Lupus (2016) 0, 1–6

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PAPER

Active haematological manifestations of systemic lupus

erythematosus lupus are associated with a high rate
of in-hospital mortality
D Miranda-Hernández1, C Cruz-Reyes1, C Monsebaiz-Mora2, E Gómez-Bañuelos3, U Ángeles4, LJ Jara5 and
MÁ Saavedra1
1
Rheumatology Department, Hospital de Especialidades Dr Antonio Fraga Mouret, Mexico City, Mexico; 2Hospital General Regional No. 1,
Charo, Mexico; 3Instituto de Investigación en Reumatologı́a y del Sistema Músculo-esquelético, Universidad de Guadalajara, Guadalajara,
Mexico; 4Direction of Epidemiology, Hospital de Especialidades Dr Antonio Fraga Mouret, Mexico City, Mexico; and 5Direction of Education
and Research, Hospital de Especialidades Dr Antonio Fraga Mouret, Mexico City, Mexico

The aim of this study was to estimate the impact of the haematological manifestations of
systemic lupus erythematosus (SLE) on mortality in hospitalized patients. For that purpose
a case–control study of hospitalized patients in a medical referral centre from January 2009 to
December 2014 was performed. For analysis, patients hospitalized for any haematological
activity of SLE (n ¼ 103) were compared with patients hospitalized for other manifestations of
SLE activity or complications of treatment (n ¼ 206). Taking as a variable outcome hospital
death, an analysis of potential associated factors was performed. The most common haem-
atological manifestation was thrombocytopenia (63.1%), followed by haemolytic anaemia
(30%) and neutropenia (25.2%). In the group of haematological manifestations, 17 (16.5%)
deaths were observed compared to 10 (4.8%) deaths in the control group (P < 0.001). The
causes of death were similar in both groups. In the analysis of the variables, it was found that
only haematological manifestations were associated with intra-hospital death (odds ratio 3.87,
95% confidence interval 1.8–88, P < 0.001). Our study suggests that apparently any manifest-
ation of haematological activity of SLE is associated with poor prognosis and contributes to
increased hospital mortality. Lupus (2016) 0, 1–6.

Key words: Systemic lupus erythematosus; thrombocytopenia; haemolytic anaemia; neutro-

penia; mortality

Introduction haematological abnormalities are leukopenia/lym-

phopenia (86%), thrombocytopenia (7–30%),
Systemic lupus erythematosus (SLE) is a multisys- autoimmune haemolytic anaemia (5–28%) and
tem autoimmune disease characterized by a diver- Fisher–Evans syndrome (3%).3–5
sity of clinical manifestations, high production of It has recently been reported that haematological
autoantibodies, circulating immune complexes and manifestations can predict the course of the dis-
extensive tissue damage.1 Haematological manifest- ease,6 they can also be predictors of mortality;7
ations of SLE are a hallmark of the disease, often they have been associated with early death,8 in-
being the initial manifestation, and generally they hospital death9,10 and reduced survival.11 The clin-
have a good prognosis.2 Haematological manifest- ical course of SLE is highly variable with frequent
ations are usually associated with SLE activity, relapses, and the increased risk of mortality is
which seems to reflect the pro-inflammatory effect mainly due to infections, kidney disease, central
on the function of the bone marrow and the sur- nervous system activity and accelerated atheroscler-
vival of peripheral blood cells.2 The most common osis.12 However, considering that the haemato-
logical manifestations can predict the course
of disease and that they are associated with
Correspondence to: Miguel Á Saavedra, s/n, Col. La Raza, Del
Azcapotzalco, 02990, Mexico City, Mexico.
increased mortality, we decided to estimate its
Email: miansaavsa@gmail.com impact on hospitalized patients with SLE in a refer-
Received 14 April 2016; accepted 8 September 2016 ral hospital.
! The Author(s), 2016. Reprints and permissions: http://www.sagepub.co.uk/journalsPermissions.nav 10.1177/0961203316672926

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 Active haematological manifestations and SLE mortality
D Miranda-Hernández et al.
2
Patients and methods
A case–control study of patients with SLE hospita-
lized in the department of rheumatology of a refer-
ral centre was conducted. Patients included in the
study were admitted from January 2009 to
December 2014. All patients met the updated
American College of Rheumatology (ACR) criteria
for SLE 1997;13 patients with associated antipho-
spholipid syndrome (APS) and met the modified
Sydney 2006 criteria.14 Our study was approved
by the local research ethics committee. The infor-
mation was obtained according to the registration
of first hospital admission for each patient. Patients
with haematological lupus (cases) were considered
only if they presented with some haematological
manifestation, or a combination of them, attributed
to disease activity when they were admitted accord-
ing to the following definitions: platelets less than
100,000 K/mL, haemolytic anaemia with haemoglo-
bin less than 10 g/dL (in the presence of elevated
lactic dehydrogenase and reticulocytes) and neutro-
penia less than 1000 K/mL. The haematological
activity was considered severe if the values of plate-
lets less than under 30,000 K/mL, haemolytic anae-
mia with haemoglobin less than 7 g/dL, and
neutrophils less than 500 K/mL at patient admis-
sion. Two patients hospitalized in the same period
of study without any haematological manifestation
for each case were included as controls. Patients
whose haematological manifestations were attribu-
ted to drug toxicity and those patients admitted
electively, e.g., for performing renal biopsy, were
excluded.
Clinical variables analyzed were age, gender, dur-
ation of the disease, type and number of organs
involved, cause of hospital admission (relapse or
complication of SLE activity), disease activity
(assessed by the Systemic Lupus Erythematosus
Disease Activity Index (SLEDAI)) and the presence
of associated APS. Immunological variables
included in the analysis were antinuclear antibodies
(ANA, determined by indirect immunofluores-
cence), serum complement C3 and C4 (determined
by nephelometry), anti-dsDNA antibodies (anti-
DNA), anti-Ro/SSA, anti-La/SSB, anti-Sm, anti-
RNP and anti-cardiolipin antibodies (aCL) IgG
and IgM isotype (determined by ELISA), which
were determined before or during hospitalization.
Statistical analysis
Descriptive statistics included quantitative
variables expressed in standard deviation, and
qualitative variables expressed in percentages.
Lupus
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We performed a bivariate analysis using the chi
square test or Student’s t test when they were
required. The odds ratio (OR) was calculated with
a confidence interval (CI) of 95%, using hospital
mortality as an outcome measure logistic regression
model using SPSS V.17 software (SPSS Inc.,
Chicago, IL, USA). A value of P < 0.05 was con-
sidered statistically significant.
Results
Characteristics of patients
A total of 309 patients with SLE were included in the
study, 103 with haematological manifestations and
206 without them. In both groups the majority were
women, the mean age and time of evolution of dis-
ease were also similar (Table 1). A greater propor-
tion of patients in the group with haematological
manifestations were admitted to hospital for relapse
of the disease (23.4% vs. 18.9%, P ¼ 0.03). A greater
proportion of patients in the control group had pre-
existing lupus nephritis (37.8% vs. 54.3%, P < 0.01)
and central nervous system involvement (3.8% vs.
11.1%, P < 0.01), compared to those patients
admitted for haematological activity. In addition,
patients with haematological manifestations had
significantly lower levels of serum complement C4
(9.5  6.5 vs. 11.2  6.6, P ¼ 0.01), and a higher fre-
quency of positive aCL IgM (33.3% vs. 20.1%,
P ¼ 0.03) compared with those patients without
haematological manifestations (Table 2). There
were no differences in serum levels of C3, titres of
anti-dsDNA or SLEDAI score at hospital admis-
sion in both groups (Table 2). The major causes
for hospitalization in patients without haemato-
logical manifestations were active lupus (52.4%),
infections (18.4%), drug toxicity (7.2%) and throm-
bosis (6.7%).
Haematological manifestations
The cell line most frequently affected in patients
with haematological manifestations was thrombo-
cytopenia in 65 cases (63.1%), followed by haemo-
lytic anaemia in 31 cases (30%) and neutropenia in
26 cases (25.2%). The mean value of platelets on
admission of patients was 19,296  17,564 K/mL,
haemoglobin of 5.72  1.57 g/dL and neutrophils
751  324 K/mL. Fifty-eight per cent of patients
with thrombocytopenia, 83% with haemolytic
anaemia and 38.4% with neutropenia filled the def-
inition for a severe case. In 19 of the patients stu-
died, more than one cell line involved was found,
 Active haematological manifestations and SLE mortality
D Miranda-Hernández et al.
3

Table 1 Characteristics of patients on admission to hospital. seven of them had Fisher–Evans syndrome, 10 had
Cases Controls
leukopenia plus thrombocytopenia and one had
(n ¼ 103) (n ¼ 206) P value pancytopenia. A higher proportion of patients
with haematological manifestations were treated
Age, mean (SD) 32.7  13.5 31.8  11.6 0.02b with pulses of glucocorticoids (55.3% vs. 38%,
Female, n (%) 87 (84.4) 80 (87.3) 0.48a
Duration of SLE, months 61  84.6 68  72.2 0.14b
P ¼ 0.01), and/or intravenous immunoglobulin
mean (SD) (18.4% vs. 5.5%, P ¼ 0.005) compared with those
Previous organ involved control patients admitted for active SLE other than
Blood, n (%) 12 (11.6) 9 (4.3) 0.02a haematological activity (n ¼ 108).
Kidney, n (%) 39 (37.8) 112 (54.3) 0.007a
Nervous system, n (%) 4 (3.8) 23 (11.1) 0.03a
Skin/joint, n (%) 35 (33.9) 31 (15) 0.0002a
Hospital mortality
Gastrointestinal, n (%) 1 (0.9) 2 (0.9) 1.0a
From the total number of patients, 27 (8.7%) hos-
Serosa, n (%) 1 (0.9) 3 (1.4) 1.0a
Lung, n (%) 0 (0) 4 (1.9) 0.3a
pital deaths occurred, 17 of which (16.5%)
Previous treatment occurred in patients with haematological disease
Cytotoxic drug, n (%) 11 (10.6) 32 (16) 0.29a and 10 (4.8%) in patients without it (P < 0.001)
Cytotoxic/GC, n (%) 36 (34.9) 89 (44.5) 0.17a (Table 3). The causes of death in patients with
Cytotoxic/GC/antimalarial, n 23 (22.3) 36 (18) 0.35a
(%)
haematological manifestations were active nephritis
Only GC, n (%) 6 (5.8) 20 (10) 0.28a lupus (n ¼ 1), gastrointestinal bleeding (n ¼ 1), cere-
No treatment, n (%) 27 (26.2) 23 (11.5) 0.001a bral haemorrhage (n ¼ 3), pulmonary haemorrhage
Relapse to hospitalization, n 24 (23.4) 39 (18.4) 0.03a (n ¼ 3), severe pre-eclampsia (n ¼ 1) and severe
(%)
infections (n ¼ 8) (pneumonia in five cases and
Antiphospholipid syndrome, 12 (11.6) 29 (14.0) 0.67a
n (%) septicemia in three cases). The causes of death in
SLEDAI, mean (SD) 10  6.8 9.4  7.2 0.54b the control group were gastrointestinal bleeding
a (n ¼ 1), cerebral haemorrhage (n ¼ 1), diffuse alveo-
Fisher exact test.
b
Student’s t test.
lar haemorrhage (n ¼ 2), active lupus nephritis
SLE: systemic lupus erythematosus; GC: glucocorticoid; SLEDAI: (n ¼ 1) and severe infections (n ¼ 5) (septicemia in
Systemic Lupus Erythematosus Disease Activity Index. four cases and neuroinfection in another case).

Analysis of variables
In the analysis of the variables potentially asso-
ciated with hospital mortality, the presence of
haematological activity was the only variable asso-
Table 2 Immunological studies of hospitalized patients ciated with mortality (OR 3.87, 95% CI 1.8–88,
Cases Controls
(n ¼ 103) (n ¼ 206) P value
Table 3 Analysis of the variables potentially associated with
C3 (mg/dL), mean (SD) 57  35.6 62.6  31.7 0.13b
hospital mortality
C4 (mg/dL), mean (SD) 9.5  6.5 11.2  6.6 0.01b
Low C3, n (%) 76 (74.5) 140 (71.4) 0.57a Variable OR 95% CI P value
Low C4, n (%) 69 (67.6) 116 (59.5) 0.17a
Positive ANA (homogenous pattern), 49 (53.2) 103 (59.5) 0.33a Women 1.12 0.37–3.4 0.77
n (%) AAN (homogenous pattern) 0.72 0.31–1.7 0.45
b
Anti-DNA antibodies, mean (SD) 674  694 636  671 0.35 Low C3 0.64 0.23–1.8 0.38
Positive anti-DNA antibodies, 59 (63.4) 119 (62.6) 0.9a Low C4 0.71 0.3–1.7 0.45
n (%) Positive anti-DNA antibodies 0.88 0.38–2.1 0.76
Positive anti-Sm antibodies, n (%) 23 (38.9) 37 (32.1) 0.37a Anti-Sm antibodies 0.95 0.31–2.9 0.93
Positive anti-Ro/SSA antibodies, n 24 (39.3) 38 (33.0) 0.41a Anti-Ro antibodies 0.14 0.1–1.1 0.04
(%)
Anti-La antibodies 0.94 0.12–7.9 1
Positive anti-La/SSB antibodies, n 5 (10.8) 8 (6.9) 0.52a
Anti-RNP antibodies 0.42 0.13–1.4 0.14
(%)
ACL IgG antibodies 0.31 0.04–2.4 0.33
Positive anti-RNP antibodies, 30 (40.1) 51 (44.3) 0.81a
n (%) ACL IgM antibodies 1.7 0.64–4.5 0.29
Anticardiolipin antibodies IgG, n 16 (19.0) 15 (16.6) 0.08a Relapse to hospitalization 0.97 0.38–2.5 0.94
(%) Antiphospholipid syndrome 1 0.33–3.1 1
Anticardiolipin antibodies IgM, n 28 (33.3) 28 (20.1) 0.03a Any haemocytopenia 3.87 1.7–8.8 0.001
(%) Thrombocytopenia 2.80 0.97–8.1 0.51
Haemolytic anaemia 0.67 0.20–2.25 0.52
a
Fisher’s exact test. Neutropenia 1.30 0.4–4.9 0.76
b
Student’s t test.

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 Active haematological manifestations and SLE mortality
D Miranda-Hernández et al.
4
P < 0.001) (Table 3). Gender, the presence of APS,
hypocomplementemia or autoantibodies were not
associated with mortality. Similarly, no haemato-
logical manifestation individually included in the
analysis was directly associated with mortality,
although thrombocytopenia showed no statistically
significant elevated risk. Neither did it influence the
severity of the haematological condition.
Discussion
Our study showed that SLE patients admitted for
any manifestation of haematological activity had
an increased risk of hospital death (OR 3.8, 95%
CI 1.1–8.8, P ¼ 0.001), mainly those with thrombo-
cytopenia compared to those patients admitted
for other manifestations of SLE activity or
complications.
The survival of patients with SLE has remark-
ably improved in recent decades. In 1955 the esti-
mated survival was less than 50% at 5 years; then,
in 1995 it was reported that the estimated survival
rate was 85% at 10 years and 75% at 20 years.15 In
the Canadian population, a decline has been
reported in standardized mortality rates in patients
with SLE, 12.6 (95% CI 9.13–17.39) in the 1970s to
3.46 (95% CI 2.71–4.40) at the beginning of the
2000s.16 The improved survival of patients with
SLE can be attributed to a number of factors
such as early diagnosis of kidney disease, better
serological surveillance, a more sensible use of cor-
ticosteroids and cytotoxic agents, availability of
advanced therapies for renal replacement and
better management of complications such as infec-
tions, hyperlipidemia and hypertension. Despite the
reduction in mortality, there is a significant risk of
estimated death of more than three times within the
general population, resulting in the loss of 14.2
years of life span.16 The causes of death in SLE
patients can be divided into those related to the
disease (activity, organ damage, accelerated athero-
sclerosis), treatment-related (which is intense and
toxic) and those not related to the disease (infec-
tions and neoplasms).17,18
Several predictors of mortality have been identi-
fied in patients with SLE, such as age of onset,
ethnicity, disease activity, renal disease, neuro-
psychiatric lupus and, especially certain haemato-
logical manifestations of the disease, including
anaemia, and thrombocytopenia.7,18 The results of
our study are in line with these previous reports.
Much of the mortality in the first 5 years of
the disease can be attributed to lupus activity.
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In several cohorts of patients with SLE, sociodemo-
graphic factors associated with premature death
have been identified, such as early or advanced
age, Hispanic and Asian ethnic groups, male
gender and low socioeconomic status. In addition,
various factors which reflect the organ damage that
influences survival, such as renal and cardiovascu-
lar disease, premature atherosclerosis (accelerated
atherosclerosis, coronary artery disease, cerebro-
vascular disease and stroke), vasculitis, elevated
serum creatinine, and elevated levels of activity in
chronic renal biopsy, low serum complement, and
haemocytopenias, have been linked to early
death.19,20
The pathophysiological mechanisms of haemato-
logical manifestations of SLE are not fully known.
For thrombocytopenia, at least three mechanisms
are known: impaired production of platelets in the
bone marrow, sequestration of platelets in the
spleen or accelerated destruction of platelets in
the peripheral circulation. Most SLE patients with
thrombocytopenia have an increased peripheral
destruction that is commonly mediated by antipla-
telet antibodies (serum platelet-binding IgG and
platelet-associated IgG), and in some subgroups
of patients with SLE, the presence of aPL antibo-
dies appear to be involved.21 Thus, thrombocyto-
penia in SLE may be caused in some instances by a
more complex interaction between aPL antibodies
and platelet-antigen antibodies. Early suspicion of
macrophage activation syndrome, a potentially
fatal entity, is another cause of thrombocytopenia
in connective tissue diseases, including SLE.21
Haemolytic anaemia in patients with SLE can
be explained by various mechanisms, such as anti-
erythrocyte antibodies which are mainly warm-type
IgG, and aPL antibodies (especially aCL antibo-
dies, IgG and IgM) that are commonly associated
with Coombs-positive haemolytic anaemia.
Moreover, underexpression of CD55 and CD59
has been shown on erythrocytes of patients with
SLE-associated haemolytic anaemia. These
membrane proteins serve as protection against
complement-induced cell lysis; consequently, the
underexpression of CD55 and CD59 can be asso-
ciated with autoimmune haemolysis.21
Hospitalized patients with disease activity repre-
sent a particularly susceptible group of high mor-
tality. In patients admitted to our hospital, age,
gender and the duration of the disease did not
differ between groups. In both groups, the most
prevalent organ involved was the kidney, and
they were treated primarily with immunosuppres-
sants and glucocorticoids. Patients with haemato-
logical activity had lower levels of complement C4,

and relapse was the main reason for hospitalization
compared with patients without haematological
activity. A retrospective study in a Mexican popu-
lation evaluated factors associated with mortality in
SLE patients who were hospitalized for the first
time by severe and acute activity of the disease
(lupus nephritis, severe thrombocytopenia
(<20,000 K/mL), lung, neuropsychiatric, gastro-
intestinal, cardiovascular, and systemic vasculitis).
The authors found that kidney function and
thrombocytopenia in addition to the infection
were factors associated with death.9 These factors,
which reflect disease activity, have also been asso-
ciated with poor prognosis in other racial groups
such as Asians and Africans.10,22 The severity of
thrombocytopenia in SLE patients can be a useful
independent prognostic factor to predict survival.
Moreover, complete remission of thrombocyto-
penia after treatment is an important prognostic
factor. The severity of thrombocytopenia and
response to treatment should be closely monitored
to predict prognosis in SLE patients.23,24 In add-
ition, the presence of haemolytic anaemia in the
first year after disease diagnosis or during the
follow-up period increased the risk of death.25
Recently, the Latin Lupus Study Group
(GLADEL) also found that haemolytic anaemia
contributes independently to damage accrual and
diminished survival in SLE patients.26
Our study has some limitations. These include the
retrospective study design, but this collected all the
information needed for the analysis of the patients.
On the other hand, it is a highly selected population
of hospitalized patients; however, it is unlikely that
other patients were treated on an outpatient basis. In
conclusion, our study suggests that any active haem-
atological manifestation in hospitalized patients with
SLE may be a factor of poor prognosis, which can
contribute to early mortality. Therefore, these mani-
festations should be timely and intensively treated
for a faster control of the disease.
Declaration of conflicting interests
The authors declared no potential conflicts of inter-
est with respect to the research, authorship, and/or
publication of this article.
Funding
The authors received no financial support for the
research, authorship, and/or publication of this
article.
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Active haematological manifestations and SLE mortality
D Miranda-Hernández et al.
5
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