Management of Venous Thrombosis in Pregnancy revised.

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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 abdominal delivery. As a result of these prothrombotic
and Maternal Medicine, University of Glasgow, Glasgow Royal changes, the incidence of VTE increases two- to fourfold
Infirmary; Professor I.A. Greer, MD, FRCP(Glas, Edin, Lond), FRCOG,
when a woman becomes pregnant, with a risk of
FRCPI, FMedSci, Dean, Hull York Medical School, University of York.
pregnancy-associated VTE of 0.1 per cent,6 and in women
enous thromboembolism (VTE) remains a major cause with a previous VTE the risk of recurrence is 2–3 per cent.
V of maternal mortality and is currently the most com-
mon direct cause of maternal death in the UK, with a
Assessment of other independent risk factors that may
be present and predispose to any of the three components
twofold higher prevalence than the next most common of Virchow’s triad is required, not only before pregnancy,
cause, haemorrhage.1 European studies have consistently but also again at the initial confirmation of pregnancy, as
calculated the pregnancy-related VTE mortality at 8.5–14 pregnancy progresses and post-delivery (Box 1).7,8
per million live births.2 The UK Confidential enquiries into
maternal deaths has shown that most of these deaths are Pre-conceptual counselling and strategies for women at
associated with substandard care, including a failure to risk of VTE in pregnancy
recognise symptoms in women who already had obvious All women at significant risk of VTE should ideally be
risk factors for VTE, delay in diagnosis, delayed or inade- identified pre-conceptually and made aware of their rela-
quate treatment for acute VTE and inadequate thrombo- tive VTE risk. Although many of the described risk factors
prophylaxis.1 Consequently, clinicians need to understand are not modifiable pre-pregnancy, the prothrombotic fac-
the implications and clinical management of thromboem- tors associated with obesity have been shown to improve
bolic disease in pregnancy. with weight loss, potentially reducing VTE risk.9 Similarly,
stabilisation of medical conditions may also potentially
Epidemiology of VTE during pregnancy improve thrombotic risk before embarking on pregnancy.
Virchow’s classic triad for VTE – hypercoagulability, venous Pre-conceptually, women need to be informed apropos
stasis and vascular damage – all occur in the course of the potential necessity for therapy as soon as pregnancy is
uncomplicated pregnancy and delivery. There are substan- achieved because of the rapid alterations in haemostatic
tial increases in factor VIII and fibrinogen; acquisition of factors. Similarly, it is essential that patients on coumarin
resistance to activated protein C (aPC) in 40 per cent of therapy are aware of the requirement to substitute low
pregnancies; reduction in protein S levels; and impaired molecular weight heparin (LMWH) for coumarin by six
fibrinolysis, all of which may persist for up to six weeks after weeks' gestation to avoid the risk of embryopathy.
birth, irrespective of the gestation at delivery.3 There is also In addition to pharmacological strategies, graduated
extensive reduction in venous flow velocity in the lower elastic compression stockings may be effective for throm-
limbs in pregnancy, with approximately a 50 per cent reduc- boprophylaxis in pregnancy.10 They may act by preventing
tion by 25–29 weeks’ gestation, reaching a nadir at 36 overdistension of veins, so preventing endothelial damage
weeks.4 Normal non-pregnant flow velocity rates are not and exposure of subendothelial collagen. They can there-
restored until about six weeks after delivery.5 Furthermore, fore be combined safely with pharmacological thrombo-
some degree of vascular endothelial damage or trauma to prophylaxis, both in the antenatal period and postnatally.
pelvic vessels appears inevitable in the course of vaginal or For women with confirmed deep venous thrombosis

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Management of Venous Thrombosis in Pregnancy revised.qxd 8/5/08 10:52 Page 4

26 Medical problems in pregnancy

test shows a clear-cut abnormality in the popliteal or

Box 1. Risk factors for venous thromboembolism in pregnancy. femoral veins, a diagnosis of proximal DVT is made. A
normal ultrasound does not exclude a calf DVT and, if
• Inherited thrombophilia • Infective and inflammatory normal in spite of a strong clinical suspicion, treatment
• Age over 35 years conditions should be commenced and the test repeated one week
• Obesity • Pre-eclampsia later to exclude the possibility of extending calf vein
• Operative delivery • Major obstetric haemorrhage thrombosis and development of a proximal DVT. If the
• Prolonged labour • Intravenous drug abuse repeat test is negative, treatment can be discontinued. If
• Gross varicose veins • Hyperemesis gravidarum an iliac DVT is suspected because of back pain and
• Immobility after delivery • Nephrotic syndrome swelling of the whole leg, pulsed Doppler and/or direct
• Prolonged bed rest • Sickle cell disease
• Air travel • Myeloproliferative disease visualisation of the iliac vein is recommended.
• Paraplegia • Ovarian hyperstimulation
• Dehydration • Acquired thrombophilia Measurement of D-dimer levels
Levels of D-dimers are increased in most patients with
DVT and PE. However, these levels increase with gestation-
(DVT), compression stockings can reduce the risk of post- al age, during complicated pregnancies, such as those
thrombotic syndrome if used for up to two years after the associated with preterm labour, abruption or gestational
event.10 It is, however, important that correctly fitted class hypertension20 and postpartum.21 These characteristics
2 graduated stockings are used, with repeat fittings as reduce the specificity of D-dimers in pregnancy and there-
pregnancy progresses.10 fore we do not recommend this test, although we accept
Various strategies combining pharmacological and that it may be complementary to venous ultrasound in
physical therapies to minimise the risk of primary throm- excluding DVT in pregnancy when both tests are negative.
bosis and VTE recurrence have been put forward based on
the woman’s past VTE and risk factor history (Table 1).11 Radiological investigations
The potential risks with the radiological tests often used
Clinical assessment of pregnant women with suspected VTE when PE is suspected are minimal when compared with
By itself, the clinical diagnosis of DVT and pulmonary the consequences of misdiagnosis (Figure 2). If the clinical
thromboembolism (PE) is unreliable (Box 2). In non- features are compatible with PE, a chest X-ray should be
pregnant individuals, DVT is confirmed in about 20–30 performed. This may identify pulmonary disease such as
per cent of suspected cases.12 In pregnancy, however, leg pneumonia, pneumothorax or lobar collapse, although
symptoms, chest pain and dyspnoea from non-thrombotic these problems are uncommon in young pregnant women.
causes are common;13 consequently, the accuracy of clini- While the chest X-ray is normal in more than 50 per cent
cal diagnosis falls to 8 per cent for DVT and to less than 5 of pregnant patients with objectively proven PE, abnormal
per cent for PE.14 features caused by PE include atelectasis, effusion, focal
Therefore, it is essential that objective testing is per- opacities, regional oligaemia or pulmonary oedema.22
formed expeditiously to avoid the risks, inconvenience Several studies have evaluated the role of ultrasound of
and costs of inappropriate anticoagulation. However, the lower limb deep veins in non-pregnant patients with
unlike in the non-pregnant population, where safe and suspected PE.23–26 The rationale is that a diagnosis of DVT
accurate algorithms are available,15 there are no well- may indirectly confirm the diagnosis of PE, and because
designed large clinical studies evaluating the accuracy of therapy is often the same for both conditions, further inves-
objective tests for the diagnosis of DVT or PE in pregnant tigation to exclude PE may be unnecessary. Performing
patients. Therefore, recommendations for the diagnosis bilateral ultrasound leg studies in pregnant women would
of DVT or PE during pregnancy are largely empirical and therefore limit the radiation doses given to the mother and
based on extrapolations from studies performed in non- fetus. If the chest X-ray and bilateral ultrasound leg studies
pregnant patients.16–18 are normal, and PE is suspected, a ventilation/perfusion
(V/Q) lung scan or computerised tomography pulmonary
Venous ultrasound angiogram (CTPA) should be performed.
Ultrasound of the entire proximal venous system is the ini- In our unit, V/Q lung scans are still the preferred ini-
tial test for suspected DVT during pregnancy (Figure 1). tial investigation of choice; consequently, if the scan is nor-
Ultrasound is known to have a high diagnostic accuracy in mal, the diagnosis of PE is excluded.27 Treatment should
non-pregnant populations;19 consequently, if the initial be continued when the lung scan reports a medium prob-

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Management of Venous Thrombosis in Pregnancy revised.qxd 8/5/08 10:52 Page 5

Medical problems in pregnancy 27

Clinical situation Suggested management

Single previous VTE (not pregnancy- or ‘pill’-related) associated Antenatal: surveillance or prophylactic doses of LMWH (eg 40mg
with a transient risk factor and no additional current risk factors, enoxaparin or 5000iu dalteparin daily) ± GECS. Discuss decision
such as obesity 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

Single previous idiopathic VTE or single previous VTE with Antenatal: prophylactic doses of LMWH (eg 40mg enoxaparin or
underlying thrombophilia and not on long-term anticoagulant 5000iu dalteparin daily) commenced as soon as pregnancy
therapy, or single previous VTE and additional current risk diagnosed ± GECS. With antithrombin deficiency there is a strong
factor(s) (eg BMI *35) 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

More than one previous episode of VTE, with no thrombophilia Antenatal: prophylactic doses of LMWH commenced (eg 40mg
and not on long-term anticoagulant therapy 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

Previous episode(s) of VTE in women receiving long-term Antenatal: switch from oral anticoagulants to LMWH therapy
anticoagulants (eg with underlying thrombophilia) (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

Thrombophilia (confirmed laboratory abnormality) but no prior VTE 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

Risk factors for VTE present antenatally but no previous VTE Carry out risk assessment for VTE. If multiple risk factors present,
or thrombophilia 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

Following Caesarean section or vaginal delivery 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

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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Management of Venous Thrombosis in Pregnancy revised.qxd 8/5/08 10:53 Page 6

28 Medical problems in pregnancy

among both radiologists and clinicians in non-pregnant

Box 2. Symptoms and signs of deep venous thrombosis and
pulmonary embolism. patients, its role in pregnancy is not clearly defined and is
often not addressed in published guidelines.32
Deep venous thrombosis A survey of American radiological practice in 2002
•Leg pain or discomfort
revealed CTPA to be the initial imaging technique of
•Swelling
choice in pregnant patients with suspected PE; however,
•Tenderness
there was great variation in the standard of practice.33 In
•Increased temperature and oedema
•Lower abdominal pain spite of concerns about the potential risks to the fetus,
•Elevated white cell count only 60 per cent of radiologists obtained informed con-
sent before imaging, only 40 per cent altered imaging
Pulmonary embolism parameters in order to reduce radiation dose, and only 17
• Dyspnoea
per cent had a written departmental policy in place.
• Collapse
Recent analysis of UK practice revealed similar lack of
• Chest pain
• Haemoptysis knowledge of fetal dosimetry in the imaging of pregnant
• Faintness women suspected of having PE.34 In practice, the choice
• Raised jugular venous pressure of diagnostic test for PE will often reflect the availability of
• Tachycardia these techniques, but clinicians should be aware of their
• Reduced PaO2 and/or PaCO2 relative merits and limitations.
• Focal signs in chest
• Abnormalities on X-ray
Treatment of VTE during pregnancy
• Symptoms and signs associated with deep venous thrombosis
Before anticoagulant treatment is commenced, blood
should be taken for a full thrombophilia screen, a full
ability and consideration given to confirmation by CTPA. blood count and a coagulation screen. Blood should also
With a high probability result for PE on lung scan, the be sent for urea, electrolytes and liver function tests, to
diagnosis of PE is confirmed.14 When the lung scan exclude renal or hepatic dysfunction, which are cautions
reports a low risk of PE and leg ultrasound studies are neg- for anticoagulant therapy. Although the results of a throm-
ative, yet there is a high degree of clinical suspicion, we bophilia screen will not influence immediate manage-
would continue anticoagulant treatment, and perform an ment, they can provide information that can influence the
alternative test such as CTPA or repeat testing in one week duration and intensity of anticoagulation, such as when
(V/Q lung scan and leg ultrasound examination).28 antithrombin deficiency is identified.7
With regard to the V/Q lung scan, during pregnancy, It is important to be aware of the effects of pregnancy
the ventilation component can often be omitted, thereby and thrombus on the results of a thrombophilia screen.
minimising the already low radiation dose. CTPA has poten- For example, protein S levels fall in normal pregnancy,
tial advantages over radionuclide (V/Q lung) imaging, making it extremely difficult to make a diagnosis of pro-
including better sensitivity and specificity,29 greater accessi- tein S deficiency during pregnancy. aPC resistance is
bility, with most maternity units in the UK having CTPA found with the aPC sensitivity ratio test in around 40 per
facilities onsite, and an even lower radiation dose to the cent of pregnancies, because of the physiological changes
fetus. In addition, it can pick up other pathology such as in the coagulation system. Anticardiolipin antibodies can
aortic dissection, but may not identify small peripheral PE. also influence the result of the test for aPC resistance.
In spite of these potential advantages, we and others Antithrombin may be reduced when extensive thrombus
continue to recommend V/Q lung scanning as the first- is present.
line investigation in pregnancy because of its high nega- Other factors can also influence the results of a throm-
tive predictive value in this situation and its lower radia- bophilia screen. Antithrombin levels are reduced in
tion dose to the mother’s breast tissue as compared to nephrotic syndrome (a condition associated with an
CTPA.18 The radiation dose to the mother’s thorax with increased risk of thrombosis), and protein C and S levels
CTPA will be around 2 rads and it is known that 1 rad will are reduced in liver disease. Clearly, genotyping for factor V
increase the lifetime risk of breast cancer by around 14 per Leiden and prothrombin G20210A will not be influenced
cent.30,31 This is an important consideration when only by pregnancy or current thrombosis. It is therefore impor-
around 1 in 20 pregnant women with suspected PE will tant that thrombophilia screens are interpreted by clini-
have the diagnosis confirmed. Therefore, although CTPA cians with specific expertise in the area; they will need
has rapidly gained acceptance as a robust technique repeating after anticoagulation therapy has finished.

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Medical problems in pregnancy 29

The anticoagulants that have been evaluated for pre-

vention and treatment of VTE in pregnancy centre on the Suspected (symptomatic)
use of unfractionated heparin (UFH) or LMWH because acute DVT
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 Consider thrombophilia screen
for the acute treatment of VTE in pregnancy, with a sys-
tematic review of LMWH in pregnancy confirming its effi- Start LMWH therapy while
cacy and safety in the management of acute thrombosis awaiting objective testing
and provision of thromboprophylaxis.35 Although several
LMWH preparations are available, the extensive pub-
Compression US of
lished experience with enoxaparin and dalteparin and
symptomatic leg
safety data suggest that these should usually be the first-
choice agents, and we recommend the use of LMWH
throughout pregnancy. Normal and low Normal but high
For the acute treatment of VTE, we initiate therapy clinical suspicion clinical suspicion
with a weight-adjusted dose based on the booking weight
(40–100mg enoxaparin twice daily). The woman should Continue treatment and repeat
be taught to self-inject by attending staff, and she can then Normal compression US in 1 week DVT present
be managed as an outpatient until delivery.
As pregnancy progresses (and most women gain
weight), the volume of distribution of LMWH changes. Continue treatment
Therefore three options are available. The first is the Stop
treatment
maintenance of the initial dose regimen throughout the
treatment period (six months and therefore usually the
Figure 1. Diagnostic algorithm for pregnant women with symptoms suggesting acute
entire pregnancy and postpartum period).
deep venous thrombosis (DVT). LMWH, Low molecular weight heparin; US, ultrasound.
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 We generally recommend induction of labour at 38–39
LMWH does not cross the placenta and therefore the weeks. The dose of enoxaparin should be reduced to
weight of the feto-placental unit is not relevant. 40mg once daily (thromboprophylactic single dose) on
The third option is to measure anti-factor Xa levels the day before induction of labour, or, if the thrombosis
four to six hours after the morning dose; the target thera- was recent, a single dose of 1.5mg/kg in the morning of
peutic range is 0.4–1.2u/ml for peak levels. If the peak the day before planned induction. Although many centres
anti-Xa level is >1.2u/ml, the dose of enoxaparin should administer 40mg of enoxaparin on the day of labour, this
be reduced and peak anti-Xa activity reassessed. prevents the use of regional anaesthetic techniques, which
We favour the first approach in most women; however, should not be used until at least 12 hours after the previ-
in extremes of maternal weight (<50kg or >90kg) or with ous prophylactic dose (40mg) of enoxaparin and 24 hours
other complicating factors putting them at high risk, it can after the last dose if still on therapeutic anticoagulation.
be useful to ensure that appropriate levels of anticoagula- After delivery, enoxaparin should not be given for at least
tion are being achieved and therefore anti-factor Xa is three hours after the epidural catheter has been removed
measured. If there has been previous exposure to unfrac- and the cannula should not be removed within six hours
tionated heparin, a platelet count will need to be checked, of the most recent injection. The treatment dose (twice-
ideally every two to three days until day 14, and at regular daily administration) should be recommenced immedi-
intervals thereafter, to exclude heparin-induced thrombo- ately following delivery.
cytopenia.36 For delivery by elective Caesarean section, the woman
should receive either a thromboprophylactic dose of
Management at the time of delivery enoxaparin (40mg once daily) or if the thrombosis was
For women on therapeutic anticoagulation, induction of recent, a single dose of 1.5mg/kg in the morning of the
labour facilitates accurate timing of events and minimises day before section. On the day of section, the morning
the risk of labour commencing on full anticoagulation. 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-

ery and the INR checked according to the British haema-
Suspected massive PE Suspected PE
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
Proceed directly to therapy while CXR, ECG, blood gases, Other causes either LMWH or warfarin. In women who have experi-
arranging baseline investigations thrombophilia screen excluded
enced a recurrent event during pregnancy, close liaison
with the haematologist is required, as lifelong therapy may
be warranted.
Start LMWH therapy while awaiting objective testing

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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