ABSTRACT

Based on the current evidence, a subsolid lesion, being located in the lower lobe, the presence of pneumothorax or hemorrhage, and lesions located above the left atrium were significant risk factors for air embolism.

A total of 154 cases of air embolism following CT-guided PTNB were reported. The reported incidence was 0.06% to 4.80%, and 35 (22.73%) patients were asymptomatic. An unconscious or unresponsive state was the most common symptom (29.87%). Air was most commonly found in the left ventricle (44.81%), and 104 (67.53%) patients recovered without sequelae. Air location (P < 0.001), emphysema (P = 0.061), and cough (P = 0.076) were associated with clinical symptoms. Air location (P = 0.015) and symptoms (P < 0.001) were significantly associated with prognosis. Lesion location [odds ratio (OR): 1.85, P = 0.017], lesion subtype (OR: 3.78, P = 0.01), pneumothorax (OR: 2.16, P = 0.003), hemorrhage (OR: 3.20, P < 0.001), and lesions located above the left atrium (OR: 4.35, P = 0.042) were significant risk factors for air embolism.

The databases of PubMed, Embase, Web of Science, Wanfang Data, VIP information, and China National Knowledge Infrastructure were searched on January 4, 2021, for studies reporting the occurrence of air embolisms following CT-guided PTNB. After study selection, data extraction, and quality assessment, the characteristics of the included cases were qualitatively and quantitatively analyzed.

To quantitatively analyze the risk factors for air embolism following computed tomography (CT)-guided percutaneous transthoracic needle biopsy (PTNB) and qualitatively review their characteristics.

Main points

• Air embolism is a rare but potentially fatal complication of computed tomography-guided percutaneous transthoracic needle biopsy.

• The most common symptoms of air embolism were an unconscious or unresponsive state, hemiplegia, hypotension, and cardiopulmonary arrest; the air was most commonly located in the left ventricle, aorta, and cerebral artery.

• Patients with emphysema, cough, and air located in the left heart, aorta, cerebral artery, and coronary artery were more likely to develop clinical symptoms than patients without these conditions; air location and symptoms were significantly related to patient prognosis.

• Lesion location (lower lung lobe), lesion subtype (subsolid), pneumothorax, hemorrhage, and lesions located above the left atrium were significant risk factors for air embolism.

Lung cancer is the leading cause of cancer incidence and mortality worldwide; with 2.1 million new cases and 1.8 million deaths in 2018, it represents approximately 18.4% of all cancer deaths.¹ As 70% of lung cancers are discovered in advanced stages and are unresectable, needle biopsy techniques are the primary diagnostic methods.² These techniques include computed tomography- (CT) or ultrasound-guided percutaneous transthoracic needle biopsy (PTNB) and endobronchial ultrasound-guided biopsy.³ Endobronchial ultrasound-guided biopsy is best suited to central lesions. The use of ultrasound-guided PTNB is limited by its low resolution and is suitable only for lesions of the peripheral lung, chest wall, and mediastinum.⁴ CT-guided PTNB is the most widely used technique due to its high-resolution display of lung lesions, its wide availability to both central and peripheral lung lesions, and its minimal invasiveness and high accuracy.^5,6

The most common complications of CT-guided PTNB are pneumothorax and hemorrhage.^7,8 Air embolisms are rare but potentially fatal complications.^7,9 The direct injection of 2 mL of air into the cerebral circulation is enough to be fatal, and just 0.5–1.0 mL of air injected into a coronary artery can cause cardiac arrest.¹⁰ The clinical features of air embolism vary from confusion to stroke, arrhythmia, cardiac ischemic features, loss of consciousness, and death.

As the incidence of air embolism is rare, few studies have systematically reported the characteristics and risk factors for air embolism following CT-guided PTNB. Thus, we conducted this systematic review and meta-analysis to qualitatively summarize the characteristics of air embolism following CT-guided PTNB and quantitatively analyze its risk factors.

Methods

This manuscript was reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.¹¹ Ethical approval was not required.

Search strategy

A literature search was performed on January 4, 2021, on the PubMed, Embase, and Web of Science databases and on three Chinese databases (Wanfang Data, VIP information, and China National Knowledge Infrastructure) using combinations of the following search terms and their synonyms and variations without time and language restrictions: “lung,” “chest,” “biopsy,” “air embolism,” and “systematic air embolism.” Medical subject headings were applied if available. The reference lists of the retrieved articles, including reviews, were searched manually for other relevant studies. Two authors performed the search independently and reviewed all the identified publications for inclusion using predetermined criteria.

Inclusion criteria

The inclusion criteria were (a) air embolism defined as air density in the cardiovascular system found on CT images and (b) if air embolism was found during, immediately after, or at least in a clear temporal coincidence with CT-guided PTNB. The exclusion criteria were (a) air embolism caused by trauma, transbronchial lung biopsy, CT-guided marking of lung lesions, or CT-guided radiofrequency ablation other than CT-guided biopsy; (b) comments and review articles in which the exact data of patients with air embolism could not be extracted; and (c) studies reported neither in Chinese nor in English.

Data extraction and quality assessment

A standardized extraction form was used to collect the characteristics of the study: (a) study characteristics, including the first author, publication year, and country; (b) patient characteristics, including age and sex; (c) lesion characteristics, including location (upper, middle, or lower lobe), diameter (maximum axial diameter of the lesion), and cavity contained in the lesion; (d) CT-guided biopsy characteristics, including the number of biopsies, the diameter of the biopsy needle, patient’s position when biopsied, and the use of the coaxial biopsy technique; (e) complications, including pneumothorax, pulmonary hemorrhage or hemoptysis, and cough, and (f) the location of air in the cardiovascular system (the air location in each patient was analyzed individually), clinical symptoms, treatments, and prognoses.

The methodological quality of the studies included in the meta-analysis was assessed using the Newcastle–Ottawa Scale.¹² Data extraction and quality assessment were performed independently by two reviewers, and any disagreement was resolved by consensus.

Statistical analysis

Information about the number of air embolism cases, patient characteristics, lesions, biopsy processes, treatments, and prognoses was extracted from the individual cases in the included studies. These clinical characteristics were reported as mean ± standard values or proportions according to whether they were continuous or categorical variables. Differences in these variables in different symptomatic groups and prognostic groups were compared, and a two-sided value of P < 0.05 was considered statistically significant. A chi-squared test or Fisher’s exact test was used for nominal variables, while a Mann–Whitney test was used for continuous variables with an abnormal distribution. The above statistical analyses were performed using SPSS 21.0 software (IBM).

Odds ratios (ORs) and corresponding 95% confidence intervals (CIs) were used to assess the strength of the association between the different factors and the occurrence of air embolism. Heterogeneity between different studies was evaluated by an I² test, with values of 25%, 50%, and 75% indicating low, moderate, and high heterogeneity, respectively. A random-effects model (the DerSimonian–Laird model) was used if I² > 50% or P ≤ 0.01. Otherwise, a fixed-effects model (the Mantel–Haenszel model) was used. Publication bias was evaluated using a Begg’s funnel plot. Differences were considered statistically significant if P > 0.05. Statistical analyses were performed using STATA 12.0 (StataCorp).

Results

Study selection and characteristics

Figure 1 presents this study’s PRISMA flow diagram, which summarizes the screening process and the reasons for exclusion. A total of 104 studies^{13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116} that reported the characteristics of air embolism after CT-guided PTNB were included in the systematic review (Supplementary Table 1). Five studies^{99,100,101,117,118} that reported the risk factors for air embolism were included in the quantitative meta-analysis (Supplementary Table 2).

Figure 1

Table 1

Table 2

Qualitative analysis

A total of 154 patients from 104 studies were included. The reported incidence of air embolism after CT-guided PTNB ranged from 0.06% to 4.80%. The most common symptoms were an unconscious or unresponsive state (29.87%), hemiplegia (16.23%), hypotension (14.29%), and cardiopulmonary arrest (14.29%) (Supplementary Table 3). Thirty-five patients (22.73%) were asymptomatic. Air was most commonly found in the left ventricle (44.81%), aorta (40.91%), cerebral artery (29.87%), coronary artery (22.73%), and left atrium (14.94%) (Supplementary Table 4). Air is not always present present in one site alone, but in multiple locations at the same time.

Table 3

Air location was significantly associated with the occurrence of clinical symptoms (P < 0.001) (Table 1), with air located in the cerebral artery, coronary artery, aorta, and left heart the most likely to result in clinical symptoms. Similarly, patients with emphysema and cough were the most likely to develop clinical symptoms (P = 0.061 and 0.076, respectively). Air location (P = 0.015) and symptoms (P < 0.001) were also significantly associated with prognosis (Table 2), with air located in the pulmonary vein/artery (100%), left heart (86.42%), aorta (78.94%), and right heart (75%) most likely to have the best outcomes. Of the 154 patients, 144 reported clinical outcomes, 104 (67.53%) recovered without sequelae, 21 (13.63%) patients recovered with sequelae, and 19 (12.34%) patients died. All asymptomatic patients recovered without sequelae.

Table 1

Table 2

Quantitative analysis

As shown in Table 3, the risk factors for air embolism following CT-guided PTNB were quantitatively analyzed. Data from 7.811 patients were extracted^{99,100,101,118} to analyze the relationship between air embolism and lesion location. The pooled OR was 1.85 (95% CI: 1.12–3.05, P = 0.017) (Figure 2). Data from 5.798 patients^{99,100,101,118} were extracted to analyze the relationship between air embolism and lesion subtype. The pooled OR was 3.78 (95% CI: 1.37–10.45, P = 0.01) (Figure 3). Data from 7.633 patients^{99,100,101,117,118} were extracted to analyze the relationship between pneumothorax and air embolism. The pooled OR was 2.16 (95% CI: 1.31–3.57, P = 0.003) (Figure 4). Data from 7.397 patients^{99,100,101,117,118} were extracted to analyze the relationship between air embolism and hemorrhage. The pooled OR was 3.20 (95% CI: 1.95–5.26, P < 0.001) (Figure 5). Data from 4.464 patients were extracted^99,117,118 to analyze the relationship between air embolism and lesion location above the level of the left atrium. The pooled OR was 4.35 (95% CI: 1.06–17.86, P = 0.042) (Figure 6). The funnel plots did not reveal any publication bias.

Table 3

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Data from five studies^{99,100,101,117,118} were used to analyze the relationship between air embolism and patient gender; the pooled OR was 0.99 (95% CI: 0.64–1.54, P = 0.979). The relationship between emphysema and air embolism was analyzed in data from four studies;^{99,100,101,118} the pooled OR was 0.96 (95% CI: 0.58–1.61, P = 0.884). Data from five studies^{99,100,101,117,118} were used to analyze the relationship between air embolism and biopsy position; the pooled OR was 1.10 (95% CI: 0.24–5.16, P = 0.901). Data from three studies^99,100,101 were used to analyze the relationship between air embolism and the use of the coaxial method; the pooled OR was 1.93 (95% CI: 0.66–5.64, P = 0.228). Data from two studies (100,118) were used to analyze the relationship between air embolism and needle-tip location; the pooled OR was 0.46 (95% CI: 0.11–1.94, P = 0.293).

Discussion

This study qualitatively summarized the characteristics of air embolism after CT-guided PTNB and quantitatively analyzed the risk factors for air embolism. The most common symptoms of air embolism were an unconscious or unresponsive state, hemiplegia, hypotension, and cardiopulmonary arrest. Air was most commonly found in the left ventricle, aorta, cerebral artery, and coronary artery. Patients with emphysema, cough, and air located in the left heart, aorta, cerebral artery, and coronary artery were more likely to develop clinical symptoms than patients without these conditions, and air location and symptoms were also significantly related to patient prognosis. Lesion location (lower lung lobe), lesion subtype (subsolid), pneumothorax, hemorrhage, and lesions located above the left atrium were significant risk factors for air embolism.

The reported incidence of air embolism after CT-guided PTNB was 0.06% to 4.80%. This varied because the controlled CT scan after CT-guided PTNB was limited to the target area, and some asymptomatic air embolism cases were not found. A study led by Monnin-Bares showed that by limiting the volume of the post-procedure CT scan to the target area, the rate of air embolism detection was just 1% instead of 4.8%.¹¹⁸ However, the good news is that, usually, these asymptomatic air embolisms will not have serious consequences. Therefore, doctors should weigh up the risk of increased radiation exposure from an enlarged scanning area against the expected benefits of an early diagnosis.

The CT-guided PTNB of lesions in the lower lobe is more likely to result in air embolism than a biopsy performed in other lobes. This difference may be due to gravity, resulting in larger vessels in the lower lobes and a more obvious respiratory motion. Thus, procedures performed in the lower lobe may pose a higher risk of injuring the veins and causing air embolism.¹⁰¹ Additionally, the respiratory motion of the lung may complicate the procedure and necessitate a high number of needle redirections to reach the lesion, leading to increased injury of the pulmonary vein and airway.¹⁰¹ Usually, a prone or lateral position with lesions on the upper side is selected to perform a CT-guided PTNB of lesions in the lower lobe. In areas higher than the left atrium, the pressure in both the pulmonary artery and alveoli is greater than that in the pulmonary vein.¹¹⁹ If a bronchopulmonary venous fistula or an alveolopulmonary vein fistula forms, the air is more likely to enter the pulmonary vein, resulting in air embolism. In fact, our study found that lesions located above the level of the left atrium are a risk factor for air embolism.

Some studies recommend transthoracic biopsy with the patient in an ipsilateral-dependent position to prevent air embolism.¹¹⁷ Even though this approach has been shown to decrease the rate of pneumothorax, it is related to increased alveolar hemorrhage.¹¹⁷ Additionally, this position may complicate the biopsy process, as the biopsy must pass through more lung area. The choice of the transthoracic biopsy position is still debatable, and we must consider the accuracy and safety of the procedure comprehensively.

Pneumothorax and hemorrhage are also risk factors. There may be two explanations for this: the first is that the presence of pneumothorax and hemorrhage means that alveolar, bronchial, or pulmonary vessels are injured. This injury can lead to a bronchovenous fistula, increasing the risk of air embolism. The second is that when hemorrhage is accompanied by cough, the intrapulmonic pressure is increased, resulting in air embolism.¹¹¹ Therefore, when a lung biopsy is performed, patients should try to avoid coughing or cough as little as possible during and after the procedure. For patients who cough frequently, medicine can be used to control their coughing before biopsy.

The lesion subtype is another risk factor. Subsolid nodules contain ground-glass opacities, which do not cover the normal parenchymal structures, including the airways and vessels, and can be visualized on chest CT images.¹²⁰ These normal parenchymal structures in the nodules increase the opportunity for air embolism during the biopsy.

Only three studies analyzed if the coaxial method was a risk for air embolism, with the results showing that it was unrelated to air embolism. In addition, only two studies analyzed if the needle-tip location was a risk factor for air embolism. Our analysis showed that it was not a risk factor; however, future studies should investigate this further.

The optimal positioning of patients following air embolism is controversial.¹⁰⁰ Some patients were placed in the right lateral decubitus or Trendelenburg position when air embolism occurred, while some studies recommend not changing the biopsy position. However, turning a patient from a prone position to a supine position should be avoided, as it can facilitate the antegrade passage of air.¹²¹ In addition to position, 100% oxygen should be administered promptly to assist nitrogen–oxygen exchange within the air bubbles and accelerate their resorption.¹²² The most effective treatment for air embolism is hyperbaric oxygen therapy, which can improve the oxygenation of the affected tissue and dissolve emboli by increasing nitrogen reabsorption.⁸¹ In our analysis, the Trendelenburg position and hyperbaric oxygen therapy were not related to patient outcome; however, further studies are required on this topic.

Our study has some limitations. First, because of limited access to all the databases and the language barrier to understanding literature not published in English or Chinese, we searched only the databases suggested by the Cochrane Reviewer's Handbook and evaluated literature published only in English and Chinese. Second, the number of studies suitable for quantitative analysis was limited, and they differed in terms of factors related to air embolism; therefore, some factors were not quantitatively analyzed. Some factors, for example, the proximity of the targeted lesion to the segmental or subsegmental airways or vascular structures (especially the pulmonary veins), may relate to air embolism but were not evaluated in the original studies. Third, most studies included were case reports; hence, data from these studies were incomplete. Fourth, in most institutions, the extent of the post-procedure CT scan was limited to the target nodule area, so some asymptomatic air embolisms may not have been found. This may have introduced bias when analyzing the risks related to asymptomatic and symptomatic air embolism following CT-guided PTNB. Finally, we analyzed only air embolism following CT-guided PTNB without considering other techniques (e.g., ultrasound-guided PTNB); as the techniques are used for different types of lung lesions, the complication rates may also differ. Additional studies can be undertaken to analyze the characteristics and risk factors for air embolism with other techniques.

Conclusion

Based on current evidence, lesion location (lower lobe) and subtype (subsolid), pneumothorax, hemorrhage, and lesions located above the left atrium were significant risk factors for air embolism following CT-guided PTNB. The most common symptoms of air embolism were an unconscious or unresponsive state, hemiplegia, hypotension, and cardiopulmonary arrest. The air was most commonly located in the left ventricle, aorta, cerebral artery, and coronary artery. Emphysema, cough, and air location were related to patient symptoms, and air location and symptoms were significantly associated with patient outcomes.

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