J. Perinat. Med.

2022; 50(2): 185–191

Filipe S. Mira*, Joana Oliveira, Filipa Sousa, Dora Antunes, Ana Carolina Figueiredo,
Andreia Borges, Maria S. J. Pais, Ana Galvão, Paulo Moura and Rui Alves

Kidney graft function before pregnancy as a

predictor of graft, maternal and fetal outcomes in
pregnant renal transplant recipients
https://doi.org/10.1515/jpm-2021-0102 syndrome). Graft function before pregnancy showed sig-
Received February 25, 2021; accepted October 19, 2021; nificant correlation with adverse outcomes.
published online November 3, 2021 Conclusions: A proteinuria >669 mg/g, serum creatinine
>1.75 mg/dL and glomerular filtration rate <36.2 mL/min/
Abstract
1.73 m2 before pregnancy were correlated to graft dysfunc-
tion during pregnancy. Similar values of proteinuria were
Objectives: Maternal and fetal complications can occur in
also associated with a risk of maternal hypertensive disor-
pregnant kidney transplant recipients. Since these are
ders and pregnancy failure. Therefore, in patients with
high-risk pregnancies, they require a multidisciplinary
proteinuria and graft dysfunction, follow-up should be
follow-up to prematurely detect adverse events. Identifying
stricter to quickly detect complications.
factors that would affect fetal, maternal and graft outcomes
is essential to further stratify the risk of pregnant kidney Keywords: graft dysfunction; kidney transplant; pre-
transplant recipients. eclampsia; pregnancy.
Methods: All pregnancies in kidney transplant recipients
followed in a single center for 30 years were included. Data
included previous transplant information and blood and
Introduction
urine tests performed before pregnancy. Impact of graft
function on fetal, maternal and graft outcomes was
Pregnancy in patients with end-stage renal disease is un-
evaluated.
common due to a reduced fertility (menstrual cycle irregu-
Results: There were 41 pregnancies among 34 patients.
larities and anovulation caused by uremia), serum
Mean gestational age of 35 ± 3 weeks. Caesarean section
hyperprolactinemia (due to lack of renal clearance) and a
was performed in 69.4% of patients. Five pregnancies were
lower libido [1–3]. Conception rates range from 0.9 to 7%
unsuccessful (12.2%). Four patients suffered an acute graft
while on dialysis [4]. After kidney transplant, if the graft is
dysfunction (9.8%) and 12 (29.3%) had a serious maternal
fully functional, fertility is usually restored in women
hypertensive disorder (preeclampsia, eclampsia or HELLP
of childbearing age 6 months after transplant (as the
hypothalamic-pituitary-ovarian axis normalizes) thus mak-
ing it easier to conceive, although with a lower likelihood
than the general population [5–7]. Obstetric complications
Filipe S. Mira and Joana Oliveira contributed equally to this work and
such as maternal hypertensive disorders (MHD), caesarean
share first authorship.
sections, fetal growth restriction, stillbirth, preterm delivery
*Corresponding author: Filipe S. Mira, MD, Nephrology Department, and low birth weight are commonly described in kidney
Coimbra University Hospital, Rua Alfredo Lopes Xisto, n° 36, 3000- transplant recipients (KTR) [8]. As pregnancy in these pa-
020, Coimbra, Portugal; and Faculty of Medicine, University of tients often requires changes in immunosuppressive drugs
Coimbra, Coimbra, Portugal, Phone: +351 932463036,
(cessation of mycophenolate mofetil and/or mTOR in-
E-mail: filipemira@netcabo.pt
Joana Oliveira, Filipa Sousa, Dora Antunes and Paulo Moura, Faculty
hibitors for example) and adjustments in other chronic
of Medicine, University of Coimbra, Coimbra, Portugal; and Obstetrics medication, there is always the risk of allograft function
A Department, Coimbra University Hospital, Coimbra, Portugal deterioration due to graft rejection (although rare during
Ana Carolina Figueiredo, Andreia Borges, Ana Galvão and Rui Alves, pregnancy – about 4.2% of cases) [9].
Nephrology Department, Coimbra University Hospital, Coimbra, According to kidney disease: improving global out-
Portugal; and Faculty of Medicine, University of Coimbra, Coimbra,
comes (KDIGO) guidelines, transplant recipients should
Portugal
Maria S. J. Pais, Obstetrics A Department, Coimbra University wait at least one year after transplant before trying to
Hospital, Coimbra, Portugal conceive and there should have been no rejection episodes
186 Mira et al.: Predictors of adverse outcomes in KTR

for the past year. They should also only attempt it once Gestational diabetes was defined as the diagnosis of diabetes in
kidney function is stable (with steady immunosuppression) the second or third trimester of pregnancy, using the 2010 interna-
tional association of diabetes and pregnancy study groups (IADPSG)
and once proteinuria is less than 1 g/day, with a regular
oral glucose tolerance test as screening and diagnostic criteria [14].
multidisciplinary follow-up afterwards that includes a Preterm birth was defined as a live birth before 37 weeks of
specialized obstetrician (as it is considered a high-risk gestation. According to the ACOG guidelines, fetal growth restriction
pregnancy) [10]. Women with a glomerular filtration rate (FGR) occurs when a fetus does not reach its full growth development
(GFR) under 40 mL/min/1.73 m2 have an increased risk for potential remaining with an estimated fetal weight lower than the 10th
percentile for gestational age, and it can be diagnosed through stan-
accelerated GFR decline, as well as unfavorable fetal out-
dardized curves that estimate fetal growth patterns such as the World
comes which are similar in kidney transplant recipients [11].
Health Organization Fetal Growth Charts [15, 16]. Small for gestational
As experience with these patients increases, so does the age (SGA) fetuses are those with a weight lower than the 10th
need to identify markers that could predict a higher proba- percentile for the gestational age at the time of birth.
bility of unfavorable maternal, fetal and graft outcomes This research was conducted according to the Declaration of
therefore allowing for a closer follow-up in higher risk Helsinki and the Declaration of Istanbul ensuring that the anonymity
of all patients was guaranteed.
patients.
IBM SPSS Statistics 26 was used for statistical analysis. A
The objectives of this study were to identify potential p-value<0.05 was considered statistically significant. Mean values and
clinical and analytical markers (such as time after trans- standard deviations were calculated. Comparison of means and fre-
plant, maternal age, serum creatinine, GFR and proteinuria quencies of normally distributed variables were calculated using
at least three months before pregnancy) for unfavorable t-tests and the χ2 test. Independent samples t-test was used to compare
maternal age, time after transplant, serum creatinine, GFR and pro-
graft outcomes (acute dysfunction or graft loss during
teinuria with variables related to unfavorable graft outcome as well as
pregnancy) as well as for fetal and maternal complications.
maternal and fetal complications.

Materials and methods Results

This is a retrospective cohort study involving all pregnant kidney

Patient characteristics
transplant recipients followed in a single tertiary center over a period
of 30 years (from 1989 until 2019). These patients had a follow-up There were 41 pregnancies (40 single pregnancies and one
performed by multidisciplinary team including a nephrologist and a twin pregnancy) among 34 renal transplant recipients. The
specialized obstetrician. Appointments were conducted every two majority (87.8%) were successful (live birth) leading to the
weeks during the first two trimesters and weekly in the third trimester.
delivery of 37 newborns.
From January 1989 to December 2019 there were 41 pregnancies in 34
kidney transplant recipients followed in our institution. Our sample’s median maternal age was 28 years (inter-
Maternal details such as race, age at conception, time in renal quartile range 24–32 years) with a median transplantation-
substitution therapy before the transplant, time between transplant to-pregnancy interval of 51 months (interquartile range
and pregnancy, number of gestations, body mass index (BMI), pre- 23–84 months) and a median duration of end stage kidney
vious diseases (such as type 2 diabetes mellitus or hypertension) as
disease (ESKD) before transplant of 36 months (interquartile
well as chronic medication intake (including immunosuppressants)
were all collected retrospectively from the existing patient records.
range 18–70 months). The cause for ESKD was unknown
Serum creatinine and proteinuria (calculated from a spot urine in nine patients (26.5%), pyelonephritis in seven patients
protein/creatinine ratio) were collected at least three months before (23.5%), glomerulonephritis in seven patients (23.5%),
pregnancy and GFR was calculated from the values obtained from hypertension in six patients (17.6%), secondary to polycystic
this investigation (using the modification of diet in renal disease – kidneys in three patients (8.8%) and caused by renal
MDRD Study Group Equation) [12]. Serum creatinine three months
vascular disease in two patients (5.9%). Most of the patients
after delivery was collected to calculate the differential with the
value three months before conception. Obstetric and neonatal out- (97.1%) were caucasian. Median body mass index (BMI)
comes such as gestational age at birth, birthweight and neonatal before pregnancy was 28 kg/m2 (interquartile range 26–30).
death were also collected. Twenty three patients (67.6%) had been previously diag-
Allograft dysfunction was defined as an increase in serum nosed with hypertension and five (14.7%) had a previous
creatinine >0.3 mg/dL during pregnancy using as a baseline the value
diagnosis of type 2 diabetes mellitus (Table 1).
obtained just before conception.
Diagnosis of MHD such as preeclampsia, eclampsia and hemo-
Although, during these last few years, changes have
lysis, elevated liver enzymes, low platelet count (HELLP) syndrome been made on the field of transplant nephrology as well as
was defined according to the international society for the study of obstetrics and natal care, the maternal characteristics were
hypertension in pregnancy (ISSHP) guidelines [13]. similar between patients pregnant in the first 15 years of our
 Mira et al.: Predictors of adverse outcomes in KTR 187

Table : Maternal characteristics of pregnant kidney transplant time of renal substitution therapy before transplant and
recipients. allograft dysfunction. However, patients that had an acute
graft dysfunction during pregnancy had a significantly
Patients (n=)
higher mean serum creatinine (p=0.002) before conception
Age when pregnant, years  ± . (mean 2.05 ± 0.8 mg/dL) when compared to patients with
Number of pregnancies per patient
stable graft function (mean 1.14 ± 0.48 mg/dL). GFR before
– One  (.)
pregnancy was also significantly lower (p<0.05) in patients
– Two  (.)
– Three  (.) that developed an acute allograft dysfunction (mean:
Living kidney donor  (.) 41.1 ± 18.4 mL/min/1.73 m2) than in patients with a stable
Caucasian  (.) graft function (mean: 72.1 ± 29.2 mL/min/1.73 m2). Finally,
Pre-pregnancy hypertension  (.) mean proteinuria before pregnancy was also significantly
Pre-pregnancy diabetes  (.)
higher (p<0.001) in patients who developed an acute
Transplantation-to-pregnancy, monthsa  ± 
– ≤1 year after transplant  (.) dysfunction during pregnancy (mean: 833.7 ± 106.4 mg/g)
– >1 year after transplant  (.) comparing to patients with a stable function (mean:
a 303.6 ± 292.6 mg/g). Using a logistic regression, these three
Each pregnancy was calculated separately.
Values are given as n (%) or mean ± SD. variables were responsible for 53% of the variance within
the sample.
sample when compared to the last 15 years. There were no By using ROC curves for these three variables, we
significant differences in maternal age, duration of ESKD and were able to discriminate cut-off points for each of them
transplantation-to-pregnancy interval. The only significant that would help to discriminate a higher likelihood of
change was the calcineurin inhibitor used that was different acute graft dysfunction during pregnancy (Figure 1A–C).
in the last four patients (tacrolimus instead of cyclosporine). Regarding serum creatinine, the ROC curve obtained an
area under the curve (AUC) of 0.855 (Figure 1A) and using
the Youden index, a cut-off point of 1.75 mg/dL was
Allograft function obtained (with a sensitivity of 75% and a specificity
of 92%) allowing to discriminate a greater likelihood for
In most cases (26 pregnancies) the immunosuppressive acute graft dysfunction during pregnancy. The ROC curve
regimen had to be changed before pregnancy due to the concerning GFR (Figure 1B) obtained an AUC of 0.82 with
presence of mycophenolate mofetil. The remainder had no a cut-off point of 36.2 mL/min/1.73 m2 (with a sensitivity of
need to change immunosuppression. Most kidney grafts in 92% and a specificity of 75%). Finally, in terms of pro-
this sample had come from a deceased donor, as only one teinuria before pregnancy (Figure 1C), the ROC curve had
was from a living donor. Human leukocyte antigen (HLA) an AUC of 0.93 with a cut-off point of 669 mg/g (with a
compatibilities ranged from 0 to 6 but most of the patients sensitivity of 100% and a specificity of 84%).
had three compatibilities. Only four patients became
pregnant less than one year after being transplanted (only
one of those less than six months after being transplanted). Maternal outcomes
All patients had at least one serum creatinine and pro-
teinuria value before pregnancy. Serum creatinine before There were 12 pregnancies complicated with a MHD during
pregnancy had a mean value of 1.2 ± 0.58 mg/dL while follow-up (29.3%) and four patients that developed gesta-
proteinuria had a median value of 180 mg/g (interquartile tional diabetes (9.8%). Both complications had no correla-
range 85–669 mg/g). Glomerular filtration rate had a mean tion with previous diseases, transplantation-to-pregnancy
value of 69 ± 29.7 mL/min/1.73 m2. In 10 of the pregnancies interval, maternal age, cause of ESKD or duration of kidney
(24.4%), the patient’s serum creatinine was ≥1.4 mg/dL substitution therapy. In 24 of the pregnancies (58.5%), the
before pregnancy. patient had been medicated with low-dose aspirin (14 of
During pregnancy there were four cases (9.8%) of these patients had a prior diagnosis of hypertension). There
acute allograft dysfunction, all of them occurred in patients was no statistical correlation between the use of low-dose
that had their immunosuppression altered at least two aspirin in patients with prior hypertension and developing
months before conception. There was no need for renal MHD although most patients who developed MHD (58.3%)
substitution therapy in any of those cases. No correlation were not under low-dose aspirin prophylaxis.
was verified between maternal age, previous diseases, Patients that developed MHD in pregnancy had a
compatibilities, transplantation-to-pregnancy interval, or higher serum creatinine (with a mean of 1.43 ± 0.64 mg/dL
188 Mira et al.: Predictors of adverse outcomes in KTR

Figure 1: ROC curves on the variables that discriminate a higher likelihood of acute graft dysfunction during pregnancy.
(A) Creatinine before pregnancy; (B) GFR before pregnancy; (C) proteinuria before pregnancy.

when compared with the other patients with a mean of 1.14 ± 0.47 mg/dL (p=0.008). Regarding mean pregestational
1.15 ± 0.54 mg/dL) and a lower GFR (56.8 ± 28.7 vs. proteinuria, unsuccessful pregnancies had also higher
74.2 ± 29 mL/min/1.73 m2) before conception than patients values than successful pregnancies (719.6 ± 142.9 mg/g
that did not develop this condition, although this differ- vs. 304.8 ± 306 mg/g) revealing a significant difference
ence was not statistically significant (p>0.05). On the other (p<0.001). By using a ROC curve for proteinuria, an AUC of
hand, mean pregestational proteinuria before pregnancy 0.84 was obtained with a cut-off point of 452 mg (with a
had a significant correlation with the development of MHD sensitivity of 100% and a specificity of 75%) for a higher risk
during pregnancy follow-up comparing to patients who of an unsuccessful pregnancy. Although there was a differ-
did not develop this condition (560.2 ± 359 mg/g vs. ence between both unsuccessful and successful childbirth
270.6 ± 267.4 mg/g), p=0.008. By using a ROC curve, a cut- regarding GFR (48.4 ± 28 and 72 ± 29.1 mL/min/1.73 m2
off point of 750 mg/g was obtained with an AUC of 0.77 respectively), this difference did not retain its statistical
(with a specificity of 93.1%) for a higher risk of developing significance (p=0.09).
MHD during pregnancy. Finally, there was also a statistically significant cor-
relation between pregestational proteinuria and preterm
deliveries with a higher value of proteinuria in patients that
Fetal outcomes had a preterm delivery (403.6 ± 341 mg/g) when compared
to other patients (149.4 ± 150.2 mg/g), p=0.04. Although
Thirty-six of the 41 pregnancies were successful (87.8%). both a higher serum creatinine and a lower GFR before
Most of the deliveries were through caesarean section pregnancy were indicative of a greater chance of a preterm
(25 out of 36–69.4%). The mean gestational age at delivery delivery, they were not statistically significant.
was of 35 ± 3 weeks with a minimum of 29 weeks and a Table 2 includes the full results on every single
maximum of 39 weeks, counting a total of 22 preterm de- outcome studied according to allograft function.
liveries (61.1%). There were eight cases (19.5%) of FGR and
12 SGA fetuses (29.3%) with a mean live birth weight of
2,399 ± 679 g.
There was no correlation between fetal outcomes and Discussion
maternal variables. There was, however, a significant corre-
lation between graft function before pregnancy and fetal Although kidney transplant increases the likelihood of
outcomes. Unsuccessful pregnancies (fetal death) had a pregnancy in patients previously under dialysis, success is
mean pregestational serum creatinine of 1.86 ± 0.9 mg/dL not a guarantee as maternal and fetal adverse effects are
whereas successful pregnancies had a mean value of more common than in the general population.
 Mira et al.: Predictors of adverse outcomes in KTR 189

Table : Allograft function and study outcomes. number of preterm deliveries in women with higher pre-
gestational mean proteinuria. This may portray that an
Yes: n ± σ, % No: n ± σ, % p-Value unstable allograft may contribute negatively to the fetus’
Allograft outcomes development and a proteinuria higher than 450 mg may
Allograft dysfunction  (.)  (.) contribute as a risk factor for an unsuccessful pregnancy,
– Mean pregestational . ± . . ± . .a
which goes according to the existing literature [22].
serum creatinine,
Allograft function during pregnancy usually re-
mg/dL
– Mean pregestational . ± . . ± . .a mains unchanged and rejection is a rare occurrence
GFR, mL/min/1.73 m2 (4.2% of cases) [17]. In our population, regarding graft
– Mean pregestational . ± . . ± . <.a function during pregnancy, a serum creatinine higher
proteinuria, mg than 1.75 mg/dL, a proteinuria higher than 669 mg and a
Maternal outcomes
GFR lower than 36.2 mL/min/1.73 m2 before pregnancy
MHD  (.)  (.)
– Mean pregestational . ± . . ± . >. were important in our population to predict a higher
serum creatinine, chance of gestational allograft dysfunction.
mg/dL Finally, MHD rate in our population was slightly higher
– Mean pregestational . ± . . ±  >. than the results portrayed in the existing literature [17]. MHD
GFR (mL/min/1.73 m2)
are well-known risk factors for FGR, SGA newborns, preterm
– Mean pregestational . ±  . ± . .a
delivery and graft function deterioration. According to the
proteinuria, mg
Fetal outcomes American College of Obstetricians and Gynecologists, low-
Preterm delivery  (.)  (.) dose aspirin prophylaxis should be initiated in women with
– Mean pregestational . ± . . ± . >. a high risk of preeclampsia since it reduces its risk in women
serum creatinine, at a higher risk for adverse perinatal outcome, shifting
mg/dL
preeclampsia in those patients to later gestational ages [23].
– Mean pregestational . ± . . ± . >.
GFR, mL/min/1.73 m2 Pregnant kidney transplant patients, due to their high
– Mean pregestational . ±  . ± . .a comorbidity rates may benefit from this prophylaxis if their
proteinuria, mg risk of preeclampsia is high since aspirin use has been
Unsuccessful pregnancy  (.)  (.) proven to be safe during pregnancy in this population. In
– Mean pregestational . ± . . ± . .a
our population, 58.5% of pregnancies were medicated with
serum creatinine,
prophylactic low-dose aspirin, most of them (58.3%) with a
mg/dL
– Mean pregestational . ±   ± . . prior diagnosis of hypertension. There was no correlation
GFR, mL/min/1.73 m2 between the use of low-dose aspirin and both the value of
– Mean pregestational . ± . . ±  <.a proteinuria and serum creatinine. Although not statistically
proteinuria, mg significant (p=0.067), most patients with MHD were not
a
p<.. under any low-dose aspirin (58.3%) and as such, this may
emphasize the role of low-dose aspirin prophylaxis in
In our study, most KTR had successful pregnancies pregnant kidney transplant patients. Proteinuria also
(although most of the newborns were born preterm), which showed a significant influence in the development of MHD
is consistent with the existing literature on the topic during pregnancy, and a value of 750 mg was indicative of a
[17–19]. Preterm deliveries were frequent and average birth higher chance of MHD. Contrary to current literature, graft
weight was significantly lower than in the general popu- function calculated from pregestational serum creatinine
lation, which is also corroborated in literature [20]. was not a significant predictor of the development of MHD
Nevertheless, our mean live birth weight in KTR was higher during pregnancy but patients that developed one of these
when compared to the study conducted by Bachmann F. entities showed a higher mean serum creatinine at least
et al. but similar to Mariano S. et al.’s work (both of them three months before conception [24].
with different studied populations) [20, 21]. Graft function Contrary to what was expected, transplantation-to-
before pregnancy was the main predictor to the success of pregnancy interval did not have an impact in our popula-
pregnancies in KTR, specifically proteinuria at least three tion regarding the chance for acute graft dysfunction or an
months before conception. This variable was not only increase in maternal or fetal complications.
significant in terms of pregnancy success but also Unfortunately, in KTR proteinuria is usually controlled
regarding the timing of delivery as we observed a high using angiotensin-converting enzyme inhibitors or
190 Mira et al.: Predictors of adverse outcomes in KTR

angiotensin receptor blockers, which are not recom- intellectual input. All authors have accepted responsibility
mended during pregnancy. Although in our population, for the entire content of this manuscript and approved its
prior hypertension did not prove to be a statistically sig- submission.
nificant risk factor for developing MHD, especially pre- Competing interest: Authors state no conflict of interest.
eclampsia, in literature, chronic hypertension is common Informed consent: Not applicable.
in kidney transplanted women and it remains as a risk Ethical approval: This research was conducted according
factor not only for adverse maternal outcomes but also as a to the Declaration of Helsinki and the Declaration of
higher risk of fetal death when blood pressure is not Istanbul ensuring that the anonymity of all patients was
controlled [24]. This emphasizes the need for strict control guaranteed.
of hypertension in kidney transplanted women. Control-
ling blood pressure alone can sometimes stabilize pro-
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