Review Article

Novel Cardiovascular Biomarkers Associated with Increased Cardiovascular Risk in Women With Prior Preeclampsia/HELLP Syndrome: A Narrative Review

Register or Login to View PDF Permissions
Permissions× For commercial reprint enquiries please contact Springer Healthcare: ReprintsWarehouse@springernature.com.

For permissions and non-commercial reprint enquiries, please visit Copyright.com to start a request.

For author reprints, please email rob.barclay@radcliffe-group.com.
Information image
Average (ratings)
No ratings
Your rating

Abstract

Evidence has shown that women with a history of preeclampsia or haemolysis, elevated liver enzymes and low platelets (HELLP) syndrome have an increased risk of cardiovascular disease later in life. Recommendations for screening, prevention and management after such pregnancies are not yet defined. The identification of promising non-traditional cardiovascular biomarkers might be useful to predict which women are at greatest risk. Many studies are inconsistent and an overview of the most promising biomarkers is currently lacking. This narrative review provides an update of the current literature on circulating cardiovascular biomarkers that may be associated with an increased cardiovascular disease risk in women after previous preeclampsia/HELLP syndrome. Fifty-six studies on 53 biomarkers were included. From the summary of evidence, soluble fms-like tyrosine kinase-1, placental growth factor, interleukin (IL)-6, IL-6/IL-10 ratio, high-sensitivity cardiac troponin I, activin A, soluble human leukocyte antigen G, pregnancy-associated plasma protein A and norepinephrine show potential and are interesting candidate biomarkers to further explore. These biomarkers might be potentially eligible for cardiovascular risk stratification after preeclampsia/HELLP syndrome and may contribute to the development of adequate strategies for prevention of hypertension and adverse events in this population.

Disclosure:AM is a section editor on the European Cardiology Review editorial board; and MG and AM are the Guest Editors of the Women and Heart Disease special collection this did not influence peer review. EB has no conflicts of interest to declare.

Received:

Accepted:

Published online:

Correspondence Details:Angela HEM Maas, Department of Cardiology, Radboud University Medical Center, Geert Grooteplein-Zuid 10, 6525GA Nijmegen, the Netherlands. E: angela.maas@radboudumc.nl

Open Access:

This work is open access under the CC-BY-NC 4.0 License which allows users to copy, redistribute and make derivative works for non-commercial purposes, provided the original work is cited correctly.

Hypertensive disorders of pregnancy (HDP) are a group of four disorders, whose definition depends on how far along in the pregnancy the hypertension occurs and the presence of maternal organ dysfunction: chronic hypertension (CH), gestational hypertension (GH), preeclampsia (PE) and superimposed preeclampsia (SPE). HDP is a complication seen in approximately 5–15% of all pregnancies.1–4 In previous years, evidence has shown that PE and its severe variant termed haemolysis, elevated liver enzymes and low platelets (HELLP) syndrome are associated with a significant increased risk of maternal cardiovascular diseases (CVD) later in life including hypertension, coronary artery disease, heart failure, MI and stroke.5–11 PE/HELLP syndrome and CVD share common pathophysiological pathways and markers such as endothelial dysfunction, inflammation and angiogenic factors, which may explain this association.12 These findings have led to the acknowledgement of PE/HELLP syndrome as an important female-specific risk factor for CVD later in life by the American Heart Association (AHA), American Stroke Association and the European Society of Cardiology (ESC).13–15

As yet there is no consensus regarding clinical guidelines on how to optimally screen, prevent and manage CVD risk after pregnancies complicated in this way.16,17 The AHA recommends that healthcare professionals obtain pregnancy history in risk assessment for CVD, but this is infrequently implemented.13,17 Despite PE being listed as a risk enhancer of CVD by the AHA/ESC, women with a history of PE/HELLP syndrome and their doctors are often not aware of the increased risk. This may result in undetected hypertension and lack of adequate treatment and further cardiovascular risk assessment.18–20 Nonetheless, not all women who experienced PE/HELLP syndrome develop CVD later in life, indicating the existence of different levels of future risk. Currently, risk counselling for CVD is mainly based on traditional risk factors and biochemical markers (e.g. LDL and HDL cholesterol, triglycerides, glucose), only partially explaining the increased prevalence of CVD in these women.11,21,22 The identification of circulating non-traditional cardiovascular biomarkers of relevance for myocardial and coronary artery function may therefore be of additional value to determine which women are at greatest risk and to better understand the pathophysiological mechanism of CVD. Our understanding of these cardiovascular biomarkers in women has grown over the years. However, study designs vary widely and their findings have not been consistent. To date, a clear overview of the most promising biomarkers associated with CVD risk is lacking.23 The aim of this narrative review is to provide an update of the current literature on circulating non-traditional cardiovascular biomarkers in blood that may be associated with an increased cardiovascular risk in women after a previous PE/HELLP syndrome.

Flow Diagram of Study Selection Process

Article image

Review Methods

Classification and Definitions of Hypertensive Disorders of Pregnancy

PE and HELLP syndrome are characterised by hypertension developing after 20 weeks of gestation in combination with maternal organ dysfunction. In older definitions, proteinuria was mandatory, but this has been deleted in the latest guidelines.24,25 PE can be divided into early onset (e-PE) occurring before 34 weeks of gestation and late onset if it develops at 34 weeks of gestation or later (l-PE). The precise definitions of hypertension in pregnancy, PE, HELLP syndrome, GH, CH and SPE are presented in Supplementary Material Table 1.24–26

Source and Search Strategy

To find corresponding cardiovascular biomarkers, a literature search was performed in the PubMed database from inception to February 2021. The search was specified on cardiovascular biomarkers that may be associated with future CVD risk in women with a previous hypertensive disorder of pregnancy. Supplementary Material Table 2 presents the synonyms used to build a comprehensive search strategy. Further relevant studies were identified by examining the reference lists of the selected studies.

Study Selection

Observational studies, (systematic) reviews and meta-analyses were eligible for inclusion if written in English. First, titles and keywords were screened for containing terms for both PE/HELLP syndrome or HDP, as well as CVD or associated biomarkers. In addition, attention was paid to whether it concerns the risk of developing CVD in the future, not the risk of developing PE/HELLP syndrome. CVDs of interest were all pathological conditions involving the cardiovascular system including the heart, the blood vessels or the pericardium. In case there was doubt whether the study should be selected based on its title, the abstract was reviewed. Thereafter, the abstracts were screened for mentioning biomarkers in blood samples of women with (previous) PE/HELLP syndrome, linking this with CVD. Potential eligible studies were subsequently assessed by reading the full text, after which a final selection of publications was made. Studies comparing biomarker levels between women with a previous PE/HELLP syndrome and women who experienced uncomplicated, normotensive pregnancies were eligible for inclusion. Furthermore, studies investigating overlapping biomarkers between PE and any kind of CVD or studies evaluating the correlation between biomarkers and cardiovascular risk factors in women with (previous) PE/HELLP syndrome were eligible for inclusion. Biomarkers of interest were circulating non-traditional cardiovascular markers of relevance for myocardial and coronary artery function. Studies investigating only traditional markers were excluded (lipids, lipoproteins, markers of glucose metabolism, C-reactive protein). In order to gain information about women after a previous PE/HELLP syndrome, studies including only a case/group of women with GH, CH or SPE were excluded. Moreover, there was a preference for studies using a PE cohort or studies separately analysing the results of the different disorders of HDP in order to comment on PE/HELLP syndrome.

Outcomes of Interest

The primary outcome of interest is non-traditional cardiovascular biomarkers in blood that differentiate whether women with a history of PE/HELLP syndrome may have an elevated risk to develop any kind of CVD in the future or not. Another outcome measure of interest is cardiovascular biomarkers shown to be significantly different in women after previous PE/HELLP syndrome compared to controls or biomarkers correlated with cardiovascular risk factors in women with a history of PE/HELLP syndrome.

Results

Literature Identification

The process of study inclusion and exclusion is depicted in Figure 1. The initial search in PubMed yielded 843 articles. After removing non-English studies, 809 studies were screened for retrieval and finally 45 studies were included and 11 studies were added from the reference lists of selected studies. The total of 56 studies included 53 different non-traditional cardiovascular biomarkers.

Study Characteristics

Study characteristics of included studies are shown in the Supplementary Material Table S3. Included studies were published from 2001 to 2021. Most studies assessed PE/HELLP syndrome separately from other HDP; four studies used a combined group of GH and PE or other pregnancy complications. As the definition of PE has changed over the years, there is a slight difference in study population between studies. The follow-up period varied from 3–6 days to decades after pregnancy. The 53 identified biomarkers were grouped according to their biochemical function (Table 1): angiogenesis, endothelial function, inflammation, cardiac, thrombotic, micro-RNA (miRNA) and a remaining group of biomarkers that do not fit well in one of these categories and/or have only been assessed in a single study.

For the following parts of the review, women with a history of PE/HELLP syndrome are referred to as cases and women with a history of uncomplicated normotensive pregnancy as controls. If another case and/or control-group is used in the included study, this will be described.

Biomarkers of Angiogenesis

Soluble fms-like Tyrosine Kinase-1 and Placental Growth Factor

Benschop et al. associated lower mid-pregnancy placental growth factor (PlGF) concentrations with worse cardiac structure and systolic blood pressure at 6–9 years postpartum in a mixed cohort of complicated and uncomplicated pregnancies. These associations persisted after exclusion of women with complicated pregnancies.27 Another study associated increased soluble fms-like tyrosine kinase-1 (sFlt-1) and decreased PlGF values in third trimester of PE with cardiovascular risk factors at 12 years postpartum, such as increased carotid intima media thickness (cIMT) measurements and worse lipid profiles.28 Neuman et al. found lower third trimester PlGF levels in women with PE with subsequent hypertension 1-year postpartum compared to women with PE without subsequent hypertension. However, third trimester PlGF and sFlt-1 values did not show significant value to predict hypertension at one year postpartum.29

In the first 10 years after delivery, several studies found some differences in biomarker levels between cases and controls. Kvehaugen et al. reported increased sFlt-1 values, but not PlGF, in cases both at delivery and 5–8 years postpartum.30 Three other studies reported significantly higher sFlt-1 levels in cases as well at 1, 1.5 and 4.5 years postpartum.31–33 Akhter et al. additionally observed a correlation between angiogenic factors and signs of arterial aging, measured by intima thickness and intima/media thickness ratio (I/M ratio).32 In contrast, Noori et al. and Yinon et al. found comparable sFlt-1 levels in cases and controls at 12 weeks and 6–24 months postpartum. However, they used smaller subject sample sizes compared to the above mentioned studies.34,35 Noori et al. did find higher PlGF levels 12 weeks postpartum in cases, whereas Escouto et al. found comparable levels in cases and controls at 6 weeks postpartum in a larger cohort of 288 cases.34,36

After a decade postpartum, four studies reported comparable sFlt-1 and PlGF levels in cases and controls.28,37–39 Finally, a meta-analysis found modestly higher sFlt-1 levels in women with previous HDP in a pooled analysis of 704 women (359 prior HDP and 345 controls). This difference was more pronounced when the sFlt-1 level was measured closer to the pregnancy (before 94 months postpartum).40

Soluble Endoglin and Vascular Endothelial Growth Factor

Four studies found comparable soluble endoglin (sEng) levels, and six studies mentioned comparable vascular endothelial growth factor (VEGF) levels in cases and controls in the postpartum period, ranging from weeks to 12 years postpartum.28,30,31,34,35,37,39,40

Biomarkers of Endothelial Function

Soluble Intercellular Adhesion Molecule-1 and Soluble Vascular Cell Adhesion Molecule-1

In the first decade after PE, seven studies reported no difference between cases and controls for soluble intercellular adhesion molecule-1 (sICAM-1) levels.23,33,41–45 Of note, one study even described lower levels 0.7 years postpartum in women with prior e-PE.46 Between 10–20 years postpartum, three studies described higher levels in cases and one study additionally related these high levels of sICAM-1 to features of the metabolic syndrome (MetS).38,47,48 In contrast, Tanz et al. reported comparable sICAM-1 levels 17 years postpartum in cases and controls.49 However, the use of a combined case group of PE and GH, and being based on women self-reporting makes the study less reliable.49 Studies including soluble vascular cell adhesion molecule-1 (sVCAM-1) levels, ranging from 1 to 20 years postpartum, have demonstrated no difference in cases and controls.23,28,33,38,39,43,45,48 Additionally, two meta-analyses found comparable sICAM-1 and sVCAM-1 levels in cases and controls.40,50

Biomarkers and Categories

Article image

Soluble E-selectin

In a small study of 12 women with severe PE, there was a significant increase in soluble E-selectin (sE-selectin) in cases compared to controls at 3–6 days and then 12–15 weeks postpartum.51 Similarly, Chambers et al. reported higher levels in cases 3 years postpartum.42 Nonetheless, other studies have demonstrated no difference in sE-selectin at 1 and 2.5 years postpartum when comparing cases and controls.41,43 Four studies found comparable sE-selectin values 4.5–20 years postpartum in cases and controls, while Drost et al. described higher levels 10 years postpartum in a large cohort of 339 women with a history of e-PE.23,33,37,47,48

Soluble P-selectin, Soluble Intercellular Adhesion Molecule-3 and Vascular Endothelial-Cadherin

Soluble P-selectin, sICAM-3 and vascular endothelial-cadherin were mentioned in a single study, reporting no difference between cases and controls.37,51

Biomarkers of Inflammation

Interleukin 6 and Interleukin 10

Two studies reported higher interleukin (IL)-6 levels 12–14 weeks and 0.7 year postpartum in cases compared to controls.46,52 In contrast, three studies found comparable levels in cases and controls at 6 months, 1 and 2.5 years postpartum, with one of these studies examining a combined cohort of PE and GH.53–55 At 8, 9–16 and 17 years postpartum, three studies found higher levels of IL-6 in cases.47,49,56 One study observed a trend towards increased IL-6 levels and decreased IL-10 levels resulting in a higher IL-6/IL-10 ratio 20 years postpartum in cases compared to controls.57

Tumour Necrosis Factor α and Tumour Necrosis Factor Receptor 1

Vitoratos et al. found higher tumour necrosis factor (TNF)-α levels 12–14 weeks postpartum in a case-group of 17 women and Ehrenthal et al. showed higher values one year postpartum in a combined PE and GH group.52,54 However, six studies described comparable TNF-α levels in cases and controls, ranging from 6 months to 20 years postpartum, and one study even reported lower levels in cases 8 years postpartum.39,47,53,55–58 Östlund et al. found higher levels of TNF receptor 1 at 12 years postpartum in cases compared to controls.38

Other Markers of Inflammation

Two studies reported on interleukins other than IL-6 and IL-10, interferon-γ and macrophage inflammatory protein-1α at 6 months and 1.5–3.5 years postpartum. Both found comparable baseline levels but one study observed associations between inflammatory markers and multiple MetS parameters in cases and not controls and the other study showed alterations in the innate and adaptive immune response after a preeclamptic pregnancy.53,55 Finally, pentraxin-3, neutrophil gelatinase-associated lipocalin, granulocyte-macrophage colony-stimulating factor, fractalkine, calprotectin and myeloperoxidase showed no distinctive results.30,36,38,53,55,59

Biomarkers of Cardiac Function

Studies assessing postpartum levels of brain natriuretic peptide (BNP) and N-terminal prohormone BNP (NT-proBNP) described comparable levels in cases and controls.28,36,38,60 However, Alma et al. concluded that NT-proBNP and BNP differentiate both women with diastolic dysfunction from controls as well as women with preeclampsia from controls, implying common pathophysiology.61

Muijsers et al. found a strong association between high-sensitivity cardiac Troponin I (hs-cTnI) and blood pressure. Among formerly preeclamptic women, hs-cTnI levels were higher in currently hypertensive women compared to their normotensive counterparts.62

Levels of Troponin T and mid-regional pro atrial natriuretic peptide were comparable in cases and controls 12 and 5–8 years postpartum respectively.28,63

Biomarkers of Thrombosis

Fibrinogen and von Willebrand Factor

Six studies described comparable fibrinogen levels in cases and controls, ranging from 1 year to decade(s) after pregnancy.11,39,43,55,64,65 One study found increased fibrinogen levels 0.7 years postpartum in women with a previous e-PE compared to controls.46

Three studies found no difference in von Willebrand factor (VWF) values between cases and controls at 0.7-year, 1 year and decade(s) postpartum, whereas Blaauw et al. reported higher VWF levels 4.5 years postpartum in 17 women with prior e-PE.43,44,46,65 Furthermore, a meta-analysis showed no differences in cases and controls for these markers.50

Homocysteine

Five studies, of which three used a sample size of <20 cases, described comparable homocysteine (Hcy) levels in cases and controls at 3, 4.5, 5.5, 3-11 and 11 years postpartum.38,42,44,66,67 Three studies found higher levels in cases at 2.5, 8 years and decade(s) postpartum, although one study used a combined cohort of GH and PE, in which women self-reported making it less reliable.56,68,69 Wu et al. showed that cases with high Hcy levels have an increased arterial stiffness compared to cases with normal Hcy levels.70 Finally, a meta-analysis pooling 390 cases and 342 controls showed higher Hcy levels in cases.50

Plasminogen Activator Inhibitor-1, Tissue Plasminogen Activator, Endothelin-1, Thrombomodulin and D-dimer

Included studies described no significant difference in the postpartum levels of plasminogen activator inhibitor-1, tissue plasminogen activator, endothelin-1 and thrombomodulin in cases compared with controls.23,37,43,56,64,71 One study evaluated D-dimer levels 6 years postpartum and found higher levels in cases compared to controls.64

miRNA

Five studies were identified that assessed miRNA levels, all investigating different sets of miRNAs and therefore without confirmation in another study.72–76 Results of these studies are shown in Supplementary Material Table S4.

Other Biomarkers

Fifteen biomarkers examined to date show little potential: asymmetric dimethylarginine, symmetric dimethylarginine, l-arginine, homoarginine, neopterin, midregional pro adrenomedullin, adrenomedullin, cancer antigen 125, superoxide dismutase, cathepsin B, cathepsin S, cystatin C, pro neurotensin and prorelaxin 2 and neutrophil count and (re)activity.38,39,44,61,77,78 On the other hand, activin A, soluble human leukocyte antigen G (sHLA-G), pregnancy-associated plasma protein A (PAPPA) and norepinephrine did show interesting results. Shahul et al. showed that third trimester activin A levels in women with PE correlated positively with abnormal global longitudinal strain one year postpartum and that postpartum activin A level are associated with increased left ventricular mass index and worse diastolic function.79 Jacobsen et al. described that women with previous e-PE have higher levels of sHLA-G compared to controls at 1 and 3 years postpartum. This difference was not observed in the previous l-PE group.80 Drost et al. reported higher levels of PAPPA 10 years postpartum in women with a history of e-PE compared to controls after adjustment for traditional cardiovascular risk factors.23 Lampinen et al. found higher plasma norepinephrine levels 6 years postpartum in the resting lying supine position in cases compared to controls.71

Discussion

Main Findings

This narrative review presents an updated overview of the evidence available on non-traditional cardiovascular biomarkers in women with a previous PE/HELLP syndrome. After a complete review of the literature, nine biomarkers stand out as potential markers: sFlt-1, PlGF, IL-6, IL-6/IL-10 ratio, hs-cTnI, activin A, sHLA-G, PAPPA and norepinephrine.

The angiogenic marker sFlt-1 shows potential until 8 years after the index pregnancy as multiple studies show differences between cases and controls (not after 10 years postpartum). In addition, the association between the angiogenic markers sFlt-1 and PlGF and later CVD risk may be even stronger when these markers are determined during pregnancy (mid-pregnancy or third trimester). sFlt-1 is a soluble form of the VEGF receptor and neutralises both proangiogenic factors VEGF and PlGF by binding. An anti-angiogenic environment created by an increase in sFlt-1 (and sEng), and thereby decrease in PlGF and VEGF, plays a major role in the development of PE.81–84 Angiogenic factors are also associated with the development and progression of CVD. sFlt-1 levels are elevated in patients with heart failure and high levels are associated with adverse cardiovascular outcomes such as ischaemic heart disease.85–88 PlGF levels are also elevated in heart failure and are associated with intima thickening, pathophysiology of atherosclerosis, coronary heart disease and adverse cardiovascular events.89–93 Altered sFlt-1 and PlGF levels during pregnancy and the first few years postpartum may predispose these women for future CVD.

Markers of endothelial function examined to date show little potential. From the few studies that do find a difference and take time of biomarker determination into consideration, there seems to be some small trend towards increased sICAM-1 levels in cases more than 10 years postpartum, when compared with controls. However, the evidence remains too uncertain to conclude usability. In addition, results on sE-selectin are highly variable, making it unlikely to be meaningful for CVD risk stratification.

For the inflammatory biomarkers, IL-6 and the IL-6/IL-10 ratio appear to be the most promising. Years after PE, studies demonstrate a tendency towards increased proinflammatory IL-6 and decreased anti-inflammatory IL-10 levels, therefore the ratio could increase the sensitivity for detecting (subclinical) inflammation. Studies on other inflammatory biomarkers mainly showed comparable levels in cases and controls. However, two studies showed no baseline differences but alterations in inflammatory response and unique correlations between inflammatory markers and MetS in women with previous PE. Together this might hint that the alteration in baseline levels after PE is very small, or not measurable, and that an enhanced inflammatory response or unique associations explain the increased CVD risk. Inflammation plays a major role in the pathogenesis of PE, but also in atherosclerosis and coronary artery disease.94–100 Small changes in inflammatory baseline levels or response after a pregnancy with PE may explain the link with CVD.

The cardiac biomarker hs-cTnI appears to be promising as it is significantly higher in hypertensive women with a history of PE compared to their normotensive counterparts. Hs-cTnI is a widely used marker for cardiac tissue damage, such as MI, coronary heart disease, heart failure and is also associated with hypertension.101–106 Elevated levels in formerly preeclamptic women with hypertension may indicate some ongoing myocardial cell injury. BNP, NT-proBNP and MR-proANP show comparable postpartum levels in cases and controls, but these markers are increased during a preeclamptic pregnancy and are predictive for PE.61,63,107 Further research is suggested to investigate whether BNP, NT-proBNP and MR-proANP levels in pregnancy are associated with CVD risk later in life as these are known markers of heart failure.108,109

As for the thrombotic markers, only studies on Hcy show some diversity. However, no obvious trend is manifest and other thrombotic markers show comparable postpartum levels in cases and controls.

miRNA is a relatively new category of biomarker and a wide variety of miRNAs are associated with cardiovascular diseases. However, there are just a few studies linking PE and future CVD using miRNAs. These studies mainly investigate different miRNAs and lack the ability to conclude causality. At this point it is thought to be too early to make a statement on the utility of miRNAs in CVD risk stratification after PE/HELLP syndrome and studies express the need for further research.72–76

Four biomarkers were noteworthy in the remaining category: activin A, sHLA-G, PAPPA and norepinephrine. Activin A is a member of the transforming growth factor-ß family and associated with myocardial remodelling, cardiac fibrosis and involved in the pathogenesis of heart failure.110–112 sHLA-G has immunosuppressive effects and high levels indicate low-grade proinflammatory state and have been linked to negative cardiovascular health outcomes, such as decreased ejection fraction and heart failure.113–116 PAPPA is a metalloproteinase and increased levels are associated with atherosclerotic plaques, acute coronary syndrome and cardiovascular death.117–119 Finally, elevated norepinephrine levels increase arterial pressure and promote atherosclerosis and insulin resistance.120–122

The most interesting non-traditional cardiovascular biomarkers, including notification of the time period in which the biomarker level differs between cases and controls, are presented in the timeline of Figure 2. These biomarkers suggest alterations in different pathways which together might contribute to the increased cardiovascular risk seen in these women postpartum.

Strengths and Limitations

In this review we assessed differences in non-traditional cardiovascular biomarker levels between women with a previous PE/HELLP syndrome and women with a prior uncomplicated pregnancy, taking the timepoint of biomarker measurement into account. Among the included studies were also two meta-analyses. These contain pooled studies with different points in time at follow-up, ranging from weeks to decades. However, it cannot be ruled out that there might be an (optimal) point in time when the biomarker levels between cases and controls do differ from each other. This is where the present review provides new insights: by separately analysing the different studies while taking the timepoint of biomarker analyses into account. It should be noted that apart from biomarkers, there are studies investigating the potential role of imaging techniques (e.g. measuring cIMT, I/M ratio) and vascular functional testing (e.g. pulse wave velocity, augmentation index, flow mediated dilation) to screen these women postpartum.32,35,39,43,44 The predictive value of imaging and functional testing was out-of-scope for this review. The focus was on biomarkers as these are considered to be more favourable because they are easier, faster and cheaper to measure. However, the combination of most potential circulating biomarkers and functional tests could be of significance in the whole process of biomarker validation.

This review has some limitations. First, some articles may have been missed by the search strategy because they do not use the keyword ‘biomarker’, or a synonym, but the name of the biomarker itself. However, the reference lists of included studies have been scanned, so it is highly likely that these initially missed articles have nevertheless been included in the review. Overall, studies on cardiovascular biomarkers in women after PE/HELLP syndrome are quite inconsistent. This is probably due to a variety of reasons: heterogeneity of included patients (early, late, severe or mild PE, combined cohort of PE and GH), difference in the definition of PE (in older studies proteinuria was required), dissimilarities in recognition of confounders (e.g. known risk factors such as smoking and obesity) and the subsequent statistical models to adjust for it, and finally the difference in time interval between pregnancy and biomarker assessment. Besides there might be some technical variability between studies, i.e. different analysing methods, within- and between-person variation in biomarker levels and the biomarker’s stability during sample storage. The overall conclusion on the potential value of the biomarkers in this review should therefore be interpreted with some caution. Additionally, all studies were performed during or after pregnancy, making it unclear whether differences in biomarker levels were already present prepartum. Studies assessing pre-pregnancy levels do not (yet) exist, but would give information whether PE/HELLP syndrome is at least partly caused by pre-existing cardiovascular risk factors, thus potentially due to reverse causality. Furthermore, as we conducted a narrative review, the quality of the included studies has not been systematically been assessed by multiple reviewers and according to strict criteria. Of note, many studies used small sample sizes of dozens of women with a history of PE/HELLP syndrome. Also, studies compared biomarker levels at a certain time postpartum in women with a history of PE and women with a prior uncomplicated pregnancy, without discussion of the clinical relevance and implication of found statistically significant differences. For some biomarkers the (postpartum) reference range is not known, making it questionable if increased values actually are abnormal. Additionally, due to the retrospective designs of most included studies, they are able to measure association between biomarkers and CVD risk factors, but such designs are not strong enough to draw conclusions on causality. Finally, the review’s conclusion of the biomarkers in the remaining category is based on just a single published study on each particular biomarker.

Promising Biomarkers and Indication of Timepoints

Article image

Perspective

This narrative review summarises current evidence in literature on potential of non-traditional cardiovascular biomarkers in the postpartum period of PE/HELLP syndrome. At this time, sFlt-1, PlGF, IL-6, IL-6/IL-10, hs-cTnI, Activin A, sHLA-G, PAPPA and norepinephrine appear to be potential biomarkers that warrant further investigation in this population of women. Further investigations should focus on the prospective assessment of these biomarkers in women with preeclampsia and investigate whether these markers are able to distinguish women who subsequently develop hypertension and CVD, compared to those who don’t. Biomarker validation might benefit from combination with imaging or functional tests in such prospective studies to establish a link with clinical implication and predictive value for CVD in this particular population.

Click here to view Supplementary Material.

References

  1. Booker WA. Hypertensive disorders of pregnancy. Clin Perinatol 2020;47:817–33.
    Crossref | PubMed
  2. Khedagi AM, Bello NA. Hypertensive disorders of pregnancy. Cardiol Clin 2021;39:77–90.
    Crossref | PubMed
  3. Stuart JJ, Tanz LJ, Cook NR, et al. Hypertensive disorders of pregnancy and 10-year cardiovascular risk prediction. J Am Coll Cardiol 2018;72:1252–63.
    Crossref | PubMed
  4. Sutton ALM, Harper LM, Tita ATN. Hypertensive disorders in pregnancy. Obstet Gynecol Clin North Am 2018;45:333–47.
    Crossref | PubMed
  5. Vahedi FA, Gholizadeh L, Heydari M. Hypertensive disorders of pregnancy and risk of future cardiovascular disease in women. Nurs Womens Health 2020;24:91–100.
    Crossref | PubMed
  6. Bellamy L, Casas JP, Hingorani AD, Williams DJ. Pre-eclampsia and risk of cardiovascular disease and cancer in later life: systematic review and meta-analysis. BMJ 2007;335:974.
    Crossref | PubMed
  7. Brown MC, Best KE, Pearce MS, et al. Cardiovascular disease risk in women with pre-eclampsia: systematic review and meta-analysis. Eur J Epidemiol 2013;28:1–19.
    Crossref | PubMed
  8. Veiga ECA, Rocha PRH, Caviola LL, et al. Previous preeclampsia and its association with the future development of cardiovascular diseases: a systematic review and meta-analysis. Clinics (Sao Paulo) 2021;76:e1999.
    Crossref | PubMed
  9. McDonald SD, Malinowski A, Zhou Q, et al. Cardiovascular sequelae of preeclampsia/eclampsia: a systematic review and meta–analyses. Am Heart J 2008;156:918–30.
    Crossref | PubMed
  10. Wu P, Haththotuwa R, Kwok CS, et al. Preeclampsia and future cardiovascular health: A systematic review and meta-analysis. Circ Cardiovasc Qual Outcomes 2017;10.
    Crossref | PubMed
  11. Drost JT, Arpaci G, Ottervanger JP, et al. Cardiovascular risk factors in women 10 years post early preeclampsia: The Preeclampsia Risk EValuation in FEMales study (PREVFEM). Eur J Prev Cardiol 2012;19:1138–44.
    Crossref | PubMed
  12. Suvakov S, Bonner E, Nikolic V, et al. Overlapping pathogenic signalling pathways and biomarkers in preeclampsia and cardiovascular disease. Pregnancy Hypertens 2020;20:131–6.
    Crossref | PubMed
  13. Mosca L, Benjamin EJ, Berra K, et al. Effectiveness-based guidelines for the prevention of cardiovascular disease in women--2011 update: a guideline from the American Heart Association. Circulation 2011;123:1243–62.
    Crossref | PubMed
  14. Bushnell C, McCullough LD, Awad IA, et al. Guidelines for the prevention of stroke in women: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2014;45:1545–88.
    Crossref | PubMed
  15. Piepoli MF, Hoes AW, Agewall S, et al. 2016 European Guidelines on cardiovascular disease prevention in clinical practice: The Sixth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of 10 societies and by invited experts) Developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR). Eur Heart J 2016;37:2315–81.
    Crossref | PubMed
  16. Gamble DT, Brikinns B, Myint PK, Bhattacharya S. Hypertensive disorders of pregnancy and subsequent cardiovascular disease: Current national and international guidelines and the need for future research. Front Cardiovasc Med 2019;6:55.
    Crossref | PubMed
  17. Heida KY, Bots ML, de Groot CJ, et al. Cardiovascular risk management after reproductive and pregnancy-related disorders: A Dutch multidisciplinary evidence-based guideline. Eur J Prev Cardiol 2016;23:1863–79.
    Crossref | PubMed
  18. Young B, Hacker MR, Rana S. Physicians’ knowledge of future vascular disease in women with preeclampsia. Hypertens Pregnancy 2012;31:50–8.
    Crossref | PubMed
  19. Brown MC, Bell R, Collins C, et al. Women’s perception of future risk following pregnancies complicated by preeclampsia. Hypertens Pregnancy 2013;32:60–73.
    Crossref | PubMed
  20. Dijkhuis TE, Bloem F, Kusters LAJ, et al. Investigating the current knowledge and needs concerning a follow-up for long-term cardiovascular risks in Dutch women with a preeclampsia history: a qualitative study. BMC Pregnancy Childbirth 2020;20:486.
    Crossref | PubMed
  21. Magnussen EB, Vatten LJ, Smith GD, Romundstad PR. Hypertensive disorders in pregnancy and subsequently measured cardiovascular risk factors. Obstet Gynecol 2009;114:961–70.
    Crossref | PubMed
  22. Stekkinger E, Zandstra M, Peeters LLH, Spaanderman MEA. Early-onset preeclampsia and the prevalence of postpartum metabolic syndrome. Obstet Gynecol 2009;114:1076–84.
    Crossref | PubMed
  23. Drost JT, Maas AH, Holewijn S, et al. Novel cardiovascular biomarkers in women with a history of early preeclampsia. Atherosclerosis 2014;237:117–22.
    Crossref | PubMed
  24. Brown MA, Magee LA, Kenny LC, et al. The hypertensive disorders of pregnancy: ISSHP classification, diagnosis & management recommendations for international practice. Pregnancy Hypertens 2018;13:291–310.
    Crossref | PubMed
  25. Gestational Hypertension and Preeclampsia: ACOG Practice Bulletin, Number 222. Obstet Gynecol 2020;135:e237–e60.
    Crossref | PubMed
  26. American College of Obstetricians and Gynecologists’ Committee on Practice Bulletins—Obstetrics. ACOG Practice Bulletin No. 203: Chronic Hypertension in Pregnancy. Obstet Gynecol 2019;133:e26–e50.
    Crossref | PubMed
  27. Benschop L, Schalekamp-Timmermans S, Broere-Brown ZA, et al. Placental growth factor as an indicator of maternal cardiovascular risk after pregnancy. Circulation 2019;139:1698–709.
    Crossref | PubMed
  28. Garrido-Gimenez C, Mendoza M, Cruz-Lemini M, et al. Angiogenic factors and long-term cardiovascular risk in women that developed preeclampsia during pregnancy. Hypertension 2020;76:1808–16.
    Crossref | PubMed
  29. Neuman RI, Figaroa AMJ, Nieboer D, et al. Angiogenic markers during preeclampsia: Are they associated with hypertension 1 year postpartum? Pregnancy Hypertens 2020;23:116–22.
    Crossref | PubMed
  30. Kvehaugen AS, Dechend R, Ramstad HB, et al. Endothelial function and circulating biomarkers are disturbed in women and children after preeclampsia. Hypertension 2011;58:63–9.
    Crossref | PubMed
  31. Wolf M, Hubel CA, Lam C, et al. Preeclampsia and future cardiovascular disease: potential role of altered angiogenesis and insulin resistance. J Clin Endocrinol Metab 2004;89:6239–43.
    Crossref | PubMed
  32. Akhter T, Wikström AK, Larsson M, et al. Association between angiogenic factors and signs of arterial aging in women with pre-eclampsia. Ultrasound Obstet Gynecol 2017;50:93–9.
    Crossref | PubMed
  33. Tuzcu ZB, Asicioglu E, Sunbul M, et al. Circulating endothelial cell number and markers of endothelial dysfunction in previously preeclamptic women. Am J Obstet Gynecol 2015;213:533.e1–7.
    Crossref | PubMed
  34. Noori M, Donald AE, Angelakopoulou A, et al. Prospective study of placental angiogenic factors and maternal vascular function before and after preeclampsia and gestational Hypertension Circulation 2010;122:478–87.
    Crossref | PubMed
  35. Yinon Y, Kingdom JC, Odutayo A, et al. Vascular dysfunction in women with a history of preeclampsia and intrauterine growth restriction: insights into future vascular risk. Circulation 2010;122:1846–53.
    Crossref | PubMed
  36. Escouto DC, Green A, Kurlak L, et al. Postpartum evaluation of cardiovascular disease risk for women with pregnancies complicated by Hypertension Pregnancy Hypertens 2018;13:218–24.
    Crossref | PubMed
  37. Gaugler-Senden IP, Tamsma JT, van der Bent C, et al. Angiogenic factors in women ten years after severe very early onset preeclampsia. PLoS One 2012;7:e43637.
    Crossref | PubMed
  38. Östlund E, Al-Nashi M, Hamad RR, et al. Normalized endothelial function but sustained cardiovascular risk profile 11 years following a pregnancy complicated by preeclampsia Hypertens Res 2013;36:1081–7.
    Crossref | PubMed
  39. Sandvik MK, Leirgul E, Nygård O, et al. Preeclampsia in healthy women and endothelial dysfunction 10 years later. Am J Obstet Gynecol 2013;209:569.e1–e10.
    Crossref | PubMed
  40. Grand’Maison S, Pilote L, Okano M, et al. Markers of vascular dysfunction after hypertensive disorders of pregnancy: A systematic review and meta-analysis. Hypertension 2016;68:1447–58.
    Crossref | PubMed
  41. Alma LJ, De Groot CJM, De Menezes RX, et al. Endothelial dysfunction as a long-term effect of late onset hypertensive pregnancy disorders: High BMI is key. Eur J Obstet Gynecol Reprod Biol 2018;225:62-9.
    Crossref | PubMed
  42. Chambers JC, Fusi L, Malik IS, et al. Association of maternal endothelial dysfunction with preeclampsia. JAMA 2001;285:1607–12.
    Crossref | PubMed
  43. Hamad RR, Eriksson MJ, Silveira A, et al. Decreased flow-mediated dilation is present 1 year after a pre-eclamptic pregnancy. J Hypertens 2007;25:2301–7.
    Crossref | PubMed
  44. Blaauw J, Souwer ET, Coffeng SM, et al. Follow up of intima-media thickness after severe early-onset preeclampsia. Acta Obstet Gynecol Scand 2014;93:1309–16.
    Crossref | PubMed
  45. Portelinha A, Belo L, Tejera E, Rebelo I. Adhesion molecules (VCAM-1 and ICAM-1) and C-reactive protein in women with history of preeclampsia. Acta Obstet Gynecol Scand 2008;87:969–71.
    Crossref | PubMed
  46. van Rijn BB, Franx A, Steegers EA, et al. Maternal TLR4 and NOD2 gene variants, pro-inflammatory phenotype and susceptibility to early-onset preeclampsia and HELLP syndrome. PLoS One 2008;3:e1865.
    Crossref | PubMed
  47. Bokslag A, Franssen C, Alma LJ, et al. Early-onset preeclampsia predisposes to preclinical diastolic left ventricular dysfunction in the fifth decade of life: An observational study. PLoS One 2018;13:e0198908.
    Crossref | PubMed
  48. Sattar N, Ramsay J, Crawford L, et al. Classic and novel risk factor parameters in women with a history of preeclampsia. Hypertension 2003;42:39–42.
    Crossref | PubMed
  49. Tanz LJ, Stuart JJ, Missmer SA, et al. Cardiovascular biomarkers in the years following pregnancies complicated by hypertensive disorders or delivered preterm. Pregnancy Hypertens 2018;13:14–21.
    Crossref | PubMed
  50. Visser S, Hermes W, Ket JC, et al. Systematic review and metaanalysis on nonclassic cardiovascular biomarkers after hypertensive pregnancy disorders. Am J Obstet Gynecol2014;211:373.e1–9.
    Crossref | PubMed
  51. Papakonstantinou K, Economou E, Koupa E, et al. Antepartum and postpartum maternal plasma levels of E-selectin and VE-cadherin in preeclampsia, gestational proteinuria and gestational Hypertension J Matern Fetal Neonatal Med 2011;24:1027–32.
    Crossref | PubMed
  52. Vitoratos N, Economou E, Iavazzo C, et al. Maternal serum levels of TNF-alpha and IL-6 long after delivery in preeclamptic and normotensive pregnant women. Mediators Inflamm 2010;2010:908649.
    Crossref | PubMed
  53. Murphy MS, Tayade C, Smith GN. Evidence of inflammation and predisposition toward metabolic syndrome after pre–eclampsia. Pregnancy Hypertens 2015;5:354–8.
    Crossref | PubMed
  54. Ehrenthal DB, Rogers S, Goldstein ND, et al. Cardiovascular risk factors one year after a hypertensive disorder of pregnancy. J Womens Health (Larchmt) 2015;24:23-9.
    Crossref | PubMed
  55. van Rijn BB, Bruinse HW, Veerbeek JH, et al. Postpartum circulating markers of inflammation and the systemic acute-phase response after early-onset preeclampsia. Hypertension 2016;67:404–14.
    Crossref | PubMed
  56. Girouard J, Giguère Y, Moutquin JM, Forest JC. Previous hypertensive disease of pregnancy is associated with alterations of markers of insulin resistance. Hypertension 2007;49:1056–62.
    Crossref | PubMed
  57. Freeman DJ, McManus F, Brown EA, et al. Short- and long-term changes in plasma inflammatory markers associated with preeclampsia. Hypertension 2004;44:708–14.
    Crossref | PubMed
  58. Wu F, Zhou J, Zheng H, Liu G. Decreased heart rate recovery in women with a history of pre-eclampsia. Pregnancy Hypertens 2018;13:25-9.
    Crossref | PubMed
  59. Akhter T, Wikström AK, Larsson M, et al. Serum Pentraxin 3 is associated with signs of arterial alteration in women with preeclampsia. Int J Cardiol 2017;241:417–22.
    Crossref | PubMed
  60. Bokslag A, Teunissen PW, Franssen C, et al. Effect of early-onset preeclampsia on cardiovascular risk in the fifth decade of life. Am J Obstet Gynecol 2017;216:523.e1–.e7.
    Crossref | PubMed
  61. Alma LJ, Bokslag A, Maas A, et al. Shared biomarkers between female diastolic heart failure and pre-eclampsia: a systematic review and meta-analysis. ESC Heart Fail 2017;4:88–98.
    Crossref | PubMed
  62. Muijsers HEC, Westermann D, Birukov A, et al. High-sensitivity cardiac troponin I in women with a history of early-onset preeclampsia. J Hypertens 2020;38:1948–54.
    Crossref | PubMed
  63. Sugulle M, Herse F, Hering L, et al. Cardiovascular biomarker midregional proatrial natriuretic peptide during and after preeclamptic pregnancies. Hypertension 2012;59:395–401.
    Crossref | PubMed
  64. Portelinha A, Cerdeira AS, Belo L, et al. Haemostatic factors in women with history of preeclampsia. Thromb Res 2009;124:52–6.
    Crossref | PubMed
  65. Vickers M, Ford I, Morrison R, et al. Markers of endothelial activation and atherothrombosis in women with history of preeclampsia or gestational Hypertension. Thromb Haemost 2003;90:1192–7.
    Crossref | PubMed
  66. Hromadnikova I, Kotlabova K, Dvorakova L, Krofta L. Maternal cardiovascular risk assessment 3-to-11 years postpartum in relation to previous occurrence of pregnancy-related complications. J Clin Med 2019;8.
    Crossref | PubMed
  67. Gaugler-Senden IP, Berends AL, de Groot CJ, Steegers EA. Severe, very early onset preeclampsia: subsequent pregnancies and future parental cardiovascular health. Eur J Obstet Gynecol Reprod Biol 2008;140:171–7.
    Crossref | PubMed
  68. White WM, Turner ST, Bailey KR, et al. Hypertension in pregnancy is associated with elevated homocysteine levels later in life. Am J Obstet Gynecol 2013;209:454.e1–7.
    Crossref | PubMed
  69. Visser S, Hermes W, Blom HJ, et al. homocysteinemia after hypertensive pregnancy disorders at term. J Womens Health (Larchmt) 2015;24:524–9.
    Crossref | PubMed
  70. Wu F, Yang H, Liu B. Association between homocysteine and arterial stiffness in women with a history of preeclampsia. J Vasc Res 2019;56:152–9.
    Crossref | PubMed
  71. Lampinen KH, Rönnback M, Groop PH, et al. Increased plasma norepinephrine levels in previously pre-eclamptic women J Hum Hypertens 2014;28:269–73.
    Crossref | PubMed
  72. Dayan N, Schlosser K, Stewart DJ, et al. Circulating MicroRNAs implicate multiple atherogenic abnormalities in the long-term cardiovascular sequelae of preeclampsia. Am J Hypertens 2018;31:1093–7.
    Crossref | PubMed
  73. Hromadnikova I, Kotlabova K, Dvorakova L, Krofta L. Postpartum profiling of microRNAs involved in pathogenesis of cardiovascular/cerebrovascular diseases in women exposed to pregnancy-related complications. Int J Cardiol 2019;291:158–67.
    Crossref | PubMed
  74. Mohseni Z, Spaanderman MEA, Oben J, et al. Cardiac remodeling and pre-eclampsia: an overview of microRNA expression patterns. Ultrasound Obstet Gynecol 2018;52:310–7.
    Crossref | PubMed
  75. Schlosser K, Kaur A, Dayan N, et al. Circulating miR-206 and Wnt-signaling are associated with cardiovascular complications and a history of preeclampsia in women. Clin Sci (Lond) 2020;134:87–101.
    Crossref | PubMed
  76. Murphy MS, Casselman RC, Tayade C, Smith GN. Differential expression of plasma microRNA in preeclamptic patients at delivery and 1 year postpartum. Am J Obstet Gynecol 2015;213:367.e1–9.
    Crossref | PubMed
  77. Zoet GA, van Rijn BB, Rehfeldt M, et al. Similar pro-NT and pro-RLX2 levels after preeclampsia and after uncomplicated pregnancy. Maturitas 2017;106:87–91.
    Crossref | PubMed
  78. Meeuwsen JAL, de Vries J, Zoet GA, et al. Circulating neutrophils do not predict subclinical coronary artery disease in women with former preeclampsia. Cells 2020;9.
    Crossref | PubMed
  79. Shahul S, Ramadan H, Nizamuddin J, et al. Activin A and late postpartum cardiac dysfunction among women with hypertensive disorders of pregnancy. Hypertension 2018;72:188–93.
    Crossref | PubMed
  80. Jacobsen DP, Lekva T, Moe K, et al. Pregnancy and postpartum levels of circulating maternal sHLA-G in preeclampsia. J Reprod Immunol 2021;143:103249.
    Crossref | PubMed
  81. Leaños-Miranda A, Campos-Galicia I, Isordia-Salas I, et al. Changes in circulating concentrations of soluble fms-like tyrosine kinase-1 and placental growth factor measured by automated electrochemiluminescence immunoassays methods are predictors of preeclampsia. J Hypertens 2012;30:2173–81.
    Crossref | PubMed
  82. Levine RJ, Maynard SE, Qian C, et al. Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 2004;350:672–83.
    Crossref | PubMed
  83. Lapaire O, Shennan A, Stepan H. The preeclampsia biomarkers soluble fms-like tyrosine kinase-1 and placental growth factor: current knowledge, clinical implications and future application. Eur J Obstet Gynecol Reprod Biol 2010;151:122–9.
    Crossref | PubMed
  84. Lam C, Lim KH, Karumanchi SA. Circulating angiogenic factors in the pathogenesis and prediction of preeclampsia. Hypertension 2005;46:1077–85.
    Crossref | PubMed
  85. Onoue K, Uemura S, Takeda Y, et al. Usefulness of soluble Fms-like tyrosine kinase-1 as a biomarker of acute severe heart failure in patients with acute myocardial infarction Am J Cardiol 2009;104:1478–83.
    Crossref | PubMed
  86. Kameda R, Yamaoka-Tojo M, Makino A, et al. Soluble Fms-like tyrosine kinase 1 is a novel predictor of brain natriuretic peptide elevation. Int Heart J 2013;54:133–9.
    Crossref | PubMed
  87. Ky B, French B, Ruparel K, et al. The vascular marker soluble fms-like tyrosine kinase 1 is associated with disease severity and adverse outcomes in chronic heart failure. J Am Coll Cardiol 2011;58:386–94.
    Crossref | PubMed
  88. Hammadah M, Georgiopoulou VV, Kalogeropoulos AP, et al. elevated soluble fms-like tyrosine kinase-1 and placental-like growth factor levels are associated with development and mortality risk in heart failure. Circ Heart Fail 2016;9:e002115.
    Crossref | PubMed
  89. Doyle B, Caplice N. Plaque neovascularization and antiangiogenic therapy for atherosclerosis. J Am Coll Cardiol 2007;49:2073–80.
    Crossref | PubMed
  90. Khurana R, Moons L, Shafi S, et al. Placental growth factor promotes atherosclerotic intimal thickening and macrophage accumulation. Circulation 2005;111:2828–36.
    Crossref | PubMed
  91. Cassidy A, Chiuve SE, Manson JE, et al. Potential role for plasma placental growth factor in predicting coronary heart disease risk in women. Arterioscler Thromb Vasc Biol 2009;29:134–9.
    Crossref | PubMed
  92. Draker N, Torry DS, Torry RJ. Placenta growth factor and sFlt-1 as biomarkers in ischemic heart disease and heart failure: a review. Biomark Med 2019;13:785–99.
    Crossref | PubMed
  93. Matsumoto T, Uemura S, Takeda Y, et al. An elevated ratio of placental growth factor to soluble fms-like tyrosine kinase-1 predicts adverse outcomes in patients with stable coronary artery disease. Intern Med 2013;52:1019–27.
    Crossref | PubMed
  94. Lau SY, Guild SJ, Barrett CJ, et al. Tumor necrosis factor-alpha, interleukin-6, and interleukin-10 levels are altered in preeclampsia: a systematic review and meta-analysis. Am J Reprod Immunol 2013;70:412–27.
    Crossref | PubMed
  95. Xie C, Yao MZ, Liu JB, Xiong LK. A meta-analysis of tumor necrosis factor-alpha, interleukin-6, and interleukin-10 in preeclampsia. Cytokine 2011;56:550–9.
    Crossref | PubMed
  96. Blake GJ, Ridker PM. Inflammatory bio-markers and cardiovascular risk prediction. J Intern Med 2002;252:283–94.
    Crossref | PubMed
  97. Liberale L, Montecucco F, Schwarz L, et al. Inflammation and cardiovascular diseases: lessons from seminal clinical trials. Cardiovasc Res 2021;117:411–22.
    Crossref | PubMed
  98. Tzoulaki I, Murray GD, Lee AJ, et al. C-reactive protein, interleukin-6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population: Edinburgh Artery Study. Circulation 2005;112:976–83.
    Crossref | PubMed
  99. Ross R. Atherosclerosis--an inflammatory disease. N Engl J Med. 1999;340:115–26.
    Crossref | PubMed
  100. Zakynthinos E, Pappa N. Inflammatory biomarkers in coronary artery disease. J Cardiol 2009;53:317–33.
    Crossref | PubMed
  101. de Lemos JA. Increasingly sensitive assays for cardiac troponins: a review. JAMA 2013;309:2262–9.
    Crossref | PubMed
  102. Neumann JT, Twerenbold R, Ojeda F, et al. Application of high-sensitivity troponin in suspected myocardial infarction. N Engl J Med. 2019;380:2529–40.
    Crossref | PubMed
  103. McKie PM, AbouEzzeddine OF, Scott CG, et al. High-sensitivity troponin I and amino-terminal pro--B-type natriuretic peptide predict heart failure and mortality in the general population. Clin Chem 2014;60:1225–33.
    Crossref | PubMed
  104. Zeller T, Tunstall-Pedoe H, Saarela O, et al. High population prevalence of cardiac troponin I measured by a high-sensitivity assay and cardiovascular risk estimation: the MORGAM Biomarker Project Scottish Cohort. Eur Heart J 2014;35:271–81.
    Crossref | PubMed
  105. Aeschbacher S, Schoen T, Bossard M, et al. Relationship between high-sensitivity cardiac troponin I and blood pressure among young and healthy adults. Am J Hypertens 2015;28:789–96.
    Crossref | PubMed
  106. McKie PM, Heublein DM, Scott CG, et al. Defining high-sensitivity cardiac troponin concentrations in the community. Clin Chem 2013;59:1099–107.
    Crossref | PubMed
  107. Sadlecki P, Grabiec M, Walentowicz-Sadlecka M. Prenatal clinical assessment of NT-proBNP as a diagnostic tool for preeclampsia, gestational hypertension and gestational diabetes mellitus. PLoS One 2016;11:e0162957.
    Crossref | PubMed
  108. Paulus WJ, Tschöpe C, Sanderson JE, et al. How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur Heart J 2007;28:2539–50.
    Crossref | PubMed
  109. Nadar SK, Shaikh MM. Biomarkers in routine heart failure clinical care. Card Fail Rev 2019;5:50–6.
    Crossref | PubMed
  110. Goletti S, Gruson D. Personalized risk assessment of heart failure patients: more perspectives from transforming growth factor super-family members. Clin Chim Acta 2015;443:94–9.
    Crossref | PubMed
  111. Yndestad A, Ueland T, Øie E, et al. Elevated levels of activin A in heart failure: potential role in myocardial remodeling. Circulation 2004;109:1379–85.
    Crossref | PubMed
  112. Hu J, Wang X, Wei SM, et al. Activin A stimulates the proliferation and differentiation of cardiac fibroblasts via the ERK1/2 and p38-MAPK pathways. Eur J Pharmacol 2016;789:319–27.
    Crossref | PubMed
  113. Fournel S, Aguerre-Girr M, Huc X, et al. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J Immunol 2000;164:6100–4.
    Crossref | PubMed
  114. Lila N, Rouas-Freiss N, Dausset J, et al. Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism. Proc Natl Acad Sci USA. 2001;98:12150–5.
    Crossref | PubMed
  115. Almasood A, Sheshgiri R, Joseph JM, et al. Human leukocyte antigen-G is upregulated in heart failure patients: a potential novel biomarker. Hum Immunol 2011;72:1064–7.
    Crossref | PubMed
  116. Olesen LL, Hviid TV. Upregulation of soluble HLA-G in chronic left ventricular systolic dysfunction. J Immunol Res 2016;2016:8417190.
    Crossref | PubMed
  117. Bonaca MP, Scirica BM, Sabatine MS, et al. Prospective evaluation of pregnancy-associated plasma protein-a and outcomes in patients with acute coronary syndromes. J Am Coll Cardiol 2012;60:332–8.
    Crossref | PubMed
  118. Iversen KK, Teisner B, Winkel P, et al. Pregnancy associated plasma protein-A as a marker for myocardial infarction and death in patients with stable coronary artery disease: a prognostic study within the CLARICOR Trial. Atherosclerosis 2011;214:203–8.
    Crossref | PubMed
  119. Bayes-Genis A, Conover CA, Overgaard MT, et al. Pregnancy-associated plasma protein A as a marker of acute coronary syndromes. N Engl J Med 2001;345:1022–9.
    Crossref | PubMed
  120. Pauletto P, Scannapieco G, Pessina AC. Sympathetic drive and vascular damage in hypertension and atherosclerosis. Hypertension 1991;17(4 Suppl):Iii75–81.
    Crossref | PubMed
  121. Mancia G, Bousquet P, Elghozi JL, et al. The sympathetic nervous system and the metabolic syndrome. J Hypertens 2007;25:909–20.
    Crossref | PubMed
  122. Al-Sharea A, Lee MKS, Whillas A, et al. Chronic sympathetic driven hypertension promotes atherosclerosis by enhancing hematopoiesis. Haematologica 2019;104:456–67.
    Crossref | PubMed