Management of Venous Thrombosis in Pregnancy revised.
qxd 8/5/08 10:52 Page 2
24 Medical problems in pregnancy
Management of venous thrombosis
in pregnancy
SCOTT M. NELSON AND IAN A. GREER
The management of venous thromboembolism in pregnancy is challenging, as many diagnostic tests are less
accurate in pregnant than in non-pregnant patients, and some of the radiological procedures are potentially
hazardous to the fetus. In addition, anticoagulant treatment with coumarins can cause embryopathy. The authors
recommend strategies for women at risk of deep venous thrombosis or pulmonary thromboembolism during
pregnancy and outline appropriate investigations and treatment.
Dr S.M. Nelson, BSc, PhD, MRCOG, Clinician Scientist, Reproductive
and Maternal Medicine, University of Glasgow, Glasgow Royal
Infirmary; Professor I.A. Greer, MD, FRCP(Glas, Edin, Lond), FRCOG,
FRCPI, FMedSci, Dean, Hull York Medical School, University of York.
enous thromboembolism (VTE) remains a major cause
V of maternal mortality and is currently the most com-
mon direct cause of maternal death in the UK, with a
twofold higher prevalence than the next most common
cause, haemorrhage.1 European studies have consistently
calculated the pregnancy-related VTE mortality at 8.5–14
per million live births.2 The UK Confidential enquiries into
maternal deaths has shown that most of these deaths are
associated with substandard care, including a failure to
recognise symptoms in women who already had obvious
risk factors for VTE, delay in diagnosis, delayed or inade-
quate treatment for acute VTE and inadequate thrombo-
prophylaxis.1 Consequently, clinicians need to understand
the implications and clinical management of thromboem-
bolic disease in pregnancy.
Epidemiology of VTE during pregnancy
Virchow’s classic triad for VTE – hypercoagulability, venous
stasis and vascular damage – all occur in the course of
uncomplicated pregnancy and delivery. There are substan-
tial increases in factor VIII and fibrinogen; acquisition of
resistance to activated protein C (aPC) in 40 per cent of
pregnancies; reduction in protein S levels; and impaired
fibrinolysis, all of which may persist for up to six weeks after
birth, irrespective of the gestation at delivery.3 There is also
extensive reduction in venous flow velocity in the lower
limbs in pregnancy, with approximately a 50 per cent reduc-
tion by 25–29 weeks’ gestation, reaching a nadir at 36
weeks.4 Normal non-pregnant flow velocity rates are not
restored until about six weeks after delivery.5 Furthermore,
some degree of vascular endothelial damage or trauma to
pelvic vessels appears inevitable in the course of vaginal or
Trends in Urology Gynaecology & Sexual Health May/June 2008
abdominal delivery. As a result of these prothrombotic
changes, the incidence of VTE increases two- to fourfold
when a woman becomes pregnant, with a risk of
pregnancy-associated VTE of 0.1 per cent,6 and in women
with a previous VTE the risk of recurrence is 2–3 per cent.
Assessment of other independent risk factors that may
be present and predispose to any of the three components
of Virchow’s triad is required, not only before pregnancy,
but also again at the initial confirmation of pregnancy, as
pregnancy progresses and post-delivery (Box 1).7,8
Pre-conceptual counselling and strategies for women at
risk of VTE in pregnancy
All women at significant risk of VTE should ideally be
identified pre-conceptually and made aware of their rela-
tive VTE risk. Although many of the described risk factors
are not modifiable pre-pregnancy, the prothrombotic fac-
tors associated with obesity have been shown to improve
with weight loss, potentially reducing VTE risk.9 Similarly,
stabilisation of medical conditions may also potentially
improve thrombotic risk before embarking on pregnancy.
Pre-conceptually, women need to be informed apropos
the potential necessity for therapy as soon as pregnancy is
achieved because of the rapid alterations in haemostatic
factors. Similarly, it is essential that patients on coumarin
therapy are aware of the requirement to substitute low
molecular weight heparin (LMWH) for coumarin by six
weeks' gestation to avoid the risk of embryopathy.
In addition to pharmacological strategies, graduated
elastic compression stockings may be effective for throm-
boprophylaxis in pregnancy.10 They may act by preventing
overdistension of veins, so preventing endothelial damage
and exposure of subendothelial collagen. They can there-
fore be combined safely with pharmacological thrombo-
prophylaxis, both in the antenatal period and postnatally.
For women with confirmed deep venous thrombosis
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Management of Venous Thrombosis in Pregnancy revised.qxd
26 Medical problems in pregnancy
Box 1. Risk factors for venous thromboembolism in pregnancy.
• Inherited thrombophilia • Infective and inflammatory
• Age over 35 years conditions
• Obesity • Pre-eclampsia
• Operative delivery • Major obstetric haemorrhage
• Prolonged labour • Intravenous drug abuse
• Gross varicose veins • Hyperemesis gravidarum
• Immobility after delivery • Nephrotic syndrome
• Prolonged bed rest • Sickle cell disease
• Air travel • Myeloproliferative disease
• Paraplegia • Ovarian hyperstimulation
• Dehydration • Acquired thrombophilia
(DVT), compression stockings can reduce the risk of post-
thrombotic syndrome if used for up to two years after the
event.10 It is, however, important that correctly fitted class
2 graduated stockings are used, with repeat fittings as
pregnancy progresses.10
Various strategies combining pharmacological and
physical therapies to minimise the risk of primary throm-
bosis and VTE recurrence have been put forward based on
the woman’s past VTE and risk factor history (Table 1).11
Clinical assessment of pregnant women with suspected VTE
By itself, the clinical diagnosis of DVT and pulmonary
thromboembolism (PE) is unreliable (Box 2). In non-
pregnant individuals, DVT is confirmed in about 20–30
per cent of suspected cases.12 In pregnancy, however, leg
symptoms, chest pain and dyspnoea from non-thrombotic
causes are common;13 consequently, the accuracy of clini-
cal diagnosis falls to 8 per cent for DVT and to less than 5
per cent for PE.14
Therefore, it is essential that objective testing is per-
formed expeditiously to avoid the risks, inconvenience
and costs of inappropriate anticoagulation. However,
unlike in the non-pregnant population, where safe and
accurate algorithms are available,15 there are no well-
designed large clinical studies evaluating the accuracy of
objective tests for the diagnosis of DVT or PE in pregnant
patients. Therefore, recommendations for the diagnosis
of DVT or PE during pregnancy are largely empirical and
based on extrapolations from studies performed in non-
pregnant patients.16–18
Venous ultrasound
Ultrasound of the entire proximal venous system is the ini-
tial test for suspected DVT during pregnancy (Figure 1).
Ultrasound is known to have a high diagnostic accuracy in
non-pregnant populations;19 consequently, if the initial
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8/5/08 10:52 Page 4
test shows a clear-cut abnormality in the popliteal or
femoral veins, a diagnosis of proximal DVT is made. A
normal ultrasound does not exclude a calf DVT and, if
normal in spite of a strong clinical suspicion, treatment
should be commenced and the test repeated one week
later to exclude the possibility of extending calf vein
thrombosis and development of a proximal DVT. If the
repeat test is negative, treatment can be discontinued. If
an iliac DVT is suspected because of back pain and
swelling of the whole leg, pulsed Doppler and/or direct
visualisation of the iliac vein is recommended.
Measurement of D-dimer levels
Levels of D-dimers are increased in most patients with
DVT and PE. However, these levels increase with gestation-
al age, during complicated pregnancies, such as those
associated with preterm labour, abruption or gestational
hypertension20 and postpartum.21 These characteristics
reduce the specificity of D-dimers in pregnancy and there-
fore we do not recommend this test, although we accept
that it may be complementary to venous ultrasound in
excluding DVT in pregnancy when both tests are negative.
Radiological investigations
The potential risks with the radiological tests often used
when PE is suspected are minimal when compared with
the consequences of misdiagnosis (Figure 2). If the clinical
features are compatible with PE, a chest X-ray should be
performed. This may identify pulmonary disease such as
pneumonia, pneumothorax or lobar collapse, although
these problems are uncommon in young pregnant women.
While the chest X-ray is normal in more than 50 per cent
of pregnant patients with objectively proven PE, abnormal
features caused by PE include atelectasis, effusion, focal
opacities, regional oligaemia or pulmonary oedema.22
Several studies have evaluated the role of ultrasound of
the lower limb deep veins in non-pregnant patients with
suspected PE.23–26 The rationale is that a diagnosis of DVT
may indirectly confirm the diagnosis of PE, and because
therapy is often the same for both conditions, further inves-
tigation to exclude PE may be unnecessary. Performing
bilateral ultrasound leg studies in pregnant women would
therefore limit the radiation doses given to the mother and
fetus. If the chest X-ray and bilateral ultrasound leg studies
are normal, and PE is suspected, a ventilation/perfusion
(V/Q) lung scan or computerised tomography pulmonary
angiogram (CTPA) should be performed.
In our unit, V/Q lung scans are still the preferred ini-
tial investigation of choice; consequently, if the scan is nor-
mal, the diagnosis of PE is excluded.27 Treatment should
be continued when the lung scan reports a medium prob-
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Management of Venous Thrombosis in Pregnancy revised.qxd
Clinical situation
Single previous VTE (not pregnancy- or ‘pill’-related) associated
with a transient risk factor and no additional current risk factors,
such as obesity
Single previous idiopathic VTE or single previous VTE with
underlying thrombophilia and not on long-term anticoagulant
therapy, or single previous VTE and additional current risk
factor(s) (eg BMI *35)
More than one previous episode of VTE, with no thrombophilia
and not on long-term anticoagulant therapy
Previous episode(s) of VTE in women receiving long-term
anticoagulants (eg with underlying thrombophilia)
Thrombophilia (confirmed laboratory abnormality) but no prior VTE
Risk factors for VTE present antenatally but no previous VTE
or thrombophilia
Following Caesarean section or vaginal delivery
Table 1. Suggested management strategies for various clinical situations. Specialist advice for individualised management of patients is advisable in many of
these situations.11 VTE, Venous thromboembolism; LMWH, low molecular weight heparin; GECS, graduated elastic compression stockings.
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8/5/08 10:52 Page 5
Medical problems in pregnancy 27
Suggested management
Antenatal: surveillance or prophylactic doses of LMWH (eg 40mg
enoxaparin or 5000iu dalteparin daily) ± GECS. Discuss decision
regarding antenatal LMWH with the woman
Postpartum: anticoagulant therapy for at least 6 weeks (eg 40mg
enoxaparin or 5000iu dalteparin daily or warfarin (target INR 2–3)
with LMWH overlap until the INR is *2.0) ± GECS
Antenatal: prophylactic doses of LMWH (eg 40mg enoxaparin or
5000iu dalteparin daily) commenced as soon as pregnancy
diagnosed ± GECS. With antithrombin deficiency there is a strong
case for more intense LMWH therapy (eg enoxaparin 0.5–1mg/kg
12-hourly or dalteparin 50–100iu/kg 12-hourly)
Postpartum: anticoagulant therapy for at least 6 weeks (eg 40mg
enoxaparin or 5000iu dalteparin daily or warfarin (target INR 2–3)
with LMWH overlap until the INR is *2.0) ± GECS
Antenatal: prophylactic doses of LMWH commenced (eg 40mg
enoxaparin or 5000iu dalteparin daily) and fitted with GECS as
soon as pregnancy is diagnosed
Postpartum: anticoagulant therapy for at least 6 weeks (eg 40mg
enoxaparin or 5000iu dalteparin daily or warfarin (target INR 2–3)
with LMWH overlap until the INR is *2.0) and fit GECS
Antenatal: switch from oral anticoagulants to LMWH therapy
(eg enoxaparin 0.5–1mg/kg 12-hourly or dalteparin 50–100iu/kg
12 hourly) by 6 weeks’ gestation and fit GECS
Postpartum: resume long-term anticoagulants with LMWH overlap
until INR in pre-pregnancy therapeutic range and fit GECS
Antenatal: surveillance or prophylactic LMWH ± GECS
Postpartum: anticoagulant therapy for at least 6 weeks (eg 40mg
enoxaparin or 5000iu dalteparin daily or warfarin (target INR 2–3)
with LMWH overlap until the INR is *2.0) and fit GECS
Carry out risk assessment for VTE. If multiple risk factors present,
such as high BMI, immobility and pre-eclampsia, or if single major
risk factor present, such as morbid obesity, consider LMWH
thromboprophylaxis (eg 40mg enoxaparin or 5000iu dalteparin but
dose may need to be increased with extreme levels of BMI) ± GECS
Carry out risk assessment for VTE. If additional risk factors such as
emergency section in labour, age over 35 years, high BMI, etc
present, consider LMWH thromboprophylaxis for 3–5 days
(eg 40mg enoxaparin or 5000iu dalteparin). If multiple risk factors,
GECS should be fitted. Consider need for extended prophylaxis if
significant ongoing risk factors present
Trends in Urology Gynaecology & Sexual Health May/June 2008
Management of Venous Thrombosis in Pregnancy revised.qxd 8/5/08
28 Medical problems in pregnancy
Box 2. Symptoms and signs of deep venous thrombosis and
pulmonary embolism.
Deep venous thrombosis
•Leg pain or discomfort
•Swelling
•Tenderness
•Increased temperature and oedema
•Lower abdominal pain
•Elevated white cell count
Pulmonary embolism
• Dyspnoea
• Collapse
• Chest pain
• Haemoptysis
• Faintness
• Raised jugular venous pressure
• Tachycardia
• Reduced PaO2 and/or PaCO2
• Focal signs in chest
• Abnormalities on X-ray
• Symptoms and signs associated with deep venous thrombosis
ability and consideration given to confirmation by CTPA.
With a high probability result for PE on lung scan, the
diagnosis of PE is confirmed.14 When the lung scan
reports a low risk of PE and leg ultrasound studies are neg-
ative, yet there is a high degree of clinical suspicion, we
would continue anticoagulant treatment, and perform an
alternative test such as CTPA or repeat testing in one week
(V/Q lung scan and leg ultrasound examination).28
With regard to the V/Q lung scan, during pregnancy,
the ventilation component can often be omitted, thereby
minimising the already low radiation dose. CTPA has poten-
tial advantages over radionuclide (V/Q lung) imaging,
including better sensitivity and specificity,29 greater accessi-
bility, with most maternity units in the UK having CTPA
facilities onsite, and an even lower radiation dose to the
fetus. In addition, it can pick up other pathology such as
aortic dissection, but may not identify small peripheral PE.
In spite of these potential advantages, we and others
continue to recommend V/Q lung scanning as the first-
line investigation in pregnancy because of its high nega-
tive predictive value in this situation and its lower radia-
tion dose to the mother’s breast tissue as compared to
CTPA.18 The radiation dose to the mother’s thorax with
CTPA will be around 2 rads and it is known that 1 rad will
increase the lifetime risk of breast cancer by around 14 per
cent.30,31 This is an important consideration when only
around 1 in 20 pregnant women with suspected PE will
have the diagnosis confirmed. Therefore, although CTPA
has rapidly gained acceptance as a robust technique
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10:53 Page 6
among both radiologists and clinicians in non-pregnant
patients, its role in pregnancy is not clearly defined and is
often not addressed in published guidelines.32
A survey of American radiological practice in 2002
revealed CTPA to be the initial imaging technique of
choice in pregnant patients with suspected PE; however,
there was great variation in the standard of practice.33 In
spite of concerns about the potential risks to the fetus,
only 60 per cent of radiologists obtained informed con-
sent before imaging, only 40 per cent altered imaging
parameters in order to reduce radiation dose, and only 17
per cent had a written departmental policy in place.
Recent analysis of UK practice revealed similar lack of
knowledge of fetal dosimetry in the imaging of pregnant
women suspected of having PE.34 In practice, the choice
of diagnostic test for PE will often reflect the availability of
these techniques, but clinicians should be aware of their
relative merits and limitations.
Treatment of VTE during pregnancy
Before anticoagulant treatment is commenced, blood
should be taken for a full thrombophilia screen, a full
blood count and a coagulation screen. Blood should also
be sent for urea, electrolytes and liver function tests, to
exclude renal or hepatic dysfunction, which are cautions
for anticoagulant therapy. Although the results of a throm-
bophilia screen will not influence immediate manage-
ment, they can provide information that can influence the
duration and intensity of anticoagulation, such as when
antithrombin deficiency is identified.7
It is important to be aware of the effects of pregnancy
and thrombus on the results of a thrombophilia screen.
For example, protein S levels fall in normal pregnancy,
making it extremely difficult to make a diagnosis of pro-
tein S deficiency during pregnancy. aPC resistance is
found with the aPC sensitivity ratio test in around 40 per
cent of pregnancies, because of the physiological changes
in the coagulation system. Anticardiolipin antibodies can
also influence the result of the test for aPC resistance.
Antithrombin may be reduced when extensive thrombus
is present.
Other factors can also influence the results of a throm-
bophilia screen. Antithrombin levels are reduced in
nephrotic syndrome (a condition associated with an
increased risk of thrombosis), and protein C and S levels
are reduced in liver disease. Clearly, genotyping for factor V
Leiden and prothrombin G20210A will not be influenced
by pregnancy or current thrombosis. It is therefore impor-
tant that thrombophilia screens are interpreted by clini-
cians with specific expertise in the area; they will need
repeating after anticoagulation therapy has finished.
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Management of Venous Thrombosis in Pregnancy revised.qxd
The anticoagulants that have been evaluated for pre-
vention and treatment of VTE in pregnancy centre on the
use of unfractionated heparin (UFH) or LMWH because
of the fetal hazards of coumarins. Although for many
years UFH was the standard anticoagulant used during
and outwith pregnancy, LMWH has now replaced UFH
for the acute treatment of VTE in pregnancy, with a sys-
tematic review of LMWH in pregnancy confirming its effi-
cacy and safety in the management of acute thrombosis
and provision of thromboprophylaxis.35 Although several
LMWH preparations are available, the extensive pub-
lished experience with enoxaparin and dalteparin and
safety data suggest that these should usually be the first-
choice agents, and we recommend the use of LMWH
throughout pregnancy.
For the acute treatment of VTE, we initiate therapy
with a weight-adjusted dose based on the booking weight
(40–100mg enoxaparin twice daily). The woman should
be taught to self-inject by attending staff, and she can then
be managed as an outpatient until delivery.
As pregnancy progresses (and most women gain
weight), the volume of distribution of LMWH changes.
Therefore three options are available. The first is the
maintenance of the initial dose regimen throughout the
treatment period (six months and therefore usually the
entire pregnancy and postpartum period).
The second option is simply to alter the dose in pro-
portion to weight change; however, the volume of distribu-
tion is not directly related to pregnancy weight gain as
LMWH does not cross the placenta and therefore the
weight of the feto-placental unit is not relevant.
The third option is to measure anti-factor Xa levels
four to six hours after the morning dose; the target thera-
peutic range is 0.4–1.2u/ml for peak levels. If the peak
anti-Xa level is >1.2u/ml, the dose of enoxaparin should
be reduced and peak anti-Xa activity reassessed.
We favour the first approach in most women; however,
in extremes of maternal weight (<50kg or >90kg) or with
other complicating factors putting them at high risk, it can
be useful to ensure that appropriate levels of anticoagula-
tion are being achieved and therefore anti-factor Xa is
measured. If there has been previous exposure to unfrac-
tionated heparin, a platelet count will need to be checked,
ideally every two to three days until day 14, and at regular
intervals thereafter, to exclude heparin-induced thrombo-
cytopenia.36
Management at the time of delivery
For women on therapeutic anticoagulation, induction of
labour facilitates accurate timing of events and minimises
the risk of labour commencing on full anticoagulation.
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Medical problems in pregnancy 29
Suspected (symptomatic)
acute DVT
Consider thrombophilia screen
Start LMWH therapy while
awaiting objective testing
Compression US of
symptomatic leg
Normal and low Normal but high
clinical suspicion clinical suspicion
Continue treatment and repeat
Normal compression US in 1 week DVT present
Continue treatment
Stop
treatment
Figure 1. Diagnostic algorithm for pregnant women with symptoms suggesting acute
deep venous thrombosis (DVT). LMWH, Low molecular weight heparin; US, ultrasound.
We generally recommend induction of labour at 38–39
weeks. The dose of enoxaparin should be reduced to
40mg once daily (thromboprophylactic single dose) on
the day before induction of labour, or, if the thrombosis
was recent, a single dose of 1.5mg/kg in the morning of
the day before planned induction. Although many centres
administer 40mg of enoxaparin on the day of labour, this
prevents the use of regional anaesthetic techniques, which
should not be used until at least 12 hours after the previ-
ous prophylactic dose (40mg) of enoxaparin and 24 hours
after the last dose if still on therapeutic anticoagulation.
After delivery, enoxaparin should not be given for at least
three hours after the epidural catheter has been removed
and the cannula should not be removed within six hours
of the most recent injection. The treatment dose (twice-
daily administration) should be recommenced immedi-
ately following delivery.
For delivery by elective Caesarean section, the woman
should receive either a thromboprophylactic dose of
enoxaparin (40mg once daily) or if the thrombosis was
recent, a single dose of 1.5mg/kg in the morning of the
day before section. On the day of section, the morning
dose of enoxaparin should be omitted and the operation
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Management of Venous Thrombosis in Pregnancy revised.qxd 8/5/08 10:53 Page 8

30 Medical problems in pregnancy

farin, she can be loaded appropriately on day 3 after deliv-

Suspected massive PE
Proceed directly to therapy while
arranging baseline investigations
Start LMWH therapy while awaiting objective testing
Suspected PE
CXR, ECG, blood gases,
thrombophilia screen
ery and the INR checked according to the British haema-
tology guidelines,37 with subsequent referral for anticoag-
ulant monitoring. It is important to reassure pregnant
women and new mothers that breastfeeding is safe with
Other causes either LMWH or warfarin. In women who have experi-
excluded
enced a recurrent event during pregnancy, close liaison
with the haematologist is required, as lifelong therapy may
be warranted.

Conclusion
Compression US of DVT present, Thromboembolic disease continues to be a major cause of
both legs does not require
V/Q scan
maternal morbidity and mortality. Increased awareness of risk
factors, appreciation of the need for objective testing and
Normal
early commencement of preventive and definitive therapy are
the first steps to reducing the impact of VTE in pregnancy.

V/Q scan References

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Enquiries into Maternal Deaths in the United Kingdom. London:
CEMACH, 2007.
Low 2. Hogberg U, Innala E, Sandstrom A. Maternal mortality in Sweden,
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Trends in Urology Gynaecology & Sexual Health May/June 2008 www.tugsh.com

Management of Venous Thrombosis in Pregnancy revised.qxd
KEY POINTS
• Pregnancy is associated with a two- to fourfold increase in risk of
venous thromboembolism (VTE).
• Thromboprophylaxis should be commenced and graduated elastic
compression stockings fitted as soon as a pregnancy test is
confirmed in high-risk women.
• Thromboprophylaxis and use of compression stockings should be
continued until six weeks postpartum.
• Women on warfarin need to be converted to low molecular weight
heparin (LMWH) by six weeks of gestation to avoid coumarin
embryopathy.
• Objective testing for deep venous thrombosis or pulmonary
embolism should be undertaken if VTE is clinically suspected.
• Compression Duplex ultrasound is the primary diagnostic test for
deep venous thrombosis.
• A ventilation/perfusion lung scan or computerised tomography
pulmonary angiogram can be used for investigation of pulmonary
embolism, but consideration of radiation dose to mother or fetus is
required.
• D-dimers are often elevated in uncomplicated pregnancy and
therefore are not part of VTE algorithms.
• Enoxaparin is the preferred LMWH for therapeutic anticoagulation.
• Routine monitoring of anti-factor Xa levels is not required.
• Routine monitoring of platelets after commencement of treatment
with LMWH is not required if there is no history of unfractionated
heparin exposure.
• For women with a VTE during pregnancy, anticoagulation should be
continued for at least six weeks postnatally and until at least six
months of treatment has been given in total.
combining clinical probability, D-dimer testing, and computed
tomography. JAMA 2006; 295: 172-9.
16. Bates SM, Ginsberg JS. How we manage venous thromboembolism
during pregnancy. Blood 2002; 100: 3470-8.
17. Chan W-S, Ginsberg JS. Diagnosis of deep vein thrombosis and
pulmonary embolism in pregnancy. Thrombosis Res 2002; 107: 85-91.
18. Royal College of Obstetricians and Gynaecologists.
Thromboembolic disease in pregnancy and the puerperium: acute
management. RCOG Green Top Guideline 2007; No. 28.
19. Kassai B, Boissel JP, Cucherat M, et al. A systematic review of the
accuracy of ultrasound in the diagnosis of deep venous thrombosis in
asymptomatic patients. Thromb Haemost 2004; 91: 655-66.
20. Eichinger S. D-dimer testing in pregnancy. Semin Vasc Med 2005; 5:
375-8.
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Trends in Urology Gynaecology & Sexual Health May/June 2008