The American Journal of Medicine
Volume 123, Issue 5 , Pages 426-431, May 2010

Silent Pulmonary Embolism in Patients with Deep Venous Thrombosis: A Systematic Review

  • Paul D. Stein, MD

      Affiliations

    • Departments of Internal Medicine and Research and Advanced Studies Program, College of Osteopathic Medicine, Michigan State University, East Lansing, Mich
    • Corresponding Author InformationReprint requests should be addressed to Paul D. Stein, MD, Michigan State University, College of Osteopathic Medicine, Department of Internal Medicine, Venous Thromboembolism Research Unit, St Joseph Mercy-Oakland Hospital, 44405 Woodward Ave, Pontiac, MI 48341-5023
    • ,
  • Fadi Matta, MD

      Affiliations

    • Departments of Internal Medicine and Research and Advanced Studies Program, College of Osteopathic Medicine, Michigan State University, East Lansing, Mich
    • ,
  • Muzammil H. Musani, MD

      Affiliations

    • Department of Internal Medicine, St. Joseph Mercy Oakland, Pontiac, Mich
    • ,
  • Benjamin Diaczok, MD

      Affiliations

    • Department of Internal Medicine, St. Joseph Mercy Oakland, Pontiac, Mich

Article Outline

Abstract 

Purpose

To determine, by systematic review of the literature, the prevalence of silent pulmonary embolism in patients with deep venous thrombosis.

Methods

Twenty-eight included published investigations were identified through PubMed. Studies were selected if methods of diagnosis of pulmonary embolism were described; if pulmonary embolism was stated to be asymptomatic; and if raw data were presented. Studies were stratified according to whether silent pulmonary embolism was diagnosed by a high-probability ventilation-perfusion lung scan using criteria from the Prospective Investigation of Pulmonary Embolism Diagnosis, computed tomography pulmonary angiography, or conventional pulmonary angiography (Tier 1), or by lung scans based on non-Prospective Investigation of Pulmonary Embolism Diagnosis criteria (Tier 2).

Results

Silent pulmonary embolism was diagnosed in 1665 of 5233 patients (32%) with deep venous thrombosis. This is a conservative estimate because many of the investigations used stringent criteria for the diagnosis of pulmonary embolism. The incidence of silent pulmonary embolism was higher with proximal deep venous thrombosis than with distal deep venous thrombosis. Silent pulmonary embolism seemed to increase the risk of recurrent pulmonary embolism: 25 of 488 (5.1%) with silent pulmonary embolism versus 7 of 1093 (0.6%) without silent pulmonary embolism.

Conclusion

Silent pulmonary embolism sometimes involved central pulmonary arteries. Because approximately one third of patients with deep venous thrombosis have silent pulmonary embolism, routine screening for pulmonary embolism may be advantageous.

Keywords: Deep venous thrombosis, Pulmonary embolism, Venous thromboembolic disease

 

Pulmonary embolism was unsuspected or undiagnosed antemortem in 3268 of 3876 patients in general hospitals or communities who had pulmonary embolism at autopsy (84%; range 80%-93%).1 Even in patients with large or fatal pulmonary embolism at autopsy, the majority (1902/2448 [78%]) of embolisms were unsuspected or undiagnosed antemortem.1 Many patients with unsuspected large or fatal pulmonary embolism had advanced associated disease.1 It has been tacitly assumed that diligence and increased awareness might diminish the proportion of unsuspected cases of pulmonary embolism. Patients who have sudden and unexplained catastrophic events in the hospital are a group in whom the diagnosis might be suspected more frequently if physicians maintain a high index of suspicion.1 However, the extent to which silent pulmonary embolism explains some of the unsuspected pulmonary embolism at autopsy is uncertain. Silent pulmonary embolism has been diagnosed in living patients with deep venous thrombosis since the early 1970s.2, 3 Silent pulmonary embolism may lead to pulmonary hypertension.4 Data indicate that incidentally detected pulmonary embolism may lead to death.5

Clinical Significance

 


•Silent pulmonary embolism occurs in approximately one third of patients with deep venous thrombosis.

•Silent pulmonary embolism is more frequent in patients with proximal deep venous thrombosis than in those with distal deep venous thrombosis.

•Recurrent pulmonary embolism during treatment for deep venous thrombosis is more frequent in those with silent pulmonary embolism than a first pulmonary embolism in those with no silent pulmonary embolism.

•Silent pulmonary embolism may occur in the central pulmonary arteries.

These reports of silent pulmonary embolism identify an important problem. For patients with deep venous thrombosis, is it sufficient to have a high level of suspicion of pulmonary embolism? Should patients with deep venous thrombosis undergo pulmonary imaging even if they have no respiratory symptoms? Should routine screening be performed to prevent a misdiagnosis of pulmonary embolism resulting from treatment failure? Might unnecessary insertion of an inferior vena cava filter be avoided if it were known that silent pulmonary embolism had been present and there was no failure of treatment of deep venous thrombosis6? To approach these issues, an assessment of the prevalence of silent pulmonary embolism in patients with deep venous thrombosis is needed. Whether routine imaging of pulmonary embolism would be appropriate depends in part on the prevalence of silent pulmonary embolism in patients with deep venous thrombosis. Therefore, this systematic review was undertaken.

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Materials and Methods 

We attempted to identify all published trials in all languages that reported the prevalence of silent pulmonary embolism in patients with deep venous thrombosis. Studies were identified by searching PubMed through July 2009. Key words were “silent,” “asymptomatic,” “incidental,” “symptomless,” and “occult pulmonary embolism.” We augmented our searches by manually reviewing the reference lists of all original articles. This was done by 2 of the authors, who worked separately and then reviewed their findings together. Authors were not blinded to journal, author, or institution.

Studies were included if they met the following criteria: the methods of diagnosis of pulmonary embolism were described; the pulmonary embolism was stated to be asymptomatic; raw data on the occurrence of silent pulmonary embolism were presented in sufficient detail to permit calculations of the prevalence.

The literature search identified 958 citations. Complete versions of the articles were obtained if, from review of the title or abstract, they satisfied the inclusion criteria. Among these, 720 were unrelated to silent pulmonary embolism, 48 were case reports or case series without data on the prevalence, 151 were reviews or editorials, 22 were related to silent pulmonary embolism in circumstances other than patients with deep venous thrombosis, and 4 had data that were included in a previous investigation. The literature search identified 13 investigations that met the inclusion criteria. An additional 15 investigations were identified from the references in these investigations and from a review article of antithrombotic therapy. Although retrospective investigations were not excluded, none were found.

Investigations were stratified into 2 tiers: Tier 1 included those in which silent pulmonary embolism was diagnosed on the basis of a high-probability interpretation of the ventilation-perfusion lung scan using criteria from the Prospective Investigation of Pulmonary Embolism Diagnosis (PIOPED), computed tomography (CT) pulmonary angiography, or conventional pulmonary angiography5, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17 (Table 1). Tier 2 included those in which silent pulmonary embolism was diagnosed by ventilation-perfusion lung scan based on unstated criteria or criteria other than PIOPED2, 3, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31 (Table 2). Criteria for ventilation-perfusion lung scan other than the PIOPED criteria were those of McNeil et al32 and Biello et al.33 All included investigations (both Tier 1 and Tier 2) were prospective. In several investigations, the authors indicated that consecutive patients were studied.2, 5, 11, 12, 13, 15, 16, 17, 20, 21, 22, 24, 25, 26, 28, 29, 30

Table 1. Tier 1: Silent Pulmonary Embolism in Patients with Deep Venous Thrombosis
First Author, Year (Reference)DVT SiteMethod for DVTMethod for PESilent PE n/N (%)Note
Girard 19877ProximalVenographyPulmonary angiogram9/50 (18)
Moser 19948?VenographyHigh-probability V/Q PIOPED16/44 (36)
Kalodiki 19959
Proximal 17

Distal 12

VenographyHigh-probability V/Q PIOPED or Biello5/29 (17) PIOPED8/29 (28%) Biello
Martin 199510
Proximal 114

Distal 41

Ultrasound and venography
High-probability V/Q PIOPED

Pulmonary angiogram if not high-probability

17/155 (11)
From proximal 14/114 (12%)

From distal 3/41 (7%)

Lusiani 199611ProximalUltrasoundHigh-probability V/Q PIOPED43/93 (46)
Decousus 199812ProximalVenographyHigh-probability V/Q PIOPED or pulmonary angiogram52/400 (13)
Paul 199913Proximal?CTA or pulmonary angiogram37/63 (59)
Meignan 20005ProximalVenographyHigh-probability V/Q PIOPED121/379 (32)
V/Q abnormal:

9% ≤ 30 y

33% ≥ 60 y

Girard 200114ProximalVenographyHigh-probability V/Q PIOPED or pulmonary angiogram if V/Q not diagnostic52/193 (27)
López-Beret 200115
Proximal 151

Distal 8

UltrasoundCTA
55/159 (35) acute ± chronic

10/159 (6) chronic


From proximal 55/151 (36%)

From distal 3/8 (38%)

Monreal 200216ProximalUltrasound or venographyHigh-probability V/Q PIOPED258/1000 (26)
Jiménez 200617ProximalUltrasoundHigh-probability V/Q PIOPED or CT28/91 (31)

DVT=deep venous thrombosis; PE=pulmonary embolism; V/Q=ventilation/perfusion scan; PIOPED=Prospective Investigation of Pulmonary Embolism Diagnosis; CTA=computed tomography angiogram.

Table 2. Tier 2. Silent Pulmonary Embolism in Patients with Deep Venous Thrombosis
First Author, Year (Reference)DVT SiteMethod for DVTMethod for PESilent PE n/N (%)Note
Kistner 19722Proximal and distalVenographyV/Q20/52(38)
Browse 19743CalfFUTV/Q6/11(55)
Mostbeck 198018
Iliac 22

Thigh 24

Calf 59

FUT and radionuclear venographyV/Q ≥ 1 mismatch35/105(34)
Symptomatic and silent PE

From pelvic 17/22 (77%)

From thigh 16/24(67%)

From calf 27/59(46%)

Plate 198519ProximalVenographyV/Q ≥ 1 mismatch16/49(33)
Dorfman 198720
Proximal 49

Distal 9

Venography
High-probability V/Q

McNeil

17/58(29)
From proximal 17/49 (35%)

From distal 0/9 (0%)

Huisman 198921
Proximal 78

Distal 11

VenographyV/Q ≥ 1 segmental mismatch45/89(51)
Cuppini 199122ProximalVenography
High-probability V/Q

McNeil

59/100(59)
Hirsch 199123
Vena cava 2

Proximal 14

Calf 4

Axillary 1

VenographyV/Q ± pulmonary angiogram8/21(38)
Partsch 199224Proximal extending to pelvisRadionuclear venographyV/Q ≥ 1 mismatch69/139(50)
Monreal 199225
Proximal 160

Distal 40

Venography
High-probability V/Q

Biello

76/346(22)
From proximal 72/160 (45%)

From distal 4/40 (10%)

Nielsen 199426
Proximal 72

Distal 15

VenographyHigh-probability V/Q43/87(49)
From thigh 38/72 (53%)

From calf 5/15 (33%)

Tomkowski 199627ProximalVenographyV/Q8/18(44)
Venosi 199728ProximalUltrasoundV/Q ≥ 2 defects8/8(100)
Schellong 199929ProximalUltrasoundSPECT ≥ 1 mismatch81/122(66)
Partsch 200130
Proximal 1031

Distal 239

Ultrasound and/or venography or radionuclear venographyV/Q421/1270(33)
Symptomatic and silent PE:

From pelvic 190/356 (53%)

From thigh 355/675 (53%)

From calf 84/239 (35%)

Jünger 200631ProximalUltrasound or venographyV/Q or CTA or pulmonary angiogram50/102(49)

DVT=deep venous thrombosis; PE=pulmonary embolism; FUT=fibrinogen uptake test; V/Q=ventilation/perfusion scan; SPECT=single photon emission-computed tomography; CTA=computed tomography angiogram.

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Results 

Twelve Tier 1 studies and 16 Tier 2 studies met the inclusion criteria. Among Tier 1 studies, silent pulmonary embolism, based on pooled data, was detected in 703 of 2656 patients (27%) with deep venous thrombosis5, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17 (Table 1). Among Tier 2 studies, silent pulmonary embolism, based on pooled data, was detected in 962 of 2577 patients (37%) with deep venous thrombosis2, 3, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31 (Table 2). Altogether, by recognizing that there was heterogeneity in the methods of diagnosis, silent pulmonary embolism was diagnosed in 1665 of 5233 patients (32%) with deep venous thrombosis.2, 3, 5, 7, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31

By considering only those with proximal deep venous thrombosis, the prevalence of silent pulmonary embolism was 600 of 2269 (26%) in Tier 1 patients5, 7, 11, 12, 13, 14, 16, 17 (Table 1) and 291 of 538 (54%) in Tier 2 patients19, 22, 24, 27, 28, 29, 31 (Table 2). The overall prevalence of silent pulmonary embolism in patients with proximal deep venous thrombosis was 891 of 2807 (32%).5, 7, 11, 12, 13, 14, 16, 17, 19, 22, 24, 27, 28, 29, 31 In 5 investigations, comparisons were made of the prevalence of silent pulmonary embolism with proximal and distal deep venous thrombosis.10, 15, 20, 25, 26 In those with proximal deep venous thrombosis, silent pulmonary embolism occurred in 196 of 546 patients (36%) compared with 15 of 113 patients (13%) with distal deep venous thrombosis (P<.0001) (Table 1, Table 2). In an investigation of proximal deep venous thrombosis that extended into the pelvic veins, 69 of 139 patients (50%) showed silent pulmonary embolism24 (Table 2).

Larger perfusion defects occurred more frequently in patients with deep venous thrombosis of the thigh or pelvic veins than in those with distal deep venous thrombosis.18 Silent emboli may be extensive and involve central pulmonary arteries.15, 34, 35 Some reported involvement of more than 60% of the pulmonary circulation in patients with silent pulmonary embolism.23 The CT angiogram of a patient in our clinic with massive pulmonary embolism who was entirely asymptomatic is shown in Figure 1. The CT angiogram was obtained as a baseline evaluation for symptomatic deep venous thrombosis.

  • View full-size image.
  • Figure 1. 

    CT pulmonary angiogram obtained for baseline evaluation in a 46-year-old man with deep venous thrombosis. The patient had no signs or symptoms suggestive of pulmonary embolism. A saddle embolus in the left and right main pulmonary arteries is shown.

Several studies have shown that recurrent pulmonary embolism was more frequent among patients treated for deep venous thrombosis who had silent pulmonary embolism (25/488 [5.1%]) than was a first pulmonary embolism in patients who had deep venous thrombosis but did not have silent pulmonary embolism (7/1093 [0.6%]; P<.0001),5, 16, 22, 31 although one investigator found no difference in the prevalence12 (Table 3). Nielsen et al26 reported the progression of silent pulmonary embolism in 10 days in 13% of patients treated with anticoagulants. The rate of progression was not higher in untreated patients with silent pulmonary embolism (8%).26 Some patients with silent pulmonary embolism died suddenly, and fatal recurrent pulmonary embolism could not be excluded.5

Table 3. Pulmonary Embolism Treatment for Deep Venous Thrombosis
First Author, Year (Reference)Recurrent PE with Initial Silent PE n/N (%)New PE with No Initial Silent PE n/N (%)Clinically Apparent New or Recurrent PE n/N (%)Follow-up Method
Cuppini 1991223/59(5)0/41(0)2/3(67)Routine V/Q day 10
Meignan 200053/121(2.5)2/258(0.8)5/5(100)V/Q if suspected PE
Monreal 2002169/258(3.5)4/742(0.5)13/13(100)V/Q if suspected PE
Jünger 20063110/50(20)1/52(1.9)6/11(55)Routine V/Q or CTA days 10-12

PE=pulmonary embolism; V/Q=ventilation/perfusion scan; CTA=computed tomography angiogram.

The data suggested an increased prevalence of silent pulmonary embolism with aging. Among patients with proximal deep venous thrombosis, silent pulmonary embolism was present in 14% of those aged less than 40 years, 22% of those aged 40 to 70 years, and 40% of those aged 70 years or more.36 López-Beret et al15 similarly showed silent pulmonary embolism in 18% of patients aged less than 40 years, in 30% of patients aged 41 to 70 years, and in 42% of patients aged 71 years or more. Meignan et al5 showed abnormal ventilation-perfusion lung scan results (not necessarily proven pulmonary embolism) in 9% of patients aged 30 years or less and in 33% of patients aged 60 years or older. Data were insufficient to assess whether there was a gender difference in the prevalence of silent pulmonary embolism.

In patients who had routine screening after treatment for deep venous thrombosis, the prevalence of new silent pulmonary embolism was 103 of 1893 (5%), and the prevalence of clinical pulmonary embolism was 36 of 1893 (2%)7, 12, 19, 22, 29, 30, 31 (Table 4).

Table 4. Recurrent Pulmonary Embolism in Treated Patients with Deep Venous Thrombosis Who Had Routine Screening
First Author, Year (Reference)DVT SiteTreatmentPE on Rx No. 1TreatmentPE on Rx No. 2All PE on All RxFollow-up
Plate 198519ProximalA/C
1/29 (3.4) clinical

5/29 (17.2) silent

Thrombectomy + A/C
0/20 (0) clinical

4/20 (20) silent


1/49 (2.0) clinical

9/49 (18.4) silent

1mo
Girard 19877ProximalA/C
2/50 (4) clinical

1/50 (2) silent

15d
Cuppini 199122ProximalA/C
2/100 (2.0) clinical

1/100 (1.0) silent

10d
Decousus 199812ProximalA/C
5/200 (2.5) clinical

4/200 (2.0) silent

IVC Filter
2/200 (1.0) clinical

0/200 (0) silent


7/200 (3.5) clinical

4/200 (2.0) silent

12d
Schellong 199929ProximalBed rest + A/C
1/59 (2) clinical

9/59 (15) silent

Ambulate + A/C
0/63 (0) clinical

14/63 (22) silent


1/122 (0.8) clinical

23/122 (19) silent

8-10 d
Partsch 200130
Proximal 1031

Distal 239

Bed rest + A/C Ambulate + A/C
17/1270 (1.3) clinical

60/1270 (4.7) silent

10d
Jünger 200631ProximalBed rest + A/C
6/102 (5.9) clinical

5/102 (4.9) silent

5d

DVT=deep venous thrombosis; PE=pulmonary embolism; Rx=treatment; A/C=anticoagulants; IVC=inferior vena cava.

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Discussion 

The prevalence of silent pulmonary embolism in patients with deep venous thrombosis (27%,) according to pooled data in Tier 1 patients was based primarily on the diagnosis of pulmonary embolism by a high-probability interpretation of the ventilation-perfusion lung scan using PIOPED criteria. This is a conservative estimate of the prevalence of silent pulmonary embolism. Only 103 of 252 patients with pulmonary embolism (41%) in PIOPED had a high-probability ventilation-perfusion lung scan.37 Therefore, many additional Tier 1 patients may have had silent pulmonary embolism that was not diagnosed because of stringent ventilation-perfusion lung scan criteria. The prevalence of silent pulmonary embolism in Tier 2 patients (37%) may indicate a higher proportion of patients with silent pulmonary embolism by diagnosing some with less stringent criteria than the PIOPED criteria.

The prevalence of silent pulmonary embolism in patients with proximal deep venous thrombosis was higher than in those with distal deep venous thrombosis. This is concordant with evidence that patients with proximal deep venous thrombosis are more likely to have a symptomatic pulmonary embolism than those with distal deep venous thrombosis.38 Sparse data showed a trend suggestive of a higher prevalence of silent pulmonary embolism with aging. The prevalence of symptomatic pulmonary embolism has been shown to increase exponentially with age.39

The prevalence of fatal recurrent pulmonary embolism in symptomatic patients with pulmonary embolism has been shown to be greater than the prevalence of fatal pulmonary embolism in patients with deep venous thrombosis.40 In patients with silent pulmonary embolism, the risk of recurrent pulmonary embolism was higher than the risk of a first pulmonary embolism in patients with only deep venous thrombosis5, 16, 22, 31 (Table 3), but we have no data on the comparative risks of fatal recurrent pulmonary embolism in patients with silent pulmonary embolism.

A strength of this review is the large number of investigations that include 1665 patients with silent pulmonary embolism. A weakness of this review is that there was heterogeneity in the methods used for detection of silent pulmonary embolism.

The 32% prevalence of silent pulmonary embolism in patients with deep venous thrombosis suggests that routine screening for silent pulmonary embolism might be considered. Routine screening would give a baseline for comparison with future imaging studies if the patient subsequently were to become symptomatic and prevent a misdiagnosis of failure of therapy. Routine screening also would provide a more comprehensive evaluation and better understanding of a patient's pathophysiology. Hospitalization would need to be considered if silent pulmonary embolism were shown. These advantages of screening need to be balanced with cost, time for evaluation, and additional exposure to radiation.

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Conclusions 

Approximately one third of patients with deep venous thrombosis have silent pulmonary embolism, and this estimate is conservative. Irrespective of the advantages and disadvantages of routine screening for silent pulmonary embolism, the data clearly indicate that silent pulmonary embolism is frequent in patients with deep venous thrombosis.

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 Funding: None.

 Conflict of Interest: None of the authors have any conflicts of interest associated with the work presented in this manuscript.

 Authorship: All authors had access to the data and played a role in writing this manuscript.

PII: S0002-9343(09)01111-5

doi:10.1016/j.amjmed.2009.09.037

The American Journal of Medicine
Volume 123, Issue 5 , Pages 426-431, May 2010

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