Original Article

Joelcio Francisco Abbade

Jos Carlos Peraoli
Roberto Antonio Arajo Costa
Iracema de Mattos Paranhos
Calderon
Vera Therezinha Medeiros Borges
Marilza Vieira Cunha Rudge

ABSTRACT

CONTEXT: HELLP syndrome is a severe complication

of pregnancy characterized by hemolysis, elevated
liver enzymes and low platelet count. Some pregnant women develop just one or two of the characteristics of this syndrome, which is termed Partial
HELLP Syndrome (PHS).
OBJECTIVE: The objective of this study was to evaluate
the repercussions on maternal and perinatal outcomes among women that developed PHS and to
compare these women with those whose gestational
hypertension or preeclampsia did not show alterations for HELLP syndrome in laboratory tests.
DESIGN: Observational, retrospective and analytical study.
SETTING: Maternity Department of Hospital das Clnicas,
Faculdade de Medicina de Botucatu, Universidade
Estadual Paulista, Botucatu, So Paulo, Brazil.
SAMPLE: Pregnant or post-delivery women who had a
blood pressure elevation that was first detected after mid-pregnancy, with or without proteinuria, between January 1990 and December 1995.
MAIN MEASUREMENTS: Analysis was made of maternal age, race, parity, hypertension classification,
gestational age at the PHS diagnosis, alterations in
laboratory tests for HELLP syndrome, time elapsed
to discharge from hospital, maternal complications,
mode of delivery, incidence of preterm birth, intrauterine growth restriction, stillborn and neonatal death.
RESULTS: Three hundred and eighteen women were selected; forty-one women (12.9%) had PHS and 277
of them (87.1%) did not develop any of the alterations of the HELLP syndrome diagnosis. Preeclampsia
was a more frequent type of hypertension in the
PHS group than in the hypertension group. None of
the women with isolated chronic hypertension developed PHS. The rate of cesarean delivery, eclampsia, and preterm delivery was significantly greater
in the PHS group than in the hypertension group.
CONCLUSION: We observed that aggressive procedures
had been adopted for patients with PHS. These resulted in immediate interruption of pregnancy, with
elevated cesarean rates and preterm delivery. Such
decisions need to be reviewed, in order to reduce the
cesarean rate and the incidence of preterm delivery.

KEY WORDS: HELLP syndrome. Partial HELLP Syndrome. Preeclampsia. Maternal outcome. Perinatal outcome.

Partial HELLP Syndrome:

maternal and perinatal outcome
Maternity Department of Hospital das Clnicas, Faculdade de Medicina
de Botucatu, Universidade Estadual Paulista Jlio de Mesquita Filho,
Botucatu, So Paulo, Brazil.

INTRODUCTION

Hemolysis, elevated liver enzymes and low

platelet count are alterations in laboratory tests
that are found in pregnant or post-delivery
women who have preeclampsia. The term
HELLP syndrome was coined for this set of
alterations by Weinstein in 1982.1 Since then
many reports have been presented, but the
quantification of laboratory tests has differed
among them.2-15
Since Sibai2 proposed strict criteria for the
diagnosis of the true HELLP syndrome it
has been observed that many women with severe preeclampsia may have laboratory abnormalities such as isolated hemolysis or low
platelet count or elevated liver enzymes, without the complete HELLP syndrome. Women
with partial HELLP syndrome (PHS) should
be studied and managed separately from
women with HELLP syndrome or severe
preeclampsia.15
The incidence of HELLP syndrome is 2
to 12%,8,11,16-21 while the incidence of PHS is
unclear, but probably around 21 to 24%.15,22
There is no information about PHS incidence
in Brazil.
HELLP syndrome may begin as PHS,
because it is an insidious and progressive disease. This characteristic is corroborated by the
different elapsed times seen in laboratory tests
for its alterations and the progress of the disease. Another factor that supports this idea is
that in spite of delivery being the definitive
treatment for women with HELLP syndrome,
the condition of some women worsens over
the first 48 hours after delivery.23
The purpose of this report was to com-

pare maternal and perinatal outcomes between

women with PHS and women who had severe blood pressure elevation but normal laboratory tests for HELLP syndrome.

METHODS

This was a retrospective, observational and

analytic study. It was made in the Maternity
Department of a university hospital, Hospital das Clnicas of Universidade Estadual
Paulista, which is a third-level public hospital
located in the central region of So Paulo State,
Brazil. We searched through the perinatal database of our Maternity Department for pregnant or post-delivery women who had had a
blood pressure elevation that was first detected
after mid-pregnancy, either with proteinuria
(preeclampsia) or without it (gestational hypertension) between January 1991 and December 1995. We reviewed maternal and
neonatal medical charts.
HELLP syndrome was defined by the
presence of all of the three following criteria:
hemolysis (characteristic peripheral blood
smear, serum lactate dehydrogenase 600 U/
l, total serum bilirubin 1.2 mg/ml), elevated
liver enzymes (serum aspartate aminotransferase 70 U/l), and low platelet count (<
100,000/l). Partial HELLP syndrome (PHS)
was defined by the presence of one or two features of HELLP but not the complete syndrome.15 Patients were defined as having severe hypertension according to the criteria of
the National High Blood Pressure Education
Program (2000).24 The patients were divided
into two groups: Partial HELLP Syndrome
Group (patients with PHS) and Hypertension

Sao Paulo Med J/Rev Paul Med 2002; 120(6):180-4.

So Paulo Medical Journal - Revista Paulista de Medicina

Group (patients with severe gestational hypertension/preeclampsia but without alterations

in laboratory tests for HELLP syndrome).
Women with renal, liver or hematological disease and multiple pregnancy were excluded
from the study.
Gestational age was determined by using
the best-accepted obstetric criteria, including
menstrual history, early clinical evaluation and
ultrasonography at < 20 weeks of gestation.
The classification of the hypertensive disorders of pregnancy was done according to the
National High Blood Pressure Education Program (2000),24 i.e. chronic hypertension, gestational hypertension, preeclampsia/eclampsia, gestational hypertension or preeclampsia
superimposed upon chronic hypertension. We
evaluated the abnormal laboratory findings in
the PHS group and the gestational age at
which PHS was diagnosed. We compared the
time elapsed until discharge from hospital,
maternal complications (imminent eclampsia,
eclampsia, abruptio placentae and maternal
mortality), mode of delivery (cesarean section),
preterm delivery (gestational age < 37 weeks),
perinatal outcome (intrauterine growth restriction, stillborn and neonatal death).
Data are presented as incidences. Statistical comparisons were performed by 2 analysis, Pearson 2 analysis and exact Fisher test,
as appropriate. A p value < 0.05 was considered significant. Statistical analysis was performed using the Statistical Package in Social
Science for Windows (SPSS Inc, Chicago,
version 10.0).
The procedures above were in accordance
with the ethical standards of the Medical Ethics Committee of our university and with the
Declaration of Helsinki.25

RESULTS

During the study period, 329 patients had

clinical and laboratory findings of severe hypertension. Six women were excluded from
the analysis because they had complete
HELLP syndrome. Three women had multiple pregnancy and two had chronic renal insufficiency, and they were also excluded.
Among the remaining 318 women, 41
(12.9%) had PHS and 277 (87.1%) had elevated blood pressure levels, clinical and laboratory findings of severe gestational hypertension (GH) or preeclampsia (PE), with normal laboratory test results for HELLP syndrome. Demographic characteristics are presented in Table 1. Most of the women were in
the 19 to 34-year-old age range. White women
were more frequent in both groups. Twenty-

Sao Paulo Med J/Rev Paul Med 2002; 120(6):180-4.

181

one women (51.2 %) were nullipara in the

PHS group and 128 (46.2%) in the hypertension group. There was no significant difference in these variables between the groups.
Among these women, 9.8% had
preeclampsia and 19.5% had gestational hypertension superimposed upon chronic hypertension. Isolated preeclampsia was more frequent
in the PHS group (41.5%) than in the hypertension group (29.6%). Gestational hypertension was observed in 13 women (29.3%) in

the PHS Group and 103 (37.2%) in Hypertension Group. There were no significant differences among these factors (Table 1).
PHS was diagnosed mainly in preterm
pregnancies (66.7%). Twenty-two women
(56.4%) had gestations of less than 34 weeks
and 5 of them (12.8%) had gestations of less
than 29 weeks. Of the 41 patients with PHS,
14 (34.1%) only had hemolysis, 7 (17.1%) had
hemolysis and low platelet count and 5 (12.2%)
had hemolysis and elevated liver enzymes. Eight

Table 1. Baseline characteristics of women with partial HELLP syndrome (hemolysis,

elevated liver enzymes and low platelets) and with only hypertension, according
to maternal age, race, parity and hypertension classification
Partial HELLP

Hypertension

Syndrome Group
N
%

p - value

Group
N

0.305

Maternal age (years)

6

14.6

50

18.1

19 to 34

24

58.5

180

64.9

35

11

26.8

47

17.0

<19

0.915

Race
White
Black

33

80.5

220

79.4

19.5

57

20.6

0.858

Parity
Nullipara

21

51.2

131

47.3

1 to 4

18

43.9

128

46.2

4.9

18

6.5

0.306

Classification of hypertension
Gestational hypertension

12

29.2

103

37.2

Preeclampsia

17

41.5

82

29.6

Gestational hypertension
superimposed upon chronic
hypertension

19.5

45

16.2

Preeclampsia superimposed
upon chronic hypertension

9.8

47

17.0

Table 2. Distribution of partial HELLP syndrome (PHS) group (hemolysis, elevated liver
enzymes and low platelets), according to gestational age at which PHS was diagnosed and
type of alterations seen in laboratory tests for HELLP syndrome
Partial HELLP Syndrome Group
N

26

66.7

Gestational age at which PHS was diagnosed

< 37 weeks
23 28 weeks

12.8

29 34 weeks

17

43.6

35 36 weeks

10.3

Alterations seen in laboratory tests for HELLP syndrome

Hemolysis

14

34.1

Low platelet count

19.5

Elevated liver enzymes

7.3

Hemolysis + Low platelet count

17.1

Hemolysis + Elevated liver enzymes

12.2

Low platelet count + Elevated liver enzymes

9.8

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So Paulo Medical Journal - Revista Paulista de Medicina

women (19.5%) only had low platelet count,

4 (9.8%) had low platelet count and elevated
liver enzymes. Elevated liver enzymes alone was
observed in 3 patients (7.3%) (Table 2).
There was a significant difference in the
length of time spent in hospital between the
groups (greater than or less than four days).
Thirty-six women (87.8%) with PHS and 202
of the hypertension group (74.0%) stayed in
hospital for at least four days (Table 3).
There was no difference in the incidence
of abruptio placentae, imminent eclampsia
and maternal death. Eclampsia was more frequent in the PHS group (14.6%) than in the
hypertension group (5.8%) (Table 3), with a
significant difference between the two groups.
The mode of delivery is shown in Table
3. The overall cesarean delivery rate was significantly higher in the PHS group (90.2%)
than in the group with normal laboratory values for HELLP syndrome (77.6%).
Despite the incidence of preterm delivery
being higher in the PHS group (70.7%) than

in the hypertension group (57.7%), and the

incidence of stillbirths being higher in the hypertension group (5.1%) than in the PHS
group (0.0%), no statistically significant difference was observed. There were no differences in the incidence of intrauterine growth
restriction and neonatal death (Table 4).

DISCUSSION

Although the term HELLP syndrome was

not coined until 1982,1 its pathological features have been recognized for at least 100
years.26 However, controversies persist regarding the diagnosis, management, and prognosis of this enigmatic disease. This uncertainty
exists partly because its pathophysiological
mechanism remains obscure and partly because of disagreement about the criteria used
to define this syndrome.
Sibai2 defined standardized strict laboratory criteria for disease diagnosis, which have
been used in this study to define the group of

Table 3. Distribution of women with partial HELLP syndrome (hemolysis, elevated

liver enzymes and low platelets) and with only hypertension, according to time elapsed
to discharge from hospital, maternal complications (abruptio placentae, imminent
eclampsia, eclampsia, maternal death) and mode of delivery
Partial HELLP
Syndrome Group
N
%

Hypertension

p - value

Group
N

Time elapsed to discharge from hospital

< 4 days
5
4 days
36

12.2
87.8

72
205

26.0
74.0

0.036
-

Maternal complications
Imminent eclampsia
Eclampsia
Abruptio placentae
Maternal death

18
6
0
0

43.9
14.6
0.0
0.0

95
16
13
1

34.9
5.8
4.7
0.4

0.153
0.048
-

Mode of delivery
Vaginal
Cesarean

4
37

9.8
90.2

62
215

22.4
77.6

0.042
-

Table 4. Distribution of women with partial HELLP syndrome (hemolysis, elevated

liver enzymes and low platelets) and with only hypertension, according to incidence of
preterm delivery, stillborn, neonatal death and intrauterine growth restriction
Partial HELLP
Syndrome Group
N
%

Hypertension*

p - value

Group*
N

Preterm delivery

29

70.7

158

57.7

Term delivery

12

29.3

116

42.3

Neonatal death

7.3

24

8.8

Stillbirth

0.0

14

5.1

Birth live

38

92.7

236

86.1

Intrauterine growth restriction

11

26.8

75

27.4

* Three post-delivery women without information about childbirth.

0.760
0.309
0.897

women with HELLP syndrome. Other, previous authors used less strict criteria, consequently including in their studies women who
we would have considered to have only partial HELLP syndrome.
HELLP syndrome or PHS can be diagnosed during pregnancy or after delivery in
women whose blood pressure elevation was
first detected after mid-pregnancy, either with
or without proteinuria. Despite many authors having shown that HELLP syndrome
is a complication of preeclampsia or eclampsia, Sibai2 and Martin et al.23 observed that
hypertension and proteinuria may be absent
or only slight. Even though HELLP syndrome is considered to be a variant or an
atypical variant form of severe preeclampsia,
its severity is reflected in its laboratory parameters, and not in the usual clinical parameters of blood pressure and proteinuria
that typically reflect preeclampsia disease severity.27 We observed that 48.7% of women
did not have proteinuria. It confirms the idea
that PHS can occur among women with gestational hypertension or gestational hypertension superimposed upon chronic hypertension. Thus, some of these patients may
have a variety of signs and symptoms, none
of which are diagnostic of classic severe
preeclampsia.
PHS can progress to HELLP syndrome
because the alterations seen in laboratory tests
may take place after different elapsed times.20
Audibert et al.15 did not observe disseminated
intravascular coagulation or other maternal
and perinatal complications among women
with PHS or severe preeclampsia. This information suggests that women with PHS have
some complications but they are not as severe
as in HELLP syndrome. It emphasizes the
importance of recognizing HELLP syndrome
as a distinct entity that is associated with serious maternal morbidity.
We believe that the management of women
with PHS must be different from the management of women with severe preeclampsia or
HELLP syndrome. This may be achieved by
clinical management and it may not be necessary to interrupt the pregnancy, since the maternal and perinatal outcomes among women
with PHS did not exhibit any differences in
comparison with women with severe gestational
hypertension or preeclampsia, except for the
incidence of eclampsia.
Preeclampsia increases the cesarean rate,
which ranges from 29.6 to 55.0%,28-32 and this
incidence is always significantly higher than the
incidence of cesareans among healthy pregnant
women or pregnant women with isolated

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So Paulo Medical Journal - Revista Paulista de Medicina

183

chronic hypertension. The cesarean rate among

pregnant women with hypertension is very high
in Brazil. This rate can reach 76.7%,33-35 and it
is similar to the incidence in the hypertension
group of our study (77.6%).
The cesarean rate in the PHS group was
very high, because when the disease was diagnosed we opted for the interruption of the
pregnancy, so as to avoid evolution from PHS
to HELLP syndrome and worsening of the
maternal and perinatal outcomes. Audibert et
al.15 and Abramovici et al.22 showed elevated
cesarean rates among women with PHS, 36%
and 54% respectively, but these rates were
lower than the rate in the PHS group in our

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study (90.3%). This means that we should not

indicate immediate delivery by cesarean section for almost all women with PHS, but try
to encourage the conservative management of
these patients.
Gestational hypertension and preeclampsia must be diagnosed as soon as possible, so as to get the best maternal and perinatal outcomes. Consequently, it is recommended that all pregnant or post-delivery
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12. Brazy JE, Grimm JK, Little VA. Neonatal manifestations of severe maternal hypertension occurring before the thirty-sixth
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13. van Pampus MG, Wolf H, Westenberg SM, van der Post JA,
Bonsel GJ, Treffers PE. Maternal and perinatal outcome after
expectant management of the HELLP syndrome compared with
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Reprod Biol 1998;76:31-6.
14. Aarnoudse JG, Houthoff HJ, Weits J, Vellenga E, Huisjes HJ.
A syndrome of liver damage and intravascular coagulation in
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16. Roberts WE, Perry KG, Woods JB, Files JC, Blake PG, Martin
JN. The intrapartum platelet count in patients with HELLP
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17. Takiuti NH, Kahhale S, Carrara W, Alves EA, Zugaib M.
Sndrome HELLP Resultados materno-fetais. Rev Latinam
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EB, Mesquita C. HELLP sndrome. GO Atual 1997;10:20-9.
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CONCLUSION

HELLP syndrome in pregnant or postdelivery women with gestational hypertension or preeclampsia needs to be diagnosed
as early as possible. But in cases with a diagnosis of partial HELLP syndrome, we observed that aggressive procedures had been
adopted. These resulted in immediate interruption of pregnancy, with elevated
cesarean rates and preterm delivery. Such
decisions need to be reviewed and a management strategy of monitoring could be
attempted, in order to improve perinatal and
maternal outcomes.

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184

Publishing
information

Joelcio Francisco Abbade, MD. Disciplina de Obstetrcia,

Departamento de Ginecologia e Obstetrcia, Faculdade de
Medicina de Botucatu, Universidade Estadual Paulista (Unesp)
Jlio de Mesquita Filho, Botucatu, So Paulo, Brazil.
Jos Carlos Peraoli, MD. Disciplina de Obstetrcia,
Departmento de Ginecologia e Obstetrcia, Faculdade de
Medicina de Botucatu, Universidade Estadual Paulista (Unesp)
Jlio de Mesquita Filho, Botucatu, So Paulo, Brazil.
Roberto Antonio Arajo Costa, MD. Disciplina de
Obstetrcia, Departamento de Ginecologia e Obstetrcia,
Faculdade de Medicina de Botucatu, Universidade Estadual
Paulista (Unesp) Julio de Mesquita Filho, Botucatu, Brazil.
Iracema de Mattos Paranhos Calderon, MD.
Disciplina de Obstetrcia, Departamento de Ginecologia e
Obstetrcia, Faculdade de Medicina de Botucatu,
Universidade Estadual Paulista (Unesp) Julio de Mesquita
Filho, Botucatu, So Paulo, Brazil.
Vera Therezinha Medeiros Borges, MD. Disciplina de
Obstetrcia, Departamento de Ginecologia e Obstetrcia,
Faculdade de Medicina de Botucatu, Universidade Estadual
Paulista (Unesp) Julio de Mesquita Filho, Botucatu, So
Paulo, Brazil.
Marilza Vieira Cunha Rudge, MD. Disciplina de
Obstetrcia, Departamento de Ginecologia e Obstetrcia,
Faculdade de Medicina de Botucatu, Universidade Estadual
Paulista (Unesp) Julio de Mesquita Filho, Botucatu, So
Paulo, Brazil.

Conflict of interest: Not declared

Sources of funding: Not declared
Date of first submission: December 20, 2001
Last received: May 27, 2002
Accepted: June 27, 2002
Address for correspondence
Departamento de Ginecologia e Obstetrcia
Faculdade de Medicina de Botucatu, Universidade
Estadual Paulista
Caixa Postal 530
Botucatu/SP - Brasil - CEP 18618-970
Tel. (+55 14) 6802-6227
E-mail: [email protected]

So Paulo Medical Journal - Revista Paulista de Medicina

CONTEXTO: A sndrome HELLP uma grave

complicao da gestao caracterizada por
hemlise, elevao das enzimas hepticas e
plaquetopenia. Algumas gestantes desenvolvem
somente uma ou duas dessas caractersticas da
sndrome HELLP. Esse quadro denominado
de sndrome HELLP parcial (SHP).
OBJETIVO: O objetivo deste estudo foi avaliar
as repercusses maternas e perinatais das
mulheres que desenvolveram SHP e comparar os resultados com mulheres que tiveram
hipertenso gestacional ou pr-eclmpsia sem
alteraes dos exames laboratoriais para
sndrome HELLP.
TIPO DE ESTUDO: Observacional, retrospectivo e analtico.
LOCAL: Maternidade do Hospital das Clnicas
da Faculdade de Medicina de Botucatu, Universidade Estadual Paulista, Botucatu, So
Paulo, Brasil.
AMOSTRA: Foram selecionadas gestantes ou
purperas que tiveram elevao dos nveis
pressricos detectada pela primeira vez aps
a primeira metade da gestao com ou sem
proteinria entre janeiro/1990 a dezembro/
1995. As mulheres foram divididas em dois
grupos: Grupo SHP quando as mulheres
com hipertenso arterial tinham pelo menos
uma, mas no todas as alteraes de exames
que demonstravam hemlise, elevao das
enzimas hepticas ou plaquetopenia e Grupo Hipertensas pacientes com hipertenso

RESUMO

sem alteraes nos exames laboratoriais para

sndrome HELLP.
PRINCIPAIS VARIVEIS: Analisamos idade
materna, raa, paridade, classificao da hipertenso, idade gestacional no diagnstico
da SHP, alteraes nos exames laboratoriais
para sndrome HELLP, tempo de permanncia no hospital, complicaes maternas,
via de parto, incidncia de prematuridade,
restrio de crescimento intra-uterino,
natimortos e neomortos.
RESULTADOS: 318 mulheres foram selecionadas,
das quais 41 (12,9%) tiveram SHP e 277
(87,1%) no desenvolveram alteraes dos exames laboratoriais que compem o diagnstico
da sndrome HELLP. A pr-eclmpsia foi um
tipo de hipertenso mais freqente no grupo
SHP que no grupo hipertensas. No houve
pacientes com hipertenso crnica isolada que
desenvolveram SHP. A taxa de cesrea,
eclmpsia e de partos prematuros foi significativamente mais freqente no grupo SHP que
no grupo hipertensas.
CONCLUSO: Observamos uma conduta agressiva nas pacientes com SHP, que resultou na
interrupo imediata da gestao, com elevada taxa de cesrea e de recm-nascido prtermo. Esta conduta deve ser revista para a
reduo desses ndices.
PALAVRAS CHAVES: Sndrome HELLP.
Sndrome HELLP parcial. Pr-eclmpsia.
Resultados maternos. Resultados perinatais.

COPYRIGHT2002, Associao Paulista de Medicina

Sao Paulo Med J/Rev Paul Med 2002; 120(6):180-4.