ARTICLE IN PRESS

Transfusion and Apheresis Science ■■ (2015) ■■–■■

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Transfusion and Apheresis Science

j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / t r a n s c i

A life-saving therapy in Class I HELLP syndrome: Therapeutic

plasma exchange
Mehmet Ali Erkurt a, Ilhami Berber a,*, Hacı Bayram Berktas b, Irfan Kuku a,
Emin Kaya a, Mustafa Koroglu a, Ilknur Nizam a, Fatma Acar Bakırhan b,
Mustafa Ozgul a
a
Department of Hematology, Faculty of Medicine, Inonu University, Malatya, Turkey
b Department of Internal Medicine, Faculty of Medicine, Inonu University, Malatya, Turkey

A R T I C L E I N F O A B S T R A C T

Article history: HELLP syndrome, which can affect multiple organ systems and cause maternal and fetal
Received 18 August 2014 mortality, is a serious complication of pregnancy characterized by microangiopathic he-
Received in revised form 17 December molytic anemia, elevation of liver enzymes, and thrombocytopenia. Delivering the infant
2014
usually suffices for the treatment of this syndrome. In cases with Class I HELLP syndrome,
Accepted 19 December 2014
however, the clinical picture may rapidly deteriorate despite delivery. In this paper we pre-
sented the outcomes with the use of therapeutic plasma exchange in cases with class I HELLP
Keywords:
syndrome. This study included 21 patients diagnosed with the Class I HELLP syndrome at
HELLP syndrome
Therapeutic plasma exchange Inonu University Faculty of Medicine, Department of Hematology between 2011 and 2014.
A central venous catheter was placed and plasma exchange therapy was begun in pa-
tients unresponsive to delivery, steroid, and supportive therapy (blood and blood products,
antihypertensive therapy, intravenous fluid administration, and antibiotics) within 24 hours
after the diagnosis of Class I HELLP syndrome according to the Mississippi Criteria. All pa-
tients underwent therapeutic plasma exchange for three sessions each with a 1:1 volume.
Hemogram and biochemical parameters of the patients were evaluated before and after
the procedure. According to results, there was a statistically significant decrease in total
bilirubin, LDH, AST, and ALT levels whereas a significant increase in platelet count was ob-
served. Hemoglobin levels were increased, although this increase was not statistically
significant. HELLP syndrome is primarily treated with the delivery of infant; however, some
cases may show disease progression despite completion of delivery. As a potential cause
of both maternal and fetal mortality, HELLP syndrome condition should be aggressively
treated. Therapeutic plasma exchange is one of the available treatment options. Our study
has found that postpartum use of plasma exchange therapy within 24 hours is an effi-
cient and lifesaving treatment choice in Class I HELLP syndrome.
© 2014 Published by Elsevier Ltd.

1. Introduction thrombocytopenia. HELLP Syndrome is an acronym where

HELLP syndrome, which can affect multiple organ
systems and cause maternal and fetal mortality, is a serious
complication of pregnancy characterized by microangio-
pathic hemolytic anemia, elevation of liver enzymes, and
* Tel.: +90 422 341 0660, ext. 4203; fax: +90 422 341 07 28.
E-mail address: drilhamiberber@hotmail.com.
the letters in the word are the first letters of Hemolysis, El-
evated Liver Enzymes, and Low Platelet Count [1]. Martin
et al. described 3 risk categories of HELLP syndrome ac-
cording to the Mississippi classification based on the platelet
count: class I: <50.000/microliter (μl), class II: 50.000–
100.000/μl, class III: 100.000–150.000/μl [2]. Maternal
mortality in HELLP syndrome changes between 1 and 25%,
and it is usually due to the severity of disease, delayed di-
agnosis, presence of infection, and acute renal failure [3].

http://dx.doi.org/10.1016/j.transci.2014.12.026
1473-0502/© 2014 Published by Elsevier Ltd.

Please cite this article in press as: Ilhami Berber, A life-saving therapy in Class I HELLP syndrome: Therapeutic plasma exchange, Transfusion and Apheresis
Science (2015), doi: 10.1016/j.transci.2014.12.026
 ARTICLE IN PRESS
2 M.A. Erkurt et al./Transfusion and Apheresis Science ■■ (2015) ■■–■■
Most maternal deaths occur among women with class 1
HELLP syndrome [4].
The main treatment in HELLP syndrome is to stabilize
the patient clinically prior to delivery. In clinically mild cases,
watchful waiting following high dose corticosteroid therapy
until after 34th week to allow full maturation of fetal
development is the recommended approach [5,6]. In severe
cases, however, delivery should be completed within at most
24–48 hours by accelerating the fetal lung maturation after
corticosteroid therapy administered in the same period.
Platelet count returns to normal within 24 hours in a ma-
jority of patients; however, a low platelet count may persist
beyond delivery [7] in some cases.
Lactate dehydrogenase is a marker of hemolysis. Besides,
stage of the disease advances at HELLP syndrome as throm-
bocytopenia gets more apparent. For this reason, best
parameters to be used for follow-up of HELLP syndrome (as
they are measured more objectively compared to clinical
presentation of the patient) are the increase in platelet count
after therapeutic plasmapheresis and a decrease in LDH [8].
The maternal mortality rate is about 1.1% with HELLP syn-
drome. The infant morbidity and mortality rate is anywhere
from 10 to 60% depending on many factors such as gestation
of pregnancy, severity of symptoms and the promptness of
treatment. Most deaths in patients with HELLP syndrome occur
with class 1 disease (60%), and neurologic abnormality due
mostly to cerebral hemorrhage/stroke is the most common
system involved at autopsy (45%) [8–10]. It has been shown
that therapeutic plasma exchange may be effective in HELLP
syndrome not responsive to delivery. Plasma exchange therapy
was successfully used in patients who have organ failure or
refractory to treatment [11,12]. Plasmapheresis can replace a
patient’s plasma by a donor plasma and remove lots of harmful
substances in the bloodstream. It also replaces the coagulat-
ing factors, albumin and biologically active substances that
normally have to be carried out by the liver cells. Plasmapher-
esis in theory can lead to the removal of ammonia, endotoxins,
bilirubin, and inflammatory cytokines from the circulation.
Also, injection of large volumes of FFP (fresh frozen plasma)
in this method can help to improve the DIC, and removing
renin angiotensin and other vasoactive factors may improve
renal function [13]. All these advantages improve hepatic, renal
and neurologic function in patients with HELLP syndrome.
Therefore, this treatment especially considering the ad-
vanced cases of HELLP syndrome is very important.
Our purpose was to investigate the effects of the post-
partum use of plasma exchange therapy within 24 hours on
outcomes of patients with Class I HELLP syndrome.
2. Methods
This study included a total of 21 patients with Class I HELLP
syndrome who underwent therapeutic plasma exchange at
Inonu University Faculty of Medicine, Department of Hema-
tology between 2011 and 2014. The patients were followed
at the intensive care unit until after their laboratory and clin-
ical symptoms returned to normal upon delivery. The study
was approved by the Ethical Committee of Inonu University
Medical School, and written informed consent was obtained
from the patients or their relatives. The criteria required
for the diagnosis of HELLP syndrome included signs of
Please cite this article in press as: Ilhami Berber, A life-saving therapy in Class I HELLP syndrome: Therapeutic plasma exchange, Transfusion and Apheresis
Science (2015), doi: 10.1016/j.transci.2014.12.026
hemolysis (LDH > 600 U/L, increased total bilirubin, presence
of fragmented erythrocytes (schistocytes) in peripheral smear),
impaired liver function tests (AST > 70 U/L), and a low plate-
let count (<150.000/μL). Thrombocyte count was confirmed
by a peripheral smear in each patient. The differential diag-
noses included other disorders with microangiopathic
hemolytic anemia (thrombotic thrombocytopenic purpura, he-
molytic uremic syndrome, disseminated intravascular
coagulation, fatty liver of pregnancy, preeclampsia and ec-
lampsia). ADAMTS13 level could not be studied, owing to lack
of equipment. HELLP syndrome was diagnosed based on the
findings of clinical and laboratory examinations. The diagno-
sis was confirmed by a favorable response given by all patients
to therapeutic plasma exchange.
A central venous catheter was placed and plasma ex-
change therapy was begun in patients unresponsive to
delivery, steroid, and supportive therapy (blood and blood
products, antihypertensive therapy, intravenous fluid ad-
ministration, and antibiotics) within 24 hours after the
diagnosis of Class 1 HELLP syndrome according to the Mis-
sissippi Criteria [2]. Fresh frozen plasma was used as the
replacement fluid in therapeutic plasma exchange proce-
dure. Each patient underwent three sessions of therapeutic
plasma exchange on average with a Spectra Optia, and plas-
mapheresis was continued until clinical recovery and the
platelet count was over treshold for spontaneous bleeding.
This threshold platelet count was accepted over 50.000/μL.
Patients’ characteristics including age, numbers of preg-
nancy and abortion, methods of delivery, blood pressure, state
of consciousness, and presence of epileptic attacks were re-
corded. All patients were evaluated in terms of Glasgow Coma
Score [14]. Additionally, serum aspartate aminotransferase
(AST), alanine aminotransferase (ALT), blood urea nitrogen
(BUN), creatinine (Cr), calcium (Ca), phosphorus, serum total
bilirubin levels, lactic dehydrogenase (LDH), total protein,
albumin, hemoglobin (Hgb), leukocyte and platelet counts,
prothrombine time (PT), international normalized ratio (INR),
activated partial thromboplastin time (aPTT), D-dimers and fi-
brinogen levels were determined daily and the worst values
were taken for statistical comparison. The complete blood
count test was performed with a Beckman Coulter Immage
(Beckman Coulter, California, USA) device using the imped-
ance method; Hgb was measured with the photometric
method and the leucocyte subgroups with the laser method;
serum BUN and creatinine were measured with Aeroset Abbott
(Abbott Laboratories, Minnesota, USA) device using the spec-
trophotometric method. Mortality rate, causes of death,
complications including renal failure, dialysis requirement,
hepatic impairment, disseminated intravascular coagulopathy
(DIC), and infection were recorded.
Statistical analyses were performed using SPSS 17.0 soft-
ware package. Shapiro–Wilk test was used to test the normality
of distribution of the quantitative data. Wilcoxon test was used
to test the differences between the measured parameters
before and after therapeutic plasma exchange.
3. Results
Four (19.04%) patients delivered via vaginal route and 17
(80.96%) via caesarean section. Three patients (14.2%) were
primigravida while 18 (85.8%) patients were multigravida. The
 ARTICLE IN PRESS
M.A. Erkurt et al./Transfusion and Apheresis Science ■■ (2015) ■■–■■
Table 1
The overall characteristics of the patients with HELLP syndrome.
Parameters (n = 21) (mean ± standard deviation)
Leukocyte count (μl) (4.300–10.300)
Hgb (g/dl) (13.6–17.2)
Platelet count (μl) (150.000–450.000)
INR (0.8–1.2)
aPTT (seconds) (28–35)
AST (U/L) (5–35)
ALT(U/L) (0–55)
Total bilirubin (mg/dl) (0.2–1.2)
Direct bilirubin (mg/dl) (0–0.5)
LDH (U/L) (125–243)
BUN (mg/dl) (8.4–25.7)
Creatinine (mg/dl) (0.72–1.25)
mean age of the patient population was 31 + 4.9 (23–38) years.
All patients were in the third trimester of pregnancy. The
average gestational age of the fetuses have been founded to
35th gestational weeks. All fetuses were delivered alive. The
most common complication of the therapeutic plasma ex-
change procedure was chills and shivering, and no serious
complication was observed related to the procedure. Mean
Glasgow Coma Scale score of all the patients at the time of di-
agnosis was 9.5. Three patients (14.2%) was in coma, 4 (19%)
had stupor, 4 (19%) was confused and 10 (47.6%) were ori-
ented. All three patients in coma were intubated. One (4%) out
of 3 patients in coma passed away. All other patients were dis-
charged as oriented after plasmapheresis. In all of the patients,
there was a statistically significant decrease in total biliru-
bin, LDH, AST, and ALT levels, whereas a significant increase
in platelet count was observed. Hemoglobin levels were in-
creased, although this increase was not statistically significant.
None of our patients experienced any symptoms attribut-
able to anemia or thrombocytopenia, and no erythrocyte or
thrombocyte supplementation was provided to any of our pa-
tients during the therapeutic plasma exchange. The overall
characteristics of the patients undergoing therapeutic plasma
exchange are shown on Table 1.
Mean creatinine levels of the patients decreased after
therapeutic plasmapheresis compared to before (2.68–
1.67). But this improvement was not statistically significant.
Three out of 20 surviving patients had creatinine levels above
2 during follow-up after discharge. But none of these pa-
tients required renal replacement treatment. All patients
except one who had different stages of confusion were dis-
charged as oriented after plasmapheresis at this study. Six
patients had pneumonia. Five patients recovered from pneu-
monia while one patient passed away due to pneumonia.
The liver functions of all patients except the deceased were
back to normal.
4. Discussion
HELLP syndrome is a disorder that affects multiple organ
systems and causes maternal and fetal mortality [15,16]. In
HELLP syndrome, delivery of infant usually suffices for treat-
ment. In some cases, however, the clinical picture may
rapidly deteriorate despite delivery. In such circumstances,
corticosteroid may be added to the therapeutic regimen
[17,18]. Advanced therapeutic regimens are needed to avoid
Please cite this article in press as: Ilhami Berber, A life-saving therapy in Class I HELLP syndrome: Therapeutic plasma exchange, Transfusion and Apheresis
Science (2015), doi: 10.1016/j.transci.2014.12.026
3
Levels before TPE Levels after TPE P
16.500 ± 6.500 12.700 ± 3.070 0.015
8.8 ± 1.8 10.1 ± 2.5 0.7
32.100 ± 10.100 174.200 ± 110.200 0.001
1.15 ± 0.28 1.08 ± 0.19 0.7
26.09 ± 12.0 25.8 ± 10.7 0.3
709.8 ± 136.2 68.7 ± 21.5 0.001
350.6 ± 64.2 47.2 ± 30.6 0.001
7.5 ± 5.7 2.3 ± 1.1 0.03
5.03 ± 3.2 1.7 ± 0.9 0.0001
1721.1 ± 1053.8 361.3 ± 217.07 0.0001
39.6 ± 25.5 29.5 ± 12.5 0.134
2.68 ± 1.51 1.67 ± 1.06 0.17
maternal and fetal mortality in severe cases with low plate-
let counts unresponsive to corticosteroids. Only a few studies
have investigated the role of plasma exchange in HELLP syn-
drome. So far, the largest case series exploring the role of
plasma exchange in HELLP syndrome studied 26 patients.
This study showed that the postpartum application of plasma
exchange therapy was successful for persistent post-
partum HELLP syndrome; however, a uniformly favorable
response could not be obtained in patients who addition-
ally had a single or multiple organ injuries [12]. The majority
of the former studies on this subject are case reports. In these
reports, many patients had organ failure or persistent HELLP
syndrome and they rapidly showed a favorable response to
plasma exchange therapy [11,19–22]. Compatible with the
literature above, we found that therapeutic plasma ex-
change was an efficient and effective treatment modality for
patients with persistent HELLP syndrome in our study.
Lactate dehydrogenase is a marker of hemolysis. Besides,
stage of the disease advances at HELLP syndrome as throm-
bocytopenia gets more apparent. For this reason, best
parameters to be used for follow-up of HELLP syndrome (as
they are measured more objectively compared to clinical
presentation of the patient) are the increase in platelet count
after therapeutic plasmapheresis and a decrease in LDH [8].
In our patients, after therapeutic plasma exchange, LDH and
AST levels decreased and trombocyte count increased.
HELLP syndrome develops in 0.5–0.9% of all pregnan-
cies and 10–20% of all preeclampsia cases [18]. This
syndrome is diagnosed at antenatal period between 26th
and 28th weeks of gestation in 70% of cases while 30% of
cases are diagnosed in the postpartum period. The mean age
at the time of diagnosis is 24–28 years [3]. Haram et al. pub-
lished about 70% of the cases that developed before delivery,
the majority between the 27th and 37th gestational weeks;
the rest occurring within 48 hours after delivery [8]. Our
study included patients with Class I HELLP syndrome who
deteriorated despite completion of delivery. In our study,
all patients were in the third trimester and none of them
was in the postpartum period. The mean age of the patient
population was 31 + 4.9 (range 23–38) years and the average
gestational age was 35 weeks.
Maternal and fetal mortality are reportedly high in HELLP
syndrome. The mortality rate of the syndrome has been
reported at 1.1% [23]. This is due to increased rates of car-
diopulmonary complications, renal or hepatic failure,
 ARTICLE IN PRESS
4 M.A. Erkurt et al./Transfusion and Apheresis Science ■■ (2015) ■■–■■
pulmonary edema, infections, hemorrhage, and DIC
[3,24–26]. Literature data suggest a maternal mortality rate
of 1–28.5%. Martin et al. found a maternal mortality rate of
3.2% in 62 patients with HELLP syndrome, while it was found
at 1.1% in a larger study enrolling 442 patients [15]. Haris
et al. reported that patients with HELLP syndrome can be
effectively treated with therapeutic plasma exchange [27].
They reported that all patients completely improved and no
fatality was observed. Eser et al. reported that 26 patients
treated with therapeutic plasma exchange were cured and
none died [12]. One (4.7%) of our patients died from sepsis
among 21 patients. According to these results, therapeutic
plasma exchange performed within 24 hours dramatically
reduces mortality rates in patients with Class I HELLP
syndrome.
Therapeutic plasma exchange clears the antibodies from
plasma [8]. Hence, it may be suggested that therapeutic
plasma exchange reduces mortality by improving hepatic,
renal, respiratory, and cerebral functions and correcting
coagulopathy. Considering that these patients are mothers,
therapeutic plasma exchange also reduces maternal mor-
tality. All patients except one who had different stages of
confusion were discharged as oriented after plasmapher-
esis at this study. Six patients had pneumonia. Five patients
recovered from pneumonia while one patient passed away
due to pneumonia. The liver functions of all patients except
the deceased were back to normal.
Renal failure is one of the most important cause of mor-
tality in HELLP syndrome [25]. Martin et al., in a 777-
patient study, reported a renal failure rate of 1.2% [28]. Two
studies reported rates of renal failure of 3.2% and 7.7%
[16,29]. Eser et al. found acute renal failure incidence of 17.2%
in 26 patients with HELLP syndrome. In their study, only 2
patients had permanent renal injury, one of whom later
underwent peritoneal dialysis [12]. We found acute renal
failure rate of 42.8% (9 of 21 patients). Acute renal failure
improved with therapeutic plasma exchange in 6 (28.5%)
patients while 3 (14.2%) patients progressed to perma-
nent renal failure, all of whom are currently under dialysis-
free follow up.
Although HELLP syndrome tends to spontaneously
improve after delivery, affected patients should be moni-
tored for 48 hours after birth. This is because patients may
develop pulmonary edema, hepatic failure, renal failure, and
cerebrovascular disorder due to microthrombus [3,30]. We
observed no cases of pulmonary edema and liver failure im-
proved after therapeutic plasma exchange. Eleven (52.3%)
patients with impaired consciousness at the time of diag-
nosis returned to normal after therapeutic plasma exchange.
Limitations to our study are not being able to evaluate
ADAM TS 13 and complement levels due to technical in-
sufficiency, and having no control group. There is no
prospective study regarding plasma exchange and its effect
in HELLP syndrome. Plasma exchange for the HELLP syn-
drome has not yet been classified in the ASFA (American
Society For Apheresis) guideline. There are suggestions in
the National Therapeutic Apheresis Guide, because treat-
ment delay for HELLP syndrome is an important reason of
mortality for both mother and infant in our country. Plas-
mapheresis should be started within 24 hours HELLP
syndrome is diagnosed, especially in class I patients [31].
Please cite this article in press as: Ilhami Berber, A life-saving therapy in Class I HELLP syndrome: Therapeutic plasma exchange, Transfusion and Apheresis
Science (2015), doi: 10.1016/j.transci.2014.12.026
In conclusion, HELLP syndrome is an important cause of
fetal and maternal mortality. Thus, it is of paramount im-
portance to timely diagnose and manage this deadly disorder.
Plasma exchange therapy applied within 24 hours should
be remembered and carried out at once when delivery and
steroid therapy are not sufficient and thrombocytopenia
worsens. Our study suggests that postpartum use of plasma
exchange within 24 hours was discovered to be an effi-
cient and lifesaving treatment option in Class I HELLP
syndrome. In order to enlighten this issue, further prospec-
tive studies with more patients are required in the future.
Consent
Written informed consent was obtained from the
patient’s next of kin for publication of this manuscript and
accompanying images. A copy of the written consent is avail-
able for review by the Editor-in-Chief of this journal.
Authors’ contributions
This report reflects the opinion of the authors and does
not represent the official position of any institution or
sponsor. MAE was responsible for reviewing previous
research, journal hand searching, and drafting the report.
HBB, MK, IN, FAB, MO were responsible for provision of
published trial bibliographies, and preparing photographs.
EK, IK contributed to the final draft of the manuscript and
analysis of relevant data. IB was responsible for project
coordination. All authors read and approved the final
manuscript.
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