, Sibai BM. Randomized trials for prevention and treatment of eclamptic convulsions In: Sibai BM, ed. Hypertensive disorders in women. Philadelphia: Saunders;. 2001;:221-227


36 Sibai BM. Magnesium sulfate prophylaxis in preeclampsia Lessons learned fromrecent trials.AmJ Obstet. Gynecol. 2004;190(6):1520-1526


37 Magee LA, Cham C, Waterman EJ, Ohlsson A, von Dadelszen P. Hydralazine for treatment of severe hypertension in pregnancy meta-analysis. BMJ. 2003;327(7421):955-960


38 Duley L, Henderson-Smart DJ, Meher S. Drugs for treatment of very high blood pressure during pregnancy. Cochrane Database Syst Rev. 2006;3(3):CD001449-CD001449


39 . The detection, investigation and management of hypertension in pregnancy executive summary. Aust N Z J Obstet Gynaecol. 2000;40(2):133-138


40 Rey E, LeLorier J, Burgess E, Lange IR, Leduc L. Report of the Canadian Hypertension Society Consensus Conference 3. Pharmacologic treatment of hypertensive disorders in pregnancy. CMAJ. 1997;157(9):1245-1254


41 Sibai BM. Diagnosis andmanagement of gestational hypertension and preeclampsia. Obstet Gynecol. 2003;102(1):181-192


42 Vigil-De Gracia P, Montufar-Rueda C, Ruiz J. Expectant management of severe preeclampsia and preeclampsia superimposed on chronic hypertension between 24 and 34 weeks' gestation. Eur J Obstet Gynecol Reprod Biol. 2003;107(1):24-27


43 Sibai B, Dekker G, Kupferminc M. Pre-eclampsia. Lancet. 2005;365(9461):785-799


44 Steegers EA, von Dadelszen P, Duvekot JJ, Pijnenborg R. Preeclampsia. Lancet. 2010;376(9741):631-644


45 Heilmann L, Gerhold S, von Tempelhoff GF, Pollow K. The role of intravenous volume expansion in moderate pre-eclampsia. Clin Hemorheol Microcirc. 2001;25(3-4):83-89


46 Duley L, Williams J, Henderson-Smart DJ. Plasma volume expansion for treatment of women with pre-eclampsia. Cochrane Database Syst Rev. 2000;4(2):CD001805-CD001805


47 Leveno KJ, Cunningham FG. Management In: Lindheimer MD, Roberts JM, CunninghamFG, eds. Chesley's hypertensive disorders in pregnancy.Amsterdam:Academic Press, Elsevier;. 2009;:389-414


48 Chaiworapongsa T, Chaemsaithong P, Korzeniewski SJ, Yeo L, Romero R. Pre-eclampsia part 2: prediction, prevention and management. Nat Rev Nephrol. 2014;10(9):531-540


49 Dang F, Croy BA, Stroman PW, Figueiró-Filho EA. Impacts of Preeclampsia on the Brain of the Offspring. Rev Bras Ginecol Obstet. 2016;:-


50 Poon LC, Nicolaides KH. Early prediction of preeclampsia. Obstet Gynecol Int. 2014;2014:297397-297397


51 Papageorghiou AT, Campbell S. First trimester screening for preeclampsia. Curr Opin Obstet Gynecol. 2006;18(6):594-600


52 O'Gorman N, Wright D, Syngelaki A. Competing risks model in screening for preeclampsia by maternal factors and biomarkers at 11-13 weeks gestation. Am J Obstet Gynecol. 2016;214(1):103. e1-103.e12


53 Roberge S, Giguère Y, Villa P. Early administration of low-dose aspirin for the prevention of severe and mild preeclampsia a systematic review and meta-analysis. Am J Perinatol. 2012;29(7):551-556


54 Roberge S, Villa P, Nicolaides K. Early administration of lowdose aspirin for the prevention of preterm and term preeclampsia a systematic review and meta-analysis. Fetal Diagn Ther. 2012;31(3):141-146


55 Roberge S, Demers S, Nicolaides KH, Bureau M, Côté S, Bujold E. Prevention of pre-eclampsia by low-molecular-weight heparin in addition to aspirin a meta-analysis. Ultrasound Obstet Gynecol. 2016;47(5):548-553