Pregnancy Hypertension: An International Journal of Women’s Cardiovascular Health 5 (2015) 303–307

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Pregnancy Hypertension: An International Journal of

Women’s Cardiovascular Health
journal homepage: www.elsevier.com/locate/preghy

Microalbuminuria is a predictor of adverse pregnancy outcomes

including preeclampsia
M. Jayaballa a,⇑, S. Sood b, I. Alahakoon a, S. Padmanabhan a, N.W. Cheung a, V. Lee a,b
a
Westmead Hospital, Sydney, NSW, Australia
b
Sydney Medical School, University of Sydney, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: Abnormal urinary protein loss is a marker associated with a diverse range of renal diseases
Received 30 April 2015 including preeclampsia. Current measures of urine protein used in the diagnostic criteria for the diagno-
Accepted 11 August 2015 sis of preeclampsia includes urine protein:creatinine ratio and 24-h urine protein. However very little is
Available online 13 August 2015
known about the value of urine albumin:creatinine ratio (uACR) in pregnancy. In this study we examined
the prognostic value of microalbuminuria detected antepartum to predict adverse pregnancy outcomes.
Keywords: Design: This is a single-centre retrospective analysis of 84 pregnant women over the age of 16 attending a
Albumin:creatinine ratio
tertiary ‘high-risk’ pregnancy outpatient clinic between July 2010 and June 2013. Utilising medical
Preeclampsia
Proteinuria
records, antepartum peak uACR level and pregnancy maternal and fetal outcomes were recorded.
Microalbuminuria Findings: The primary outcome was a composite of poor maternal and fetal outcomes including
Pregnancy preeclampsia, maternal death, eclampsia, stillbirth, neonatal death, IUGR, premature delivery and placen-
tal abruption. As the antepartum peak uACR level (in mg/mmol) increased from normoalbuminuria
(uACR < 3.5) to microalbuminuria (uACR 3.5–35) to macroalbuminuria (>35), the percentage of women
with the primary composite outcome increased in a stepwise fashion (13.8% to 24.1% to 62.1%
respectively, p < 0.001). After adjusting for covariates including history of hypertension, chronic kidney
disease and aspirin therapy during pregnancy, micro- and macroalbuminuria remained significant
predictors of the primary outcome.
Conclusions: We have shown that antepartum peak uACR is a useful simple marker to help predict
adverse maternal and fetal outcomes. Further studies are required to utilise uACR as a prognostic tool
in pregnancy before it can be applied in clinical practice.
Ó 2015 International Society for the Study of Hypertension in Pregnancy. Published by Elsevier B.V. All
rights reserved.

1. Introduction
Abnormal urinary protein loss is a marker associated with a
diverse range of renal diseases, including diabetes, glomeru-
lonephritis and preeclampsia. Established markers of protein loss
in pregnancy include positive protein testing on urinalysis and high
(>300 mg) 24 h protein excretion [1]. Uncertainty remains regard-
ing the best method of estimating abnormal urinary protein losses
in pregnancy, with the 24 h urine protein measurement used as
the gold standard at present. However there are limitations with
the 24 h urine protein measurement including incorrect evaluation
due to under- and over-collection of urine, and the cumbersome
nature of collection, especially during pregnancy. Therefore, other
methods of measuring urinary protein, including dipstick urinalysis,
urine protein-to-creatinine ratio (uPCR) (laboratory and bedside)
⇑ Corresponding author.
E-mail address: mjayaballa@gmail.com (M. Jayaballa).
and urine albumin- to- creatinine ratio (uACR) have been employed.
The dipstick test for proteinuria is easy to perform and is semi
quantitative in nature, but suffers from lack of both sensitivity
and specificity. The uPCR has been used in more recent years, how-
ever a number of systematic reviews [2–4] have shown that as a
diagnostic test, it lacks accuracy compared to the ‘‘gold standard”
24 h urine protein measurement. Despite this the uPCR is currently
part of the diagnostic criteria for the diagnosis of preeclampsia [1].
On the other hand, very little is known about the value of uACR
in pregnancy. Current guidelines use uACR in conjunction with
estimated glomerular filtration rate (eGFR) to stage chronic kidney
disease [5]. The uACR is a well-validated tool in the diagnosis and
prognosis of kidney disease outside of pregnancy. There is a scar-
city of studies that looked at the utility of uACR in predicting
adverse pregnancy outcomes in patients especially those with
underlying chronic kidney disease or diabetes.
Therefore, in this study we aimed to examine the ability of
microalbuminuria with uACR detected during the antenatal period

http://dx.doi.org/10.1016/j.preghy.2015.08.001
2210-7789/Ó 2015 International Society for the Study of Hypertension in Pregnancy. Published by Elsevier B.V. All rights reserved.
304 M. Jayaballa et al. / Pregnancy Hypertension: An International Journal of Women’s Cardiovascular Health 5 (2015) 303–307

to predict adverse pregnancy outcomes, including preeclampsia.
We hypothesized that an elevated uACR is associated with a higher
incidence of adverse pregnancy outcomes.
2. Study method
This is a single-centre retrospective analysis utilising medical
record review. The study population included pregnant women
over the age of 16 attending the renal pregnancy outpatient clinic,
also known as the ‘high-risk antenatal clinic’, at a tertiary public
hospital unit (Sydney, Australia) between July 2010 and June
2013. These patients were identified using an existing quality
assurance database in the Department of Renal Medicine. To be
included in the study, the participant had to have at least one
uACR measurement performed during pregnancy (excluding mea-
surements performed at or near to delivery). uACR measurements
were obtained at various time points in the pregnancy, from gesta-
tional periods 0–19+6 weeks, 20–27+6 weeks, 28–33+6 weeks. As
not all participants had uACR measurements at each of these time
points, the peak uACR measurement prior to 34 weeks gestation
(and prior to delivery date, to ensure that the uACR was not mea-
sured at the time of an adverse pregnancy outcome such as
preeclampsia) was chosen for the final analysis. Patient character-
istics, medications (particularly the use of aspirin and calcium),
blood pressure, urinalysis, serum creatinine, fetal and maternal
outcomes of the pregnancy were collected from patient medical
records and electronic databases. Those patients who did not have
at least one uACR performed prior to <34 weeks or did not have
data on the pregnancy outcomes of interest were excluded from
the study.
3. Data & statistical analysis
complications) [8], eclampsia, Intra Uterine Growth Restriction
(IUGR – defined by fetal weight <5th centile and abnormal uterine
doppler), premature delivery (<32 weeks) or placental abruption.
Secondary outcomes included the individual components of the
primary outcome, poor maternal outcome (including maternal
death, preeclampsia or eclampsia), and poor fetal outcome (includ-
ing miscarriage, stillbirth, neonatal death (within 7 days of birth),
IUGR, premature delivery (<32 weeks), placental abruption,
neonatal hypoglycaemia (defined as BSL < 2.5 mmol/L), neonatal
hyperbilirubinemia (defined as clinical jaundice and/or total serum
bilirubin > 86 lmol/L)), neonatal intensive care unit (NICU) or
Special Care for Neonates (SCN) admission, birth injuries or
congenital malformations.
Data analysis was performed by comparing the primary out-
come between the 3 uACR categories using Pearson’s Chi square
for 3 way comparison of normoalbuminuria vs. microalbuminuria
vs. macroalbuminuria. Covariates including age, body mass index
(BMI), pre-existing hypertension or chronic renal disease (as
recorded in medical records), history of preeclampsia, multiparity
(defined by parity P 1), multiple pregnancy, smoking before or
during pregnancy, peak serum creatinine during pregnancy (prior
to last trimester <34 weeks gestation or prior to onset of pre
eclampsia) and use of aspirin or calcium supplement (anytime
through the pregnancy) were examined to assess an association
with the primary outcome [9]. Multiple logistic regression analysis
was used to identify the independent predictors of the composite
primary outcome. Candidate variables for inclusion in the model
were those risk factors significant at p-value 6 0.05 in the univari-
ate analysis. Backward stepwise variable selection was then used
to identify the independent predictors of composite primary out-
come. Statistician support was used (with SPSS Statistics version
22 for data analysis).

Peak uACR was divided into 3 categories: <3.5 mg/mmol, 4. Results

3.5–35 mg/mmol (microalbuminuria) and >35 mg/mmol (macroal-
buminuria), categorised as per the Australasian Proteinuria
Consensus Working Group [7].
The primary outcome was a composite of any one of the follow-
ing maternal and fetal outcomes – maternal death, stillbirth,
neonatal death (within 7 days of birth), preeclampsia (PE) (defined
by ISSHP 2014 criteria: blood pressure >140/90 mmHg after
20 weeks gestation with either proteinuria >300 mg/day (or equiv-
alent) or presence of any maternal organ dysfunction i.e. renal
insufficiency, liver involvement, neurological or hematological
Out of 116 patients attending the renal pregnancy clinic
between July 2010 and June 2013, 33 patients were excluded due
to absence of at least one uACR performed prior to <34 weeks or
missing data on the pregnancy outcomes, leaving 83 patients for
the final analysis. The baseline characteristics of the patients in this
study are outlined in Table 1. The women had a mean age of 33.1
(±5.4) years. Mean BMI was 29.4 (±8.1) kg/m2. Almost half the pop-
ulation (47.6%) had a previous history of hypertension, one fifth
(20.2%) had a previous history of preeclampsia, and more than a

Table 1
Baseline characteristics of study population divided into those with primary outcome and those without.

N = 83 Primary outcome –positive N = 29 Primary outcome – negative N = 54 p-Value*

Age (years) 33.1 ± 5.4 33.7 ± 5.4 32.8 ± 5.5 –
BMI (kg/m2) 29.4 ± 8.1 29.8 ± 7.6 29.2 ± 8.4 –
Gravida 3.4 ± 2.3 3.8 ± 3.0 3.1 ± 1.8 –
Peak serum creatinine (lmol/L) 68.6 ± 46.9 90.7 ± 56.1 56.1 ± 40.3 –
Multiple pregnancy 4 (4.8%) 1 (3.4) 3 (5.6) 0.564
History of hypertension 40 (47.6%) 20 (69) 20 (36.4) 0.004
History of preeclampsia 17 (20.2%) 8 (27.6) 9 (16.4) 0.224
History of chronic kidney disease 31 (36.9%) 15 (51.7) 16 (29.1) 0.041
Diabetes mellitus (DM) 0.351**
Gestational DM 12 (14.3%) 6 (20.7) 6 (10.9)
Type 2 DM 10 (11.9%) 5 (17.2) 5 (9.1)
Type 1 DM 9 (10.7%) 2 (6.9) 7 (12.7)
Smoking before pregnancy 12 (4.3%) 7 (24.1) 5 (9.1) 0.098
Smoking during pregnancy 10 (11.9%) 6 (20.7) 4 (7.3) 0.087
Use of aspirin during pregnancy 26 (31%) 14 (48.3) 12 (21.8) 0.013
Use of calcium supplement during pregnancy 14 (17.1%) 4 (14.3) 10 (18.5) 0.762

Data is presented as n (%) or mean ± standard deviation as applicable.

*
p-Value is a comparison between the groups with and without primary outcome.
**
p-Value for all diabetic groups.
 M. Jayaballa et al. / Pregnancy Hypertension: An International Journal of Women’s Cardiovascular Health 5 (2015) 303–307 305

third (36.9%) had chronic kidney disease. Over a third of the

population (36.9%) had diabetes mellitus (DM) either in the form
of gestational diabetes mellitus (GDM), Type 2 DM or Type 1 DM.
Only a small proportion of the women had multiple pregnancy or
were smokers. Of note, about a third (31%) of the patients were
on aspirin during the pregnancy. However, documented use of cal-
cium supplementation during pregnancy in the study group was
seen only in 17.1% of patients. The median gestation at which the
peak uACR level collected in our study population was at gestation
20–27+6 weeks.
Analysis of the primary outcome in Fig. 1 (and Table A in
supplementary data) showed that as the degree of proteinuria
measured by uACR increased from normal (<3.5 mg/mmol) to
microalbuminuria (uACR 3.5 to 35 mg/mmol) to macroalbumin-
uria (uACR > 35 mg/mmol), the percentage of patients who had
the composite primary outcome increased stepwise, 13.8% to
24.1% to 62.1%, with the highest percentage in those who had
macroalbuminuria (p-value < 0.001). Similarly the same pattern
Fig. 2a. Percentage of patients with poor maternal outcome according to uACR
was seen in the reverse manner for those who did not have the pri- grouped by category. As the antepartum peak uACR increases by category from
mary outcome: as the uACR decreased, the percentage of those normoalbuminuria (<3.5 mg/mmol) to microalbuminuria (3.5–35 mg/mmol) to
without the composite primary outcome increased. macroalbuminuria (>35 mg/mmol), the percentage of patients who reached poor
We divided the population into two groups i.e. those who had maternal outcomes increased in a stepwise manner (p 6 0.001).
the composite primary outcome and those who did not, and
reviewed the differences in their characteristics (Table 1). Both were preeclampsia. Fig. 2a (and Table B in supplementary data)
groups had similar mean ages (33.7 vs. 32.8 years) and BMI (29.8 show that as the uACR increases categorically, the percentage of
vs. 29.2) respectively. However, the group with the composite pri- patients with poor maternal outcome also increased with the
mary outcome were almost twice as likely to have a history of highest percentage (59.3%) amongst those with uACR at macroal-
hypertension (66.7% vs. 37.0%, p = 0.009) and chronic kidney buminuria range (p 6 0.001). The same relationship was found
disease (50.0% vs. 29.6%, p = 0.041) as well as a higher peak serum with increasing uACR and poor fetal outcome as outlined in
creatinine (90.7 vs. 56.1 umol/L) compared to those who did not Fig. 2b (and Table C in supplementary data): as uACR increased,
reach the primary composite outcome. Those patients who were the percentage of patients with poor fetal outcome was higher
on aspirin during pregnancy also had more than twice the risk of (p = 0.001).
having the primary outcome compared to those who were not Multiple logistic regression analysis was performed using the
(46.7% vs. 22.2%, p = 0.020). The remaining variables including variables from univariate analysis which were significantly
multiple pregnancy, diabetes, previous history of preeclampsia, associated with the primary outcome. This included history of
smoking before or during pregnancy nor calcium supplements hypertension, CKD, use of aspirin during pregnancy and peak
did not show any significant difference. uACR. Only history of hypertension and uACR (peak prior to third
Since the primary outcome consisted of both poor maternal and trimester or 34 weeks gestation) remained independent predictors
fetal outcomes, we wanted to determine if the relationship of of the composite primary outcome (Table 2). After logistic regres-
higher uACR had the same effect on maternal and fetal outcomes sion, having a history of hypertension independently increased the
separately. Poor maternal outcome was defined as a composite of risk of the primary composite outcome by 3 times (OR 3.1,
maternal death, preeclampsia or eclampsia. Since none of the
patients in our study had reached maternal death, and only one
patient had eclampsia, the majority of the poor maternal outcomes

Fig. 1. Percentage of patients with composite primary outcome according to uACR
grouped by category. As the antepartum peak uACR increases by category from
normoalbuminuria (<3.5 mg/mmol) to microalbuminuria (3.5–35 mg/mmol) to
macroalbuminuria (>35 mg/mmol), the percentage of patients who reached
composite primary outcome, that comprised of both adverse maternal and fetal
outcomes, increased in a stepwise manner (p 6 0.001).
Fig. 2b. Percentage of patients with poor fetal outcome according to uACR grouped
by category. As the antepartum peak uACR increases by category from normoalbu-
minuria (<3.5 mg/mmol) to microalbuminuria (3.5–35 mg/mmol) to macroalbumin-
uria (>35 mg/mmol), the percentage of patients who reached poor fetal outcomes
increased with the highest percentage amongst those with macroalbuminuria
(p = 0.001).
306 M. Jayaballa et al. / Pregnancy Hypertension: An International Journal of Women’s Cardiovascular Health 5 (2015) 303–307
Table 2
Independent predictors of composite primary outcome (logistic regression analysis).
Independent predictors Odds ratio p-Value 95% C.I. for odds
of composite primary outcome ratio
Lower
History of hypertension 3.1 0.044 1.03
Peak uACR
(3.5–35) vs. <3.5 4.3 0.046 1.02
>35 vs. <3.5 13.5 <0.001 3.51
p = 0.044). On the other hand, women with microalbuminuria had
a 4.3 times increased risk of the primary outcome compared to
those with normoalbuminuria (p = 0.046), while the risk was 13.5
times more for those with macroalbuminuria compared to nor-
moalbuminuria (p 6 0.001).
5. Discussion
Markers of abnormal proteinuria in pregnancy include urinaly-
sis on dipstick and 24 h urine collection for protein. However, both
these tests have their limitations [2]. Thus far, there is a lack of evi-
dence demonstrating the value of spot urine albumin to creatinine
ratio (uACR) in pregnancy.
In a recent systematic review and meta-analysis, Morris
reviewed 5 studies enrolling a total of 620 women with suspected
preeclampsia [2]. Four of the studies used 24 h urine protein as the
reference standard and one used adverse pregnancy outcome [6].
Of the four studies that used 24 h collection as the reference stan-
dard, two were in a hypertensive population and two were in a
population with hypertension and proteinuria on dipstick. The
study using adverse pregnancy outcome was in a population with
hypertension only. No study has examined the value of uACR to
predict adverse pregnancy outcomes in patients with underlying
chronic kidney disease or diabetes. Three studies described the
timing of the sample, and one described the relation of the timing
of the 24 h collection. Three papers reported the use of automatic
dipstick analyzers for albumin to creatinine ratio. No meta-
analysis was possible due to the heterogeneity of the studies and
different thresholds used. The performance of uACR to predict pro-
teinuria varied widely. Gangaram et al. [6] reported results for
adverse outcome, including maternal morbidity, for which the sen-
sitivity was 0.55 (CI: 0.23 to 0.83) and specificity was 0.57 (CI: 0.48
to 0.65), and perinatal death, for which the sensitivity was 0.82 (CI:
0.48 to 0.98) and specificity was 0.59 (CI: 0.51 to 0.67).
In this single-centre retrospective study, we sought to deter-
mine if proteinuria measured during pregnancy by spot uACR can
be used as a marker to predict adverse pregnancy outcomes. The
results clearly support this hypothesis. Our results show that as
the uACR increases by category from normoalbuminuria to
microalbuminuria and macroalbuminuria, the percentage of
patients with the primary composite outcome of poor maternal
and fetal outcomes (including maternal death, stillbirth, neonatal
death, preeclampsia, eclampsia, IUGR, premature delivery, placen-
tal abruption) increases. After adjusting for history of hyperten-
sion, a high uACR (especially macroalbuminuria) in pregnancy
increased the risk of adverse pregnancy outcome by over 13 times
compared to normoalbuminuria. Importantly, we found that
microalbuminuria, which is missed by conventional means of mea-
surement such as urine dipstick, 24 h urine protein or urine pro-
tein:creatinine ratio, provided useful prognostic information
regarding the risk of adverse pregnancy outcomes.
Traditional risk factors for preeclampsia were evaluated in the
study population. Having a history of hypertension and chronic kid-
ney disease were two factors found to be more common amongst
patients with adverse pregnancy outcomes. Other previously
identified risk factors of preeclampsia include diabetes, multiple
pregnancy and history of preeclampsia [10], were not found to be
significantly correlated with the primary outcome in this study.
Those who had antepartum use of aspirin had a higher risk of
Upper adverse pregnancy outcomes compared to those who did not receive
9.08
aspirin but this likely reflects its prophylactic administration to
women thought to be at high risk of developing preeclampsia [9,11].
17.68
One of the limitations in our study is the small population size.
51.63 A number of patients had to be excluded due to lack of outcome
data. Many of these patients had been transferred to various private
hospital units for ongoing care of their pregnancy, hence their preg-
nancy outcomes were not available for our access. This could have
resulted in a selection bias of the population, as these patients
may have been the ones who tended to have a better pregnancy
course and outcomes, hence did not need the complex medical care
usually only available in public hospital systems. Furthermore, the
patients selected for the study were those who attended a ‘high risk’
antenatal clinic due to a tertiary care referral for various reasons
including co-morbidities such as diabetes, history of hypertension
or chronic kidney disease. Therefore, these patients may not be
representative of the general pregnant population. In the multiple
regression analysis, the only covariables that were statistically
significant predictors of the primary outcomes were a history of
hypertension and uACR. Other covariables that we would expect to
be statistically significant include DM, previous history of preeclamp-
sia and high BMI [10]. This may have been due to the relatively small
population size. Nonetheless, as we were unable to adjust for these
factors, we cannot exclude a confounding effect on the result.
The uACR level analysed in the study was chosen to be the peak
uACR prior to 34 weeks of gestation and/or prior to the develop-
ment of preeclampsia. The reason for this was not only to capture
the worst uACR and hence the highest risk for that patient but also
to minimise confounding antepartum proteinuria as a result of
preeclampsia. However, whether the peak uACR level was repre-
sentative of the degree of proteinuria throughout the pregnancy
needs to be further evaluated. A prospective trial collecting mea-
surements of uACR throughout pregnancy would address this issue.
This study did not compare the prognostic ability of uACR in
pregnancy to predict adverse pregnancy outcomes compared to
other measures of urinary protein such as urine dipstick, urine pro-
tein:creatinine ratio or 24 h urine protein. Such a comparison
would be useful to determine the relative merits of each method
to predict adverse pregnancy outcome, and would also be best
answered by a prospective observational trial.
In conclusion, despite the limitations of the study, we have
shown that uACR can be a useful simple marker to predict adverse
pregnancy outcomes including both poor maternal and fetal
outcomes. The results of this study requires further validation in
a prospective study with a larger population size before this can
be applied as a prognostic tool in clinical practice.
Conflict of interest
None of the authors have any conflicts of interest to declare.
Acknowledgement
We would like to acknowledge the support provided by
statistician, Karen Byth, Westmead Hospital.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.preghy.2015.08.
001.
 M. Jayaballa et al. / Pregnancy Hypertension: An International Journal of Women’s Cardiovascular Health 5 (2015) 303–307 307

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