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Suspected Pulmonary Embolism in Pregnancy
Clinical Presentation, Results of Lung Scanning, and Subsequent Maternal and Pediatric Outcomes
W. S. Chan, MD, FRCPC;
J. G. Ray, MD, FRCPC;
S. Murray, MD, FRCPC;
G. E. Coady, MRT(N);
G. Coates, MD, FRCPC;
J. S. Ginsberg, MD, FRCPC
Arch Intern Med. 2002;162:1170-1175.
ABSTRACT
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Background Ventilation-perfusion (VQ) scanning is used when pulmonary embolism
(PE) is suspected during pregnancy; however, the distribution of lung scan
results and safety of VQ scanning have never been studied.
Objective To study the distribution of lung scan results and safety of VQ scanning
as well as the safety of withholding anticoagulation therapy following a normal
or nondiagnostic scan in pregnant women.
Methods The study group comprised 120 consecutive pregnant women who presented
with suspected PE. Clinical data were collected, and the lung scans were reinterpreted
by 2 independent experts. Subsequent pregnancy and pediatric outcomes were
determined by direct patient follow-up.
Results During the study period, 120 pregnant women (mean age, 32 years) underwent
121 VQ scans. Eight cases (6.6%) were already receiving treatment for venous
thromboembolism prior to VQ scanning. In the remaining 113 scans, 83 (73.5%)
were interpreted as normal, 28 (24.8%) as nondiagnostic, and 2 (1.8%) as high
probability. In the 104 women who did not receive anticoagulation therapy
following lung scanning (80 normal and 24 nondiagnostic), no venous thromboembolic
events were reported (mean [range] length of follow-up, 20.6 [0.5-108] months).
Examination of pediatric data from 110 live births (90.2%) (mean [range] age,
20.5 [0.5-100] months) revealed no increase in the rates of congenital and
developmental anomalies.
Conclusions The prevalence of high-probability VQ scans in pregnant women with suspected
PE and probable PE is very low. Withholding anticoagulation in pregnant women
with normal or nondiagnostic VQ scans is probably safe. In addition, pediatric
risks from VQ scans are low. Large prospective studies are needed to evaluate
diagnostic strategies for pregnant women with suspected PE.
INTRODUCTION
PULMONARY EMBOLISM (PE) is a major preventable cause of maternal mortality
during pregnancy and the puerperium.1-3
As in nonpregnant patients, the diagnosis of PE during pregnancy is usually
made by combining clinical probability and the results of objective testing.4-5 Ventilation-perfusion (VQ) scanning
remains a widely used imaging technique for the investigation of PE in nonpregnant
patients.4-5 Results from PE diagnostic
studies have been extrapolated to pregnant women even though these patients
have been systematically excluded from participation in these studies largely
due to concerns (on behalf of physicians and patients) about the dangers of
fetal radiation exposure. The assumption that the results of lung scans in
nonpregnant patients are generalizable to the pregnant subject might be incorrect
because, as a group, pregnant women are younger and less likely to have concomitant
respiratory illnesses that could cause an abnormal scan, but they might have
physiological changes such as compression of the lungs by the enlarging uterus
that could cause an abnormal scan. These issues are further confounded by
nonthrombotic symptoms that mimic PE, such as shortness of breath and chest
pain, which are common during pregnancy.
In nonpregnant patients, a normal perfusion scan excludes PE and a highprobability
scan is usually diagnostic of its presence,4
whereas all other scan results (ie, abnormal perfusion but not meeting the
criteria for high probability) are nondiagnostic. Nonpregnant patients with
nondiagnostic scans are problematic because they are common, and PE is present
in up to 30%.4 To circumvent the need for pulmonary
angiography (the criterion standard), a diagnostic strategy based on combining
VQ scan interpretation5 and serial compression
ultrasonography (CUS) has been demonstrated to be useful in patients with
nondiagnostic scans.6 This strategy exploits
the use of CUS and is based on the frequent coexistence of PE and deep venous
thrombosis (DVT)7; most patients with PE have
DVT, and the absence of DVT detected by serial CUS in patients with nondiagnostic
scans obviates the need for further investigation or treatment. However, yet
again, pregnant women were excluded from this study.
In nonpregnant patients, the prevalence of high-probability, normal
perfusion, and nondiagnostic scans is from 8% to 14%, 27% to 36%, and 47%
to 59%, respectively, with most patients having nondiagnostic scans.4-5 Little is known about the distribution
of VQ scan results in pregnant patients presenting with suspected PE. Even
less is known about the safety of withholding anticoagulation treatment in
pregnant women with suspected PE and normal perfusion or nondiagnostic scans.
In addition, based on low-calculated fetal radiation dose exposure,8 VQ scanning is thought to be safe for the fetus and
should be performed in pregnant women with suspected PE. There are, however,
no clinical data to support the absence of an increase in adverse pregnancy
outcomes such as spontaneous losses, congenital malformations, or childhood
cancers. Accordingly, to assess these issues, we conducted a 2-center study
of consecutive pregnant women who presented with suspected PE and underwent
VQ scanning.
PATIENTS AND METHODS
STUDY POPULATION
The present study was approved by the institutional review boards of
the Women's College Campus, Sunnybrook and Women's Health Sciences Centre,
Toronto, Ontario (WWC), and the McMaster Division, Hamilton Health Sciences
Corporation, Hamilton, Ontario (McMaster). Consecutive pregnant women who
presented with suspected PE and underwent VQ scanning at 1 of the 2 hospitals
were identified through their nuclear medicine departments. The inclusion
periods were from January 1990 to April 2000 (WCC) and from January 1996 to
April 2000 (McMaster); in the latter facility, earlier scans were not accessible.
The hospital medical records of these patients were reviewed, and information
on maternal demographics, stage of pregnancy, symptoms at presentation, and
the most responsible physician's probable diagnosis (when available) prior
to obtaining the VQ scans was abstracted. We sought for the results of additional
relevant tests that were performed (ie, chest radiography, CUS, impedance
plethysmography, D-dimer testing, and pulmonary angiography) and abstracted
information on anticoagulation treatment and pregnancy outcomes. Patients
were contacted by telephone (2 weeks to 9 years after their presentation)
to verify information on immediate medical management at the time of suspected
PE, including use of anticoagulation therapy, and to confirm subsequent pregnancy
outcomes. Maternal venous thromboembolic events (VTEs), as well as pediatric
outcomes, were then obtained using a standardized data collection sheet. If
the woman could not be contacted directly, this information was obtained from
her family physician and/or hospital medical record.
VQ SCANS
Perfusion scans at both centers were performed using intravenous injections
of technetium Tc 99m macroaggregated albumin (99mTc-MAA), and the
ventilation scans were performed using technetium Tc 99m methylene diphosphonate
aerosol (99mTc-MDA) and technetium Tc 99m sulfur colloid (99mTc-SC) at WCC and McMaster, respectively. Patients were managed according
to local practice by the attending physician, which was usually based on a
combination of clinical probability, lung scan results, and the results of
other relevant tests.
For this study, 2 experts (J.S.G. and G.C.) reinterpreted each scan
separately using the "McMaster criteria."5
Scans were defined as normal (ie, no perfusion defects), nondiagnostic (ie,
1 or more perfusion defects associated with a corresponding ventilation defect
or a subsegmental perfusion defect with normal ventilation), or high probability
(ie, large [>75%] subsegmental or greater perfusion defects with normal ventilation).5 Both experts were blinded to the original interpretation
of the VQ scan, as well as all patient characteristics and outcomes. In cases
in which disagreements occurred, the final interpretation was based on consensus
between the 2 experts.
ANALYSES AND STATISTICS
For the distribution of lung scan results, the prevalence (and its corresponding
95% confidence interval [CI]) of patients with normal, nondiagnostic, and
high-probability scans was calculated for (1) all patients who presented for
VQ scan investigation and (2) the subgroup of patients whose primary presentation
was suspected PE (and not DVT) and had not received full-dose unfractionated
heparin or low-molecular-weight heparin for more than 2 weeks. The safety
of withholding anticoagulants in patients with normal and nondiagnostic scans
was assessed by determining the percentage (and 95% CI) of patients whose
scans were independently adjudicated as nondiagnostic or normal, who were
not anticoagulated, and who remained event free on follow-up.
The safety of VQ scanning during pregnancy was assessed by determining
the prevalence of the following adverse pregnancy outcomes: preterm labor,
preeclampsia, spontaneous loss, and stillbirths. The safety of fetal in utero
VQ scan exposure was further assessed by determining the prevalence of congenital
and developmental anomalies in these offspring and comparing these results
with the observed national rates (Canada) and that seen at one of the hospitals
(WCC). A weighted  statistic (and the corresponding 95% CI) was calculated
for interobserver agreement between the 2 experts reinterpreting these scans.
RESULTS
MATERNAL DEMOGRAPHICS AND PRESENTATION
Approximately 30 000 deliveries took place at WCC between January
1990 and April 2000, whereas approximately 12 750 deliveries occurred
at McMaster between January 1996 and April 2000. Both centers are high-risk
obstetrical referral centers in Ontario. At WCC, 57 women presented with suspected
PE and underwent lung scan testing. At McMaster there were 64 suspected episodes
of suspected PE, and lung scans were performed in 63 women (1 woman presented
twice in 2 different pregnancies and was included in the analyses both times).
Therefore, when pooling the results, 120 pregnant women presented with 121
episodes of suspected PE and underwent a total of 121 VQ scans.
The mean (range) maternal age at the time of presentation was 32 (17-41)
years. Half of the women were nulliparous and presented for investigations
after the first trimester of pregnancy (Table 1). In the 9 women previously diagnosed as having remote venous
thromboembolism (8 women) or arterial thrombosis (1 woman) prior to the pregnancy
of interest, 7 women were not receiving any anticoagulants, 1 was taking aspirin
(81 mg/d), and 1 was taking dalteparin (low-molecular-weight heparin) at a
"prophylaxis" dose of 5000 U/d; 8 other women were receiving full-dose anticoagulation
therapy prior to their presentation for VQ scan testing because of previously
diagnosed acute venous thromboembolism (PE or DVT).
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Table 1. Characteristics of the Study Population*
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The presenting symptoms of women with suspected PE who underwent VQ
scanning were available for 97 (80.2%) of the 121 cases. The most common complaints,
either alone or in combination, were dyspnea (60 [61.9%]), pleuritic chest
pain (45 [46.4%]), and nonpleuritic chest pain (18 [18.6%]). Alternate clinical
diagnoses thought to be more likely than PE were documented in 49 (40.5%)
of the 121 cases. The most common alternate diagnoses were pneumonia or bronchitis
(20 [40.8%] of 49) and exacerbation of asthma (7 [14.3%] of 49).
TESTS PERFORMED IN ADDITION TO VQ SCANS
A chest radiograph was obtained in 60 cases (49.6%) prior to lung scanning,
and 24 (40.0%) were abnormal. Ten demonstrated consolidation consistent with
clinical findings of pneumonia, 4 demonstrated atelectasis, and another 10
indicated pulmonary vascular congestion or effusion.
Bilateral CUS or impedance plethysmography was performed in 67 cases
(55.4%) (not diagnosed with recent acute DVT), and all results were negative.
Serial ultrasonography (multiple testing over 7 days) was performed in 7 women;
all results remained normal. Pulmonary angiography was performed in 2 women;
1 test result was positive for PE in a woman with a nondiagnostic scan.
DISTRIBUTION OF VQ SCAN RESULTS, MANAGEMENT, AND SUBSEQUENT OUTCOMES
OF THE STUDY POPULATION
Although 121 women underwent VQ scanning for suspected PE, 1 woman experienced
a cardiopulmonary arrest during the lung scan and died before her lung scan
was completed; therefore, reinterpretation was not performed in this patient.
The reinterpretation of the remaining 120 scans by the 2 independent readers
is summarized in Table 2. There
was agreement in 112 of 120 scans; the weighted score was excellent
at 0.86 (95% CI, 0.76-0.96). The readers interpreted 83 scans (69.2%) as normal,
25 (20.8%) as nondiagnostic, and 4 (3.3%) as high probability. In the 8 cases
in which there was disagreement, 4 scans were read as nondiagnostic by one
and normal by the other; in the other 4 cases, the converse occurred. The
discrepant scans were reviewed by the 2 readers, and consensus was achieved,
yielding the following results: 87 (72.5%) were normal; 29 (24.2%), nondiagnostic;
and 4 (3.3%), high probability.
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Table 2. Distribution of the Lung Scan Results Based on Independent
Interpretation of 120 Ventilation-Perfusion Lung Scans Performed in Pregnancy
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In the subgroup of 113 women who presented with suspected PE during
pregnancy and who were not receiving therapeutic anticoagulation, the lung
scans were normal in 83 (73.5%), nondiagnostic in 28 (24.8%), and high probability
in 2 (1.8%) (Figure 1). Based on
initial on-site investigations, 8 of these 113 women were given full-dose
anticoagulation after VQ scanning. Of these 8 scans, 2 were adjudicated as
high probability, 4 as nondiagnostic, and 2 as normal. One of the women with
a normal scan was given anticoagulation therapy because her scan had been
interpreted locally as nondiagnostic, and she refused further definitive testing.
The other woman received anticoagulation despite having a normal scan because
of acute myocardial infarction.
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Chart of study population, management, and subsequent outcomes. PE
indicates pulmonary embolism; DVT, deep venous thrombosis; VTE, venous thromboembolic
event; and CI, confidence interval.
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Of the 105 women who received no anticoagulation, a second maternal
death occurred 2 days after she had a normal lung scan. The cause of death
was the result of complications of primary pulmonary hypertension.
In the remaining 104 cases (80 normal and 24 nondiagnostic scans), no
anticoagulation was given. Follow-up was undertaken by phone contact in 88
(85%) of 104 cases and through family physicians or hospital medical records
in the rest. The mean (range) follow-up period was 20.6 (0.5-108) months.
No VTE was reported.
OBSTETRICAL AND PEDIATRIC OUTCOMES
Obstetrical and pediatric outcomes for all 121 pregnancies are presented
in Table 3. Two maternal deaths
occurred, one from massive PE and DVT at 19 weeks of gestation (incomplete
lung scan) and the other from previously diagnosed primary pulmonary hypertension
at 18 weeks (normal lung scan).
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Table 3. Rates of Various Pregnancy and Pediatric Outcomes*
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Of the remaining 119 pregnancies, 3 women experienced spontaneous pregnancy
losses (<20 weeks). In the first case, miscarriage occurred 2 days after
presentation with suspected PE during the first trimester, and in the remaining
2 cases, spontaneous loss occurred 3 to 4 weeks after the women presented
with suspected PE in the first trimester of pregnancy. Another woman had an
elective termination of pregnancy for unrelated reasons. Two women experienced
neonatal deaths after premature delivery of twins at 24 to 25 weeks of gestation.
In the first case (twin neonatal deaths), a lung scan was done 5 days earlier,
and in the second case (1 of the twins died), 2 weeks earlier. In both cases,
threatened premature labor was already present prior to investigation for
suspected PE. The rate of spontaneous abortions was 2.5% (3 of 119 pregnancies;
95% CI, 0.5%-6.1%), and the rate of infant death was 1.7% (2 of 119 pregnancies;
95% CI, 0.2%-4.8%).
Information on the mode of delivery was available for 110 of 113 pregnancies:
79 (71.8%) were delivered vaginally and 31 (28.2%) were delivered by cesarean
section. Nineteen pregnancies (16.8%) were complicated by preeclampsia. The
mean (range) gestational age at delivery for these pregnancies was 37 (25-42)
weeks; 27 (23.8%) were preterm (<37 weeks).
The mean birth weight for 112 newborns, which included 6 sets of twins
and 1 set of triplets, was 2914 g (95% CI, 2724-3104 g). We were able to obtain
follow-up pediatric data on the health of 110 children (90.2% of the total
122 live births, excluding the 3 neonatal deaths). The mean (range) age of
these offspring was 20.5 (0.5-100) months.
Of 110 women, 4 (3.6%; 95% CI, 0.9%-7.8%) reported congenital anomalies
in their offspring. The first was a child delivered at term who had hypoplastic
lungs and short stature and was diagnosed as having a rare autosomal recessive
genetic disorder. The VQ scan had been performed in the mother at 22 weeks
of gestation, who had received low-dose subcutaneous heparin until delivery.
The second case was a child diagnosed as having duplicate ureters born to
a woman who underwent VQ scanning at 11 weeks of gestation. The third case
was an infant with transposition of the great vessels; the anomaly was diagnosed
in utero prior to maternal VQ scanning. The fourth woman reported that her
child has a small hemangioma; VQ scanning had been performed at 28 weeks of
gestation (normal), and the child delivered at term.
Of 106 women, 4 (3.8%; 95% CI, 1.0%-8.2%) further reported developmental
abnormalities in their offspring. In 3 pregnancies, the children were born
severely premature. The first occurred in 1 of 2 twins, who was delivered
at 25 weeks of gestation because of premature labor and now has mild cerebral
palsy. In this case, the maternal VQ scan was performed 4 days prior to delivery,
and no anticoagulation was administered. The second child was delivered at
26 weeks because of maternal preeclampsia and now has cerebral palsy and blindness;
her mother had been investigated with VQ scanning in the first trimester when
she presented with pneumonia. The third developmental abnormality was reported
in a child delivered at 26 weeks because of maternal acute appendicitis (several
days after VQ scanning), and who now has respiratory and hearing problems
and retinopathy as a result of being born prematurely. The fourth child, who
was delivered at term and reported to have developmental abnormalities, had
seizures at age 2 years. The maternal VQ scanning was performed at 25 weeks
of gestation, and no anticoagulation was given.
No childhood cancers or leukemias were reported (0%; 95% CI, 0.0%-1.0%).
These rates of pregnancy and pediatric outcomes as well as the corresponding
rates observed at our hospitals and in Canada over the last 10 years9-11 are given in Table 3.
COMMENT
To our knowledge, our study of 121 suspected episodes of PE in 120 women
is the largest study on this topic that has been published and provides reliable
estimates of the distribution of lung scan results seen in pregnant women
with suspected PE. The results of this study show that only 1.8% of pregnant
women who primarily present with suspected PE (and did not have previously
diagnosed DVT) have high-probability scans, whereas 24.8% have nondiagnostic
and 73.5% have normal scans. Second, in the 104 women who had nondiagnostic
or normal scans and were not treated, none (0%; 95% CI, 0.0%-1.0%) developed
subsequent episodes of VTEs during a mean follow-up period of over 20 months.
Finally, the rates of spontaneous losses (2.6%, 95% CI, 0.5%-6.1%) and congenital
anomalies (3.6%; 95% CI, 0.9%-7.8%) reported by the women investigated for
PE during pregnancy were consistent with those seen in the general pregnancy
population.
This study is in a historical cohort, and is thus subject to the biases
of a retrospective study. Because the identification of eligible patients
occurred through a search of radiology records, women might have been missed;
however, the number is likely to be few because using a separate database
of medical records, we verified that at 1 of the 2 centers (WCC) all women
who underwent lung scans were identified.
We principally relied on individual patient recall to identify subsequent
VTEs, pregnancy, and pediatric outcomes. By relying on patient recall of symptoms
of VTEs or any subsequent objective testing for VTEs, we might have missed
asymptomatic events; however, published data suggest that major obstetrical
events (such as mode of delivery, peripartum complications, gestational age
at delivery, and birth weight) are accurately recalled for up to 30 years.12 Although it is possible that subtle developmental
abnormalities and childhood malignancies might not yet be detected by 20 months
of age, it is highly unlikely that major congenital anomalies would be unreported.
From this study, the VQ scan results in pregnant women with suspected
PE clearly differ from those performed in nonpregnant patients with suspected
PE. The prevalence of high-probability VQ scans in pregnant women is very
low (1.8%) compared with that reported in nonpregnant patients (about 10%);
the prevalence of normal VQ scans is much higher (73.5%) in pregnant women
than in nonpregnant subjects (about one third).4-5
Finally, nondiagnostic scans were found in one quarter of pregnant patients
compared with one half or more in nonpregnant patients.4-5
Intuitively, these results make sense; since the mean age of the women in
our study is only 32 years, they would be expected to have fewer comorbid
lung conditions that would cause abnormal perfusion scans. On the other hand,
the low rates of high probability scans among pregnant women highlight the
common occurrence of nonthrombotic causes of chest pain and dyspnea seen in
pregnancy, particularly during the second and third trimesters.
Perhaps the decision to withhold anticoagulant therapy in pregnant patients
with a nondiagnostic VQ scan (which represented about a quarter of the women
in our cohort) is still of great concern for clinicians. From a study of nonpregnant
patients,6 the use of bilateral normal leg
ultrasound to rule out the presence of DVT has been validated. If DVT is diagnosed,
PE is assumed to be present. If DVT is not diagnosed, withholding anticoagulant
therapy is a safe strategy. The safety of adopting such an approach in pregnancy
is uncertain because ultrasound diagnosis of DVT in pregnancy has never been
formally evaluated. This approach might also not be safe in pregnancy because
the source of the embolus during pregnancy might be in the pelvic veins, which
are not readily accessible by ultrasound. Although pulmonary angiography is
the criterion standard and has been advocated as a test that can be safely
performed in pregnancy,8 the invasive nature,
use of contrast, and absorption of radiation by the fetus will always remain
a concern. In our review, only 2 pulmonary angiograms were actually performed.
From our study, a normal scan safely excludes PE during pregnancy (0
of 80 women; 95% CI, 0.0%-1.2%), although 2 women with normal lung scans received
anticoagulation (1 for myocardial infarction and 1 was empirically treated
following a scan that was locally interpreted as nondiagnostic). Drawing conclusions
from the pregnant women with nondiagnostic scans might be difficult because
of the small sample size and because 4 of the 28 women had received therapeutic
anticoagulation (all with normal leg ultrasound findings). However, in the
remaining 24 women (85.7%), no subsequent VTE was reported (95% CI, 67.3%-96.0%).
Therefore, in this specific cohort of women, bilateral leg ultrasound testing
should be performed; if the result is positive for DVT, then treatment should
be given. If negative, the need for further testing should be based on the
clinician's pretest probability. Such an approach is justifiable because in
this group of women, PE is likely absent (85.7%). This strategy, however,
should be further validated.
The present study is also the first to determine fetal outcomes after
VQ imaging during pregnancy. In a survey published in 1998,13
Boiselle and coworkers reported that although most (81%) of the physicians
in the United States who responded to their survey performed VQ scanning in
pregnant women, 19% avoided the use of this test "to avoid fetal radiation
exposure." In addition, 52% of facilities routinely obtained written consent
prior to the test. From our study, no increased risk in spontaneous conception
loss or adverse pregnancy events was observed. In addition, in the follow-up
of more than 90% of these offspring after a mean age of 20 months, no increase
in developmental abnormalities or malignancies were reported.
In conclusion, the distribution of lung scan results in pregnant women
with suspected PE differs from that in nonpregnant patients, and a high-probability
scan (and presumably PE) is rare. Future prospective studies are definitely
needed to confirm our findings and to optimize the therapeutic approach for
pregnant women with nondiagnostic lung scans.
AUTHOR INFORMATION
Accepted for publication September 27, 2001.
Dr Ginsberg is a recipient of a Career Investigator Award from the Heart
and Stroke Foundation of Ontario.
Corresponding author and reprints: W. S. Chan, MD, FRCPC, Department
of Medicine, Women's College Campus, Sunnybrook and Women's College Health
Sciences Centre, 76 Grenville St, Toronto, Ontario, Canada M5S 1B2.
From the Departments of Medicine (Drs Chan and Ray) and Radiology (Dr
Murray and Mr Coady), Women's College Campus, Sunnybrook and Women's College
Health Sciences Centre, Toronto, Ontario; the Department of Clinical Epidemiology
and Biostatistics, McMaster University, Hamilton, Ontario (Dr Ray); and the
Departments of Nuclear Medicine (Dr Coates) and Medicine (Dr Ginsberg), Hamilton
Health Sciences, Hamilton, Ontario.
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