Review Article
The effect of hyperthyroidism on procoagulant, anticoagulant and
fibrinolytic factors
A systematic review and meta-analysis
Danka J. F. Stuijver
1,2
; Bregje van Zaane
1,2
; Erica Romualdi
3
; Dees P. M. Brandjes
1,2
; Victor E. A. Gerdes
1,2
; Alessandro Squizzato
3
1
Department of Internal Medicine, Slotervaart Hospital, Amsterdam, the Netherlands;
2
Department of Vascular Medicine, Academic Medical Center, Amsterdam, the Netherlands;
3
Department of Clinical Medicine, University of Insubria, Varese, Italy
Summary
Several coagulation and fibrinolytic parameters appear to be affected
by thyroid hormone excess; however, the net effect on the haemostatic
system remains unclear. We aimed to update our previous review and
systematically summarise and meta-analyse the data by assessing the
effects of thyrotoxicosis on the coagulation and fibrinolytic system in
vivo. Data sources included MEDLINE (2006–2012), EMBASE
(2006–2012), and reference lists. The sources were combined with our
previous search containing studies from 1980–2006. Eligible studies
were all observational or experimental studies. Two investigators inde-
pendently extracted data and rated study quality. Weighted mean pro-
portion and 95% confidence intervals were calculated and pooled
using a fixed and a random-effects model. A total of 29 articles consist-
ing of 51 studies were included, as in several articles more than one
study was described. We included four intervention (before and after
Correspondence to:
Danka J. F. Stuijver
Department of Internal Medicine
Slotervaart Hospital
Louwesweg 6, Amsterdam
1066 EC, The Netherlands
Tel.: +31 20 5125194, Fax: +31 20 5124783
E-mail: d.j.stuijver@amc.uva.nl
treatment in hyperthyroid patients), five cross-sectional (hyperthyroid
subjects and euthyroid controls), and four experimental (before and
after use of thyroid hormone in euthyroid subjects) medium/high
quality studies for meta-analysis. We found that thyrotoxicosis shifts
the haemostatic balance towards a hypercoagulable and hypofibrino-
lytic state with a rise in factors VIII and IX, fibrinogen, von Willebrand
factor, and plasminogen activator inhibitor-1. This was observed in en-
dogenous and exogenous thyrotoxicosis, and in subclinical as well as
overt hyperthyroidism. We conclude that both subclinical and overt hy-
perthyroidism induce a prothrombotic state, which is therefore likely to
be a risk factor for venous thrombosis.
Keywords
Thyrotoxicosis, hyperthyroidism, coagulation, fibrinolysis
Received: July 18, 2012
Accepted: August 10, 2012
Prepublished online: September 26, 2012
doi:10.1160/TH12-07-0496
Thromb Haemost 2012; 108: 1077–1088
1077 © Schattauer 2012
Thrombosis and Haemostasis 108.6/2012
Introduction
Hyperthyroidism is associated with a hypercoagulable state (1, 2).
Several coagulation and fibrinolytic parameters appear to be af-
fected by thyrotoxicosis; elevated plasma levels of factor VIII
(FVIII), factor IX (FIX), von Willebrand factor (VWF), and fibri-
nogen, and a reduced fibrinolytic activity due to increased levels of
plasminogen activator inhibitor-1 (PAI-1) have been reported in
both hyperthyroid patients and healthy subjects after taking thy-
roid hormones (1, 3–9). However, in a previous systematic review,
we found the majority of these studies to have major methodologi-
cal flaws (1). This left the net effect of thyroid hormone excess on
the haemostatic system unclear. Moreover, the question as to
whether thyrotoxicosis enhances the risk of venous thrombosis,
and to which extent, still remains controversial.
In this review, we aimed to update our previous systematic re-
view and systematically summarise and meta-analyse the data by
assessing the effects of thyrotoxicosis on the coagulation and fibri-
nolytic system in vivo (1). For the interpretation of the results we
will also discuss the recent studies on the relationship between
(supra) physiological thyroid hormone levels and VTE.
Methods
Study identification
A computer-assisted search of the MEDLINE and EMBASE elec-
tronic databases from July 2006 to March 2012 was performed to
identify published studies that evaluated the effect of thyroid hor-
mone excess on the coagulation-fibrinolytic system. The following
search terms were used for the MEDLINE search: “haemostasis,
blood coagulation tests, blood coagulation, blood coagulation fac-
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