Article Type: Clinical Article

Routine blood tests during pregnancy for predicting future increases in risk of
Accepted Article
cardiovascular morbidity 

Shira Yuval Bar-Asher 1,a, Alexander Shefer 2,a, Ilana Shoham-Vardi 3, Ruslan

Sergienko 3, Arik Wolak 1,4, Eyal Sheiner 5, Talya Wolak 1,6,*

[Note to typesetter: First names have been highlighted in green and last names

are highlighted in red]

1. Faculty of Health Sciences, Joyce & Irving Goldman Medical School at Ben-

Gurion University of the Negev, Beer-Sheva, Israel

2. Internal Medicine Department H, Soroka University Medical Center, Faculty of

Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

3. Department of Public Health, Faculty of Health Sciences, Ben-Gurion

University of the Negev, Beer-Sheva, Israel

4. Cardiology Department, Shaare Zedek Medical Center, Jerusalem, Israel.

5. Department of Obstetrics and Gynecology, Soroka University Medical Center,

Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

6. Division of Internal Medicine, Shaare Zedek Medical Center, Jerusalem, Israel

a
These authors contributed equally to the present study.

This article has been accepted for publication and undergone full peer review but has not
been through the copyediting, typesetting, pagination and proofreading process, which may
lead to differences between this version and the Version of Record. Please cite this article as
doi: 10.1002/ijgo.12592
This article is protected by copyright. All rights reserved.
 *
Correspondence: Talya Wolak

Division of Internal Medicine, Shaare Zedek Medical Center, Shmuel Byate 12

Accepted Article
Jerusalem 9103102, Israel

E-mail address: twolak@bgu.ac.il

 The present study was at the 28th European Meeting on Hypertension and

Cardiovascular Protection; June 8–11, 2018; Barcelona, Spain

Keywords: Cardiovascular disease; Creatinine; Potassium; Pregnancy; Urea; Uric

acid

Synopsis: Routine blood tests for creatinine, potassium, and urea predicted future

cardiovascular morbidity among pregnant women with no overt gestational

anomalies.

Abstract

Objective: To examine the association between routine blood tests during

pregnancy and future risk of cardiovascular morbidity.

Methods: The present case–control study was conducted among women who

delivered at a teaching hospital in Israel between January 1, 2000, and December

31, 2012. The cohort comprised women who were subsequently hospitalized owing

to cardiovascular morbidity (case group) and age-matched non-hospitalized women

(control group). Blood levels of creatinine, glucose, potassium, urea, and uric acid

were measured during pregnancy. Only women with at least one test result available

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 for all five measurements were included. The relationship between upper quartile

blood test values and cardiovascular hospitalization was assessed.

Accepted Article
Results: The study included 4115 women (212 in the case group and 3903 in the

control group). Three measures were associated with a future risk of cardiovascular

morbidity requiring hospitalization: creatinine (hazard ratio [HR] 1.86, 95%

confidence interval [CI] 1.37–2.53; P<0.001); potassium (HR 1.48, 95% CI 1.09–

2.01; P=0.013), and urea (HR 1.60, 95% CI 1.17–2.19; P=0.003). The number of

blood test results in the upper quartile also increased such risk. The HRs for two

tests and at least three tests were 1.65 (95% CI 1.06–2.56; P=0.026) and 3.32 (95%

CI 2.19–5.04; P<0.001), respectively.

Conclusions: Future cardiovascular morbidity was predicted by routine blood tests

during pregnancy.

1 INTRODUCTION

Various physiologic changes occur in the cardiovascular system during pregnancy

[1], including increases in blood volume, cardiac output, and glomerular filtration rate

(GFR) [2]. Therefore, pregnancy can be considered as a physiological stress test.

Determining how the body copes with such changes could aid prediction of future

maternal health.

Overt adverse events of pregnancy (e.g. gestational diabetes mellitus and pre-

eclampsia) can develop in response to cardiovascular and renal maladaptation [3].

Women who experience such morbidities during pregnancy are also at increased

risk of future atherosclerotic-related morbidity [4,5]. Further, subclinical conditions

such as gestational hypertension [6] and mild glucose intolerance [7] are indicators

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 of future cardiovascular morbidity. Acknowledging this relationship, the 2011

American Heart Association guidelines recommend that a detailed pregnancy history

Accepted Article
should be obtained from all women as part of their cardiovascular risk assessment

[8].

The physiologic changes of pregnancy can be identified by alterations in routine

blood test results. For example, the rise in GFR leads to decreased serum levels of

creatinine, urea, and uric acid [2]. Associations between elevated blood levels of uric

acid [9], urea [10], and creatinine [10] during uncomplicated pregnancy and future

maternal atherosclerotic morbidity have been demonstrated previously.

Consequently, abnormally high blood test results could provide an early marker for

cardiovascular and renal maladaptation during pregnancy, thus identifying maternal

risk of future cardiovascular morbidity.

The aim of the present study was to determine whether five blood tests that are

routinely conducted during pregnancy could predict subsequent cardiovascular

morbidity requiring hospitalization.

2 MATERIALS AND METHODS

The present case–control study was conducted among women who delivered at the

Soroka University Medical Center (SUMC), Beer-Sheva, Israel, between January 1,

2000, and December 31, 2012. The present study was approved by the ethics

committee of SUMC (0343-15-SOR). Informed consent was not required as the

analysis involved the retrospective review of electronic medical files (>100 000

deliveries). The identifying number of each patient was encrypted to maintain

anonymity.

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 The present study center is a 1000-bed tertiary teaching hospital serving a

population larger than 800 000.

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Inclusion criteria for the case group were delivery at SUMC and subsequent

hospitalization during the non-pregnant period, with at least one of the following

diagnoses recorded in patient medical files: cardiovascular disease; cerebrovascular

disease; chronic renal failure; and complicated diabetes mellitus and hypertension

(including diabetes mellitus and hypertension with target organ damage, and/or

acute adverse events such as diabetic ketoacidosis, hyperosmolar state, and

hypertensive crisis). Subtypes of cardiovascular morbidity were derived using the

relevant International Classification of Diseases, 9th edition codes (Table S1).

Inclusion criteria for the control group were delivery at SUMC and no atherosclerotic-

related hospitalizations during the non-pregnant period. Patients were identified for

inclusion in the control group from among women who were not hospitalized; those

who had delivered on the same dates as patients included in the case group and

who were the same age (year of birth) were included in the control group.

The exclusion criteria for both groups were multiple pregnancy and known

cardiovascular disease, renal failure, or cardiovascular risk factors (diabetes mellitus,

hypertension, and hyperlipidemia) before the first pregnancy.

Blood levels of creatinine, glucose, potassium, urea, and uric acid were measured

during pregnancy. Only women with at least one test result available for all five

measurements were included in the present study. The highest measurement

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 recorded for each test during any one pregnancy was identified for each woman. The

upper quartile was then selected for each measure: creatinine (>0.06mmol/L);
Accepted Article
glucose (>7.2 mmol/L); potassium (>4.4 mmol/L); urea (>3.8 mmol/L); and uric acid

(>0.285 mmol/L).

The existence of a comprehensive computerized database at SUMC, coupled with

the unique structure of the local health service, allowed for full availability of follow-

up data. Follow-up data for patients in the case group was until hospitalization

occurred, whereas for the control group it was until the end of the present study

period. The minimum period of follow-up for the case group between delivery and

hospitalization was at least 1 year after the last pregnancy.

The data were analyzed using SPSS version 24 (IBM, Armonk, NY, USA). Qualitative

variables were assessed using the χ2 test. Continuous variables were assessed

using one-way analysis of variance. Logistic regression analysis using Cox

regression was performed to evaluate the relationship between cardiovascular-

related hospitalization and upper quartile blood test results during pregnancy. Known

gestational risk factors for cardiovascular morbidity (maternal age, parity,

hypertensive disorders of pregnancy, gestational diabetes mellitus, preterm delivery,

and small for gestational age [SGA]) were included in two regression analyses to

confirm that the blood tests results remained linked to cardiovascular morbidity even

after adjusting for these factors. P<0.05 was considered to be statistically significant.

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 3 RESULTS

A total of 169 059 deliveries were recorded at SUMC during the present study period
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(Figure 1). In all, 4115 women met both the inclusion and exclusion criteria, 212 in

the case group (hospitalized) and 3903 in the control group (non-hospitalized).

The characteristics of the present study population are shown in Table 1. Statistically

significant between-group differences were found for parity, hypertensive disorders of

pregnancy, gestational diabetes mellitus, and delivery before 37 weeks.

Table 2 outlines the results for the five blood tests conducted during pregnancy.

Statistically significant between-group differences were found for all of these tests,

both in terms of the upper quartile values and the mean concentrations.

The Cox regression analysis of the relationship between upper quartile blood test

values and cardiovascular-related hospitalization is shown in Table 3. Three of the

five blood tests showed a relationship with hospitalization: creatinine (hazard ratio

[HR] 1.86, 95% confidence interval [CI] 1.37–2.53; P<0.001); potassium (HR 1.48,

95% CI 1.09–2.01; P=0.013); and urea (HR 1.60, 95% CI 1.17–2.19; P=0.003).

Hypertensive disorders of pregnancy, preterm delivery, and parity were also

associated with increased risk of hospitalization.

Table 4 shows the Cox regression analysis of the relationship between the number of

upper quartile values recorded and cardiovascular-related hospitalization. Any two

tests with values in the upper quartile had an HR of 1.65 (95% CI 1.06–2.56;

P=0.026). Any three or more tests with values in the upper quartile had an HR of

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 3.32 (95% CI 2.19–5.04; P<0.001). As before, hypertensive disorders of pregnancy,

preterm delivery, and parity were also associated with increased risk of
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hospitalization.

4 DISCUSSION

The present study demonstrated that women hospitalized with cardiovascular

morbidity after pregnancy had high upper quartile values recorded in their medical

files for each of five routine blood tests (creatinine, glucose, potassium, urea, and

uric acid) conducted during pregnancy. The upper quartile values for creatinine,

potassium, and urea were found to be associated with cardiovascular morbidity, both

independently of each other and when controlled for known gestational

complications (hypertensive disorders of pregnancy, gestational diabetes mellitus,

preterm delivery, and SGA). The risk of cardiovascular morbidity increased as the

number of test results in the upper quartile increased.

The current findings should be considered in light of the physiologic alterations

known to occur during pregnancy. The rise in GFR leads to decreased serum levels

of creatinine, urea, and uric acid [2]. By contrast, metabolism of potassium during

pregnancy is complicated and influenced by several factors [11]. For example, an

increase in aldosterone levels causes potassium excretion, whereas progesterone

acts as mineralocorticoid-receptor antagonist; consequently, the normal range for

plasma levels of potassium remains to be defined. High potassium levels during

pregnancy are associated with an increased risk of developing both gestational

diabetes mellitus and severe pre-eclampsia [12]. Therefore, it seems reasonable to

conclude that the high levels of creatinine, glucose, potassium, urea, and uric acid

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 found in the present study during pregnancy might indicate a subclinical anomaly

that could lead to overt cardiovascular morbidity later in life.

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Adverse events of pregnancy such as pregnancy-induced hypertension and

gestational diabetes mellitus have long been considered as potential risk factors for

future cardiovascular disease [5,13]. Indeed, pregnancy serves as a stress test that

is characterized by cardiometabolic and renal overload. Women who had

experienced pregnancy-induced hypertension were found to exhibit an increased

incidence of obesity, metabolic syndrome, and hypertension; early onset of

hypertension; high estimated vascular age; and low estimated GFR [14], underlining

the importance of pregnancy-induced hypertension as a marker of future

atherosclerotic morbidity. In another study, Cain et al. [15] found that maternal

placental syndromes (i.e. pre-eclampsia, placental infarction, and abruption) were

associated with short-term cardiovascular disease. The results of the present study

support this concept. Renal adaptation anomalies during pregnancy manifested as

high levels of creatinine, potassium, and urea. The factors, together with pregnancy-

induced hypertension, were independently associated with an increased incidence of

future hospitalization owing to cardiovascular morbidity.

Cardiovascular disease is the leading cause of death among women; furthermore,

although myocardial infarction it is less prevalent among women than men, women

have a higher mortality rate after myocardial infarction [16]. This difference partly

reflects the increased age of women at presentation, as well as the high rate of

adverse events that occur after myocardial infarction such as bleeding following

intervention and heart failure [17]. In addition, the diagnosis and treatment of

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 ischemic heart disease among women is often delayed [18]. One of the reasons for

such delay is the fact that ischemic heart disease without coronary artery obstruction
Accepted Article
is more prevalent among women than men [19]. Diagnosis and treatment of non-

obstructive coronary artery disease can be challenging because it is not apparent on

angiography and so the benefits of revascularization are reduced accordingly. Thus,

although women with ischemic heart disease have lower pretest clinical scores,

lower rates of previous myocardial infarction, and less angiographic coronary

obstruction when compared with men, they are at increased risk of poor

cardiovascular outcomes [20].

For these reasons, it is essential to identify in advance the subgroup of women that

are at high risk of future cardiovascular disease [13]. However, the standard risk

prediction methods currently in use such as exercise tests are less effective for

women than for men [21]. Women with cardiovascular risk factors are also less likely

than men to be told about their risk profile and potential risk-modification strategies

[22]. As a result, women have low access to preventive cardiac care before

experiencing myocardial infarction [23]. They also tend to have a longer period of

symptoms than men do before seeking medical help when having a myocardial

infarction [24]. Consequently, it is essential that specific tools are developed to

identify women in the high cardiovascular risk group. According to clinical guidelines

[8], pregnancy adverse event history is mandatory when evaluating cardiovascular

risk among women with suspected cardiovascular disease. Pregnancy provides a

window of opportunity to detect women who are at increased risk of future

atherosclerotic-related morbidity. Pregnancy-induced hypertension and gestational

diabetes mellitus probably reflect severe vascular and metabolic anomaly that could

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 become permanent [25]. Therefore, identifying a laboratory marker of such

subclinical injury could aid detection of high-risk women at a reversible stage.

Accepted Article
The present study had some limitations, mostly owing to the retrospective design.

For example, the possibility existed that women were hospitalized for cardiovascular

morbidity at a center other than SUMC. However, this outcome could have occurred

in both groups in an equal manner. The information held in the SUMC database

about family history, smoking status, and obesity were insufficient and so these

variables were not included in the current analysis. Future studies should therefore

evaluate these socioeconomic and demographic characteristics. Another limitation

was the potential for selection bias as not all five blood tests were performed among

all pregnant women.

To the best of our knowledge, the present study was the first to demonstrate an

association between future cardiovascular morbidity and routine blood test results

during pregnancy. Additional studies are now required to validate this relationship

and to develop a score that predicts cardiovascular morbidity risk. Simple blood tests

conducted during pregnancy could identify future cardiovascular morbidity among

women with no overt clinical gestational morbidity. Moreover, such findings could

help to prevent future morbidity by changing lifestyles and raising awareness of risk.

Author contributions

SYB-A contributed to data collection and writing the manuscript. AS contributed to

the design of the study and writing the manuscript. IS-V contributed to the design of

the study, the interpretation of data, and revising the manuscript. RS contributed to

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 the design of the study, data collection and analysis, and writing the manuscript. AW

contributed to the conception and design of the study, and revising the manuscript.
Accepted Article
ES contributed to the design of the study, the interpretation of data, and revising the

manuscript. TW was the principal investigator and contributed to the design of the

study, data collection, and writing and revising the manuscript.

Conflicts of interest

The authors have no conflicts of interest.

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Figure 1 Flow chart of the present study cohort. Abbreviation: SUMC, Soroka

University Medical Center.

Table S1 Cardiovascular morbidity stratified into three groups on the basis of the

International Classification of Diseases, 9th edition codes.

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 Table 1 Characteristics of the study population. a

Characteristic Case group (n=212) Control group (n=3903) P value b

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Age at the end of the last pregnancy c 34.9 ± 5.3 34.5 ± 6.0 0.395
Parity 5.0 (1.0–14.0) 3.0 (1.0–18.0) <0.001
Hypertensive disorders of pregnancy 87 (41.0) 865 (22.2) <0.001
Gestational diabetes mellitus 72 (34.0) 837 (21.4) <0.001
Small for gestational age 30 (14.2) 571 (14.6) 0.848
Preterm delivery (<37 wk) 96 (45.3) 1209 (31.0) <0.001

a
Values are given as mean±SD, median (range), or number (percentage), unless indicated otherwise.
b
χ2 test and one-way ANOVA; P<0.05 was considered significant.
c
Data on age was missing for 41 women in the control group.

Table 2 Comparison of blood test results. a

Measure Case group Control group OR (95% CI) b P value c

(n=212) (n=3903)
Potassium, mmol/L
>4.4 d 85 (40.1) 933 (23.9) 2.13 (1.60–2.83) <0.001
Mean ± SD 4.4 ± 0.6 4.2 ± 0.4 <0.001
Uric acid, mmol/L
>0.285 d 73 (34.4) 894 (22.9) 1.77 (1.32–2.37) <0.001
Mean ± SD 4.6 ± 1.6 4.1 ± 1.3 <0.001
Creatinine, mmol/L
>0.06 d 93 (43.9) 901 (23.1) 2.60 (1.97–3.45) <0.001
Mean ± SD 0.7 ± 0.3 0.6 ± 0.2 <0.001
Urea, mmol/L
>3.8 d 87 (41.0) 897 (23.0) 2.33 (1.76–3.10) <0.001
Mean ± SD 23.7 ± 10.4 19.6 ± 6.2 <0.001
Glucose, mmol/L
>7.2 d 77 (36.3) 938 (24.0) 1.80 (1.35–2.41) <0.001
Mean ± SD 137.3 ± 41.9 113.1 ± 68.0 <0.001

Abbreviations: CI, confidence interval; OR, odds ratio.

a
Values given as number (percentage), unless indicated otherwise.
b
Mantel–Haenszel common odds ratio estimate.
c 2
χ test; P<0.05 was considered significant.
d
Stated values represent the upper quartile.

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 Table 3 Logistic regression analysis of the relationship between upper quartile blood test results and
subsequent hospitalization.
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Variable HR (95% CI) a Adjusted P value b
Potassium >4.4 mmol/L 1.48 (1.09–2.01) 0.013
Uric Acid >0.285 mmol/L 1.03 (0.74–1.43) 0.854
Creatinine >0.06 mmol/L 1.86 (1.37–2.53) <0.001
Urea >3.8 mmol/L 1.60 (1.17–2.19) 0.003
Glucose >7.2 mmol/L 1.25 (0.90–1.73) 0.173
Hypertensive disorders of pregnancy 1.83 (1.34–2.50) <0.001
Gestational diabetes mellitus 1.25 (0.88–1.77) 0.212
Small for gestational age 0.73 (0.48–1.11) 0.136
Preterm delivery (<37 wk) 1.46 (1.08–1.96) 0.013
Parity 1.07 (1.01–1.12) 0.012
Age at the end of the last pregnancy 0.97 (0.95–1.00) 0.056

Abbreviations: CI, confidence interval; HR, hazard ratio.

a
Logistic regression backward stepwise (conditional).
b
P<0.05 was considered significant.

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 Table 4 Logistic regression analysis of the relationship between the number of upper quartile blood
test results and subsequent hospitalization.
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Variable HR (95% CI) a Adjusted P
value b
No. of blood test results in the upper quartile
0 1.00 NA
1 1.10 (0.72–1.68) 0.663
2 1.65 (1.06–2.56) 0.026
3–5 3.32 (2.19–5.04) <0.001
Hypertensive disorders of pregnancy 1.75 (1.29–2.38) <0.001
Gestational diabetes mellitus 1.25 (0.90–1.74) 0.192
Small for gestational age 0.72 (0.48–1.09) 0.128
Preterm delivery (<37 wk) 1.49 (1.11–1.99) 0.008
Parity 1.06 (1.01–1.12) 0.014
Age at the end of the last pregnancy 0.98 (0.95–1.00) 0.072

Abbreviations: CI, confidence interval; HR, hazard ratio; NA, not applicable.
a
Logistic Regression backward stepwise (conditional).
b
P<0.05 was considered statistically significant.

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