Frequency and Risk Factors for Air Embolism in Computed Tomography Fluoroscopy–Guided Biopsy of Lung Tumor With the Use of Noncoaxial Automatic Needle : Journal of Computer Assisted Tomography

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Frequency and Risk Factors for Air Embolism in Computed Tomography Fluoroscopy–Guided Biopsy of Lung Tumor With the Use of Noncoaxial Automatic Needle

Maehara, Yosuke MD; Miura, Hiroshi MD, PhD; Hirota, Tatsuya MD, PhD; Asai, Shunsuke MD; Okamoto, Toshiyuki MD; Ohara, Yu MD; Yamada, Kei MD, PhD

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Journal of Computer Assisted Tomography 47(1):p 71-77, 1/2 2023. | DOI: 10.1097/RCT.0000000000001376
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Among various complications in percutaneous computed tomography (CT)–guided lung biopsy, air embolism is known as one of the rare but serious events. Before 2000, a few case reports of air embolism with serious symptoms, including cerebral infarction, myocardial infarction, and death, were published.1 In 2006, Tomiyama et al1 conducted the first nationwide research study of a large number of biopsy cases using a multicenter survey and reported that the rate of symptomatic air embolism was 6 cases among 9783 biopsies, resulting in an incidence rate of 0.061%. The incidence is higher and variable in more recent studies that undertook retrospective investigation, with rates ranging from 0.16% to 4.8.2–9 These rates of radiological incidences have been increasing because of the detection of asymptomatic cases by CT scanning the whole chest, including the heart and aorta, just after biopsy.10 The rates are not negligible, even if they happen to be asymptomatic. If air travels into the systemic circulation without the operator knowing, especially when the patient's position changes, potential risk of myocardial and cerebral infarctions increases.11–13 Early detection of air in the systemic circulation on CT is important to reduce the risk of those fatal conditions.

Another important step to reduce the fatal risk of air embolism is to evaluate the risk factors related to the biopsy procedures.6 There have been several known risk factors, such as depth of the needle in the lesion, needle tip position outside of the nodule, endotracheal anesthesia, lesion location above the level of the left atrium (LA), lower lobe location, occurrence of parenchymal hemorrhage, larger biopsy needle, coughing during the procedure, number of samples, and prone or right-sided lateral decubitus patient positioning.4–9 The coaxial biopsy method is a widely used method for lung biopsy and is known to be highly accurate.14,15 In the coaxial biopsy method, after advancing of the coaxial needle near the target tumor, the internal stylet is removed and then the biopsy needle is inserted through the lumen. This coaxial biopsy method makes it much easier to repeat sampling, although the lumen of coaxial needles after removal internal stylet could be the route of extracorporeal air inflow to the pulmonary vein.6 Therefore, to prevent the air migration into the lumen of coaxial needle, it is recommended to occlude the needle hub with a finger and use water-seal or hemostatic valves.10,16

Another approach is use of the noncoaxial automatic needle with CT fluoroscopy. This method also has high accuracy.17–19 In noncoaxial method, biopsy needle, which has no needle lumen, is directly punctured without coaxial needle; therefore, there could be no possibility of extracorporeal air migration through the coaxial needle lumen. The purpose of this study was to examine the radiological incidence and risk factors for air embolism during CT fluoroscopy–guided lung biopsy using the noncoaxial automatic needle.


Study Design and Patients

This retrospective single-institutional study was approved by the institutional review board (ERB-C-1332). Opt-out consents were obtained for retrospective use of data.

A total of 232 cases were consecutively biopsied at our institution between February 2014 and December 2019. Fifteen cases of coaxial needle use for a large sample volume and 13 cases of noncoaxial semiautomatic needle use for cases with close position to the aorta and other organs were excluded. Patients with the following contraindications for lung biopsy were excluded: patients who could not follow instructions such as breath holding; those who were unable to stay in the appropriate position; those with refractory coagulopathy (eg, international normalized ratio ≥1.5, platelet count <50,000/mm3); and those with lesions suspected to be of vascular origin; and those with severe respiratory disease. We evaluated 204 CT fluoroscopy–guided lung biopsies in this study. The study group included 127 men and 77 women with an average age of 70.6 years (range, 26–89 years). All procedures were performed under local anesthesia. None of the patients had positive-pressure ventilation.

Computed Tomography Fluoroscopy–Guided Lung Biopsy

All procedures were performed under CT fluoroscopy guidance (Aquilion 16; Canon Medical Systems, Otawara, Japan) by either experienced board-certified interventional radiologists or by radiologists under the supervision of an experienced board-certified interventional radiologist. A whole-chest CT scan was obtained to plan the puncture routes. Needle paths that did not cross the relatively large bronchi and vessels were determined. After administration of local anesthesia, an 18-gauge automatic biopsy needle (BARD Monopty, 18 G, 22 mm; Becton, Dickinson and Company, Franklin Lakes) without coaxial needle was inserted under CT fluoroscopy (1-mm thickness) of 3 contiguous sections, including slices 1 mm cranial and caudal to the central slice. An I-I device (Hakko Medical, Chikuma, Nagano, Japan) was used to assist in precisely advancing the needle while avoiding irradiation to the operator's hands by maintaining a distance from the CT gantry.20 We advanced the needle near the tumor under inspiratory breath holding during CT fluoroscopy. After confirming the best position of the needle tip, we pulled the trigger to obtain the specimen. While the needle was advanced under CT fluoroscopy, the assistant used the panel to move the bed to visualize the needle tip and the tumor on the monitor. Immediately after trigger firing, while the patient continued breath holding, the assistant moved the bed to check the cranial/caudal slices to ensure that the lesion had been properly penetrated. Then, the breath was released and the needle was removed. The collected specimens were placed in 10% formalin for pathological examination. Immediately after the procedure, a whole-chest CT scan (1-mm thickness) was performed to evaluate complications.

Investigated Parameters

Whole-chest CT images obtained immediately after biopsy were retrospectively evaluated for air embolism by consensus of 2 radiologists (with 17 and 9 years of experience) who were blinded to the clinical information. Air embolism was defined as low density in the LA, left ventricle (LV), pulmonary vein, coronary artery, or aorta. A Hounsfield unit value of less than −200 was indicative of air.5

Variables related to the patients, tumors, and procedures were retrospectively collected from the procedure records, as were CT images obtained before, during (ie, CT fluoroscopic images), and after the procedures.

The following patient and tumor variables were collected: patient age, sex, position during procedure, presence of emphysema, location (upper, middle, or lower lobe), axial maximal diameter of the lesion, pathological diagnosis, and operator's experience of the procedure. Types of nodule were designated as follows: lesions with a ground glass opacity (GGO) component of more than 95% as pure GGO lesions, those with a GGO component of less than 5% as solid lesions, and the others as part solid GGO.5

The procedural variables were as hereinafter. The distance to pleura, the needle-pleural angle (in degrees), and the needle penetration depth were measured as shown in the Figure 1A. The level of the lesion relative to the LA was measured as the distance between horizontal lines drawn through the center of the LA and the center of the nodule (Fig. 1B).6 Penetration of a pulmonary vein was evaluated as the needle crossing the pulmonary vein on CT fluoroscopic images. Penetration of the nodule was determined by the presence of the needle tip outside the nodule. Numbers of punctures, pneumothorax, and alveolar hemorrhage were also evaluated.

Measurement examples. A, The distance to pleura was measured as the shortest distance from the pleura. The needle-pleural angle (in degrees) was measured as the angle between the pleura and the needle. Needle penetration depth was measured as the puncture distance from the pleura. B, Level of lesion relative to LA was measured as the distance between horizontal lines drawn through the center of the LA and the center of the nodule. This is a preoperative image of case no. 2 in Table 1.

The technical success of biopsy was defined as the procurement of sufficient material to establish a diagnosis and/or guide treatment decision.21 Complications were categorized according to Cardiovascular and Interventional Radiological Society of Europe guidelines.21 Major complications were those that resulted in prolonged hospital stay, permanent sequelae, or death. Minor complications resulted in no sequelae; these patients only required therapy or short hospital stay.

Statistical Analyses

Radiological incidence of air embolism was defined as the frequency of air embolism depicted on the whole-chest CT after biopsy, including asymptomatic cases.

Univariate analyses were performed with Fisher exact test for categorical values and Wilcoxon rank sum test for numerical values. Data are presented as the average and standard deviation for continuous variables and as frequency for categorical variables. Statistical analyses were performed with JMP 14 (SAS, Cary, NC). A P value less than 0.05 was defined as a significant difference.


The characteristics of patients, tumors, and procedures are shown in Table 1. In 6 cases, pathologically inadequate specimens were obtained, for a technical success rate of 97.1%.

TABLE 1 - Characteristics of Patients, Tumors, and Procedures
Patient age, y 70.6 ± 10.16 (26 to 89)
Sex Male: 127 (62.3%); Female: 77 (37.7%)
Position of patient
 Prone 110 (53.9%)
 Supine 67 (32.8%)
 Right lateral decubitus 12 (5.8%)
 Left lateral decubitus 15 (7.4%)
Emphysema 68 (33.3%)
Type of nodule
 Solid 166 (81.4%)
 Part solid GGO 22 (10.8%)
 GGO 16 (7.8%)
Location (lobe)*
 Upper 109 (53.4%)
 Middle 9 (4.4%)
 Lower 85 (41.7%)
Pathological diagnosis
 Benign 52 (25.5%)
 Malignancy 146 (71.6%)
 NA 6 (2.9%)
Operator's experience of the procedure, y 10.1 ± 3.07 (3 to 19)
Axial diameter of lesion, mm 19.5 ± 15.1 (3.1 to 96.7)
Distance to pleura, mm 10.4 ± 14.6 (0 to 65.2)
Level of lesion relative to LA, mm 53.2 ± 30.8 (−20.5 to 156.3)
Needle-pleural angle, ° 63.1 ± 17.7 (14.1 to 92.9)
Needle penetration depth, mm 35.8 ± 16.4 (11.7 to 94.6)
Penetration of pulmonary vein 60 (29.4%)
Penetration of nodule 144 (70.6%)
No. punctures, times 1.54 ± 0.67 (1 to 4)
Pneumothorax 117 (57.4%)
Alveolar hemorrhage 158 (77.5%)
Values are presented as average ± standard deviation for continuous variables with range in parentheses and as frequency for categorical variables with percentage in parentheses.
*One case was unmeasurable because of extensive adherence to the pleura.
NA indicates not available for pathological diagnosis because of incomplete specimen.

We identified 8 cases of air embolism; therefore, the radiological incidence was 3.92%. The location of the air was in the LA in 5 patients, in the LV in 6 patients, and in the aorta in 5 patients. One patient had air in both the LA and LV, 3 patients had air in the LA, LV, and aorta, and 1 patient had air in both the LV and aorta. In 5 patients, the air was seen in the slice at the puncture location, and in 3 patients, the air was seen at a location remote from the puncture site. The characteristics of these 8 cases are summarized in Table 2. Two of the 8 cases (0.98%) were symptomatic. In both of these cases, air in the LA had been missed by the operators at the time of procedure. Therefore, nonmobilization and Trendelenburg positioning were not performed. The patients were asymptomatic at the operating room; however, after the patients returned to the ward, symptoms related to air embolism occurred.

TABLE 2 - Characteristics of Eight Air Embolism Cases
Age, y/Sex Position Nodule Lobe Size, mm Distance From Lesion to LA, mm Needle Penetration Depth, mm Penetration of Pulmonary Vein Penetration of Nodule Pathological Diagnosis Symptoms
68 M Left lateral Part solid RL 12.2 79.2 61.5 Yes Yes Benign No
75 M* Prone Part solid LL 17.9 43.0 30.5 Yes Yes Malignancy Yes
66 M† Prone Solid RL 23.5 78.8 51.0 Yes Yes Malignancy Yes
82 F Right lateral Part solid LL 18.4 86.6 31.3 Yes Yes Benign No
61 M Supine Solid LU 15.3 49.0 40.1 No Yes Malignancy No
67 M Prone Solid LU 10.4 70.4 30.9 Yes Yes Malignancy No
77 M Prone Solid LL 65.2 71.4 37.5 No No Malignancy No
68 M Prone Solid RL 10.0 81.5 23.7 No Yes Malignancy No
F indicates female; Left lateral, left lateral decubitus; LL, left lower lobe; LU, left upper lobe; M, male; Right lateral, right lateral decubitus; RL, right lower lobe.
*1: The patient had difficulty walking and consciousness disturbance 3 hours after biopsy and urinary retention 6 hours after biopsy. The next day, head and spinal cord MRI were negative. From the course, the patient was diagnosed with spinal cord infarction resulting from air embolism. After 1 week, the symptoms had almost disappeared with pharmacotherapy.
†2: Two hours after biopsy, the patient developed left lower limb paresis. He was diagnosed with cerebral infarction resulting from air embolism according to head MRI the next day. Symptoms improved with pharmacotherapy, but partial symptoms remained.

One patient's symptoms were walking and consciousness disturbance, and urinary retention, which almost disappeared. The other patient's symptom was left lower limb paresis, which partially remained. The other 6 cases had no symptoms related to air embolism. In cases with detection of air embolism, patients were not moved in that position and given 100% oxygen by mask until air disappears on follow-up CT.

Table 3 shows univariate analysis of risk factors of air embolism. Penetration of pulmonary vein was observed in 62.5% in the air embolism group and 28.1% in nonoccurrence group, which was a significant risk factor (P = 0.0478). Most of them were peripheral small pulmonary vein penetration. Regarding the distance from the LA to the target, the average was 70.0 ± 15.8 mm in the air embolism group and 52.5 ± 31.2 mm in the nonoccurrence group (P = 0.0353). Lesion location higher relative to the LA was a significant risk factor for air embolism. The number of punctures was 1.63 ± 0.74 in the air embolism group and 1.53 ± 0.67 in the nonoccurrence group, which was no significantly different (P = 0.708). Operator's experience of the procedure also was not a significant risk factor; 10.5 ± 1.93 years in cases with air embolism and 10.1 ± 3.11 years in the nonoccurrence group (P = 0.471).

TABLE 3 - Univariate Analysis of Air Embolism Cases and Control Subjects
Variable Controls = 196 Cases = 8 P
Axial diameter of lesion, mm 19.5 ± 15.0 21.6 ± 18.2 0.745
Distance to pleura, mm 10.3 ± 14.6 11.9 ± 14.5 0.357
Level of lesion relative to LA, mm 52.5 ± 31.2 70.0 ± 15.8 0.0353
Needle-pleural angle, ° 63.1 ± 18.0 63.4 ± 11.4 0.807
Needle penetration depth, mm 35.7 ± 16.6 38.3 ± 12.4 0.310
Penetration of pulmonary vein, yes 55 (28.1%) 5 (62.5%) 0.0478
Penetration of nodule, yes 137 (69.9%) 7 (87.5%) 0.247
Location, lobe* 0.274
 Upper 107 (54.6%) 2 (25%)
 Middle 9 (4.6%) 0
 Lower 79 (40.3%) 6 (75%)
No. punctures, times 1.53 ± 0.67 1.63 ± 0.74 0.708
Position of patient 0.555
 Prone 105 (53.6%) 5 (62.5%)
 Supine 66 (33.7%) 1 (12.5%)
 Right lateral decubitus 11 (5.6%) 1 (12.5%)
 Left lateral decubitus 14 (7.1%) 1 (12.5%)
Type of nodule 0.0780
 Solid 161 (82.1%) 5 (62.5%)
 Part solid GGO 19 (9.7%) 3 (37.5%)
 GGO 16 (8.2%) 0
Pathological diagnosis 0.878
 Benign 50 (25.5%) 2 (25%)
 Malignancy 140 (71.4%) 6 (75%)
 NA 6 (3.1%) 0
Operator's experience of the procedure (year) 10.1 ± 3.11 10.5 ± 1.93 0.471
Emphysema (Yes) 65 (33.2%) 3 (37.5%) 0.801
Alveolar hemorrhage (Yes) 152 (77.6%) 6 (75.0%) 0.867
Values are presented as average ± standard deviation for continuous variables and as frequency for categorical variables with percentage in parentheses.
P < 0.05 was defined as significant difference.
*One case was unmeasurable because of extensive adherence to the pleura.
NA indicates not available for pathological diagnosis because of incomplete specimen.

The CT fluoroscopic images in Figure 2 show real-time movement of air into the pulmonary vein during needle tip penetration. The automatic biopsy needle was advanced toward the nodule on CT fluoroscopy under inspiratory breath holding (Fig. 2A). After the actuator button was pressed and the cannula and stylet were advanced from the front of the nodule, the needle penetrated the nodule and the pulmonary vein behind the nodule (Fig. 2B). Computed tomography fluoroscopic images were obtained during bed adjustment by the assistant to confirm the needle tip position against the nodule on the same inspiratory breath hold. These images revealed that air had moved into the pulmonary vein and migrated toward the LA (Figs. 2C, D). After confirmation of penetration of the nodule, the needle was withdrawn and the breath hold was released. Whole-chest CT images obtained just after biopsy showed air in the LA and aorta (Fig. 3).

Real-time air movement into pulmonary vein during puncturing needle. This is case no. 2 in Table 1. Computed tomography fluoroscopic images during automatic needle puncture. After confirmation of the needle tip in front of the nodule (A), the cannula and stylet were advanced. The needle penetrated the nodule and a dorsal small branch of the pulmonary vein (B: long arrow). Immediately afterward, air has moved into the pulmonary veins (C: short arrow). The air gradually flowed into the left atrium through the pulmonary veins (D: short arrow). These images were obtained during a single inspiratory breath hold.
Computed tomography image after biopsy. Computed tomography image after biopsy show air in the aorta and left atrium (arrow). Ground glass opacity at the right middle lobe is aspirated hemorrhage.

Major complications other than symptomatic air embolism occurred in 4 cases. One patient had massive hemoptysis requiring tracheal intubation, and the others had severe pneumothorax requiring trocar catheter placement.


In the present study, 8 of the 204 biopsies, including asymptomatic cases, showed air embolism on the whole-chest CT images immediately after biopsy. The radiological incidence was 3.92%. This rate was relatively higher than expected when compared with older past studies, whereas it was about the same when compared with the more recent studies that include asymptomatic cases detected by whole-chest CT right after the procedure.6,9 In our study, whole-chest scanning was also used, which may have increased the overall incidence. In our study, 3 of the 8 cases had air in the left cardiac system or aorta remote from the puncture sites. We thus consider that the whole-chest imaging is of vast importance for detection.

From recent studies and our results, the radiological incidence of air embolisms may be considered to be much more frequent than previously perceived. Many of these detected cases were asymptomatic. However, it is noteworthy that there were a couple of patients in whom air in the LA had been missed at the operating room, and they became symptomatic after returning to the ward. Thus, careful evaluation on whole-chest CT images before repositioning must be routinely undertaken. When air is identified in the left cardiac system or aorta, nonmobilization of patients (and if possible, Trendelenburg positioning) with oxygen therapy should be started immediately, until it disappears on follow-up CT.9

The true mechanism of air embolism remains unknown, but it is possible that there is creation of fistula between the air space and pulmonary vein upon the needle penetration through the lung parenchyma. There are 2 conceivable routes into the pulmonary vein. One is the direct passage of extracorporeal air through the needle lumen (ie, coaxial needle), and another is fistula formation toward the bronchi and alveolar space by the needle path through the aerated lung.9 Because we used the noncoaxial needle, the latter route mentioned previously should be discussed in our study.

It is difficult to define where and how exactly the fistula is formed by histological proof. Some risk factors related to the fistula formation were reported in previous studies, including needle path length through ventilated lung, penetration of nodule, and number of samples.7,9 These factors, however, were not significant in our present study. Instead, the incidence of pulmonary vein penetration by the needle was considerably high. We tried to avoid large pulmonary veins, but we retrospectively found that we were puncturing through small pulmonary veins visible on CT. Notably, we experienced a case in which CT fluoroscopic images captured the real-time air migration into a pulmonary vein at the moment when the needle penetrated the nodule and hit the pulmonary vein behind the nodule (Fig. 2). Jang et al7 reported that needle tip position outside of the nodule was a risk factor for air embolism. There have been other air embolism case reports caused by puncture of a visible pulmonary vein and presence of needle tip in the pulmonary veins.22,23 It is currently unclear how the size of the punctured pulmonary vein relates to air embolism, but the strategy with currently available knowledge is to avoid the visible pulmonary veins on CT, not only along the route to the target but also along the veins behind it.

In the situation of the fistula formation between the pulmonary vein and intra-alveolar space, the pressure gradient between the pulmonary vein and intra-alveolar space becomes one of the most important predisposing factors. When alveolar pressure exceeds the pulmonary venous pressure, air will migrate into it.8,10,16 Recently, Glodny et al6 reported distance between the lesion and the LA as a novel risk factor of air embolism regarding changes of pressure of pulmonary veins. The pulmonary venous pressure around the lesions above the level of the LA is lower than that at other regions; therefore, the alveolar pressure may be greater than the pulmonary venous pressure in these cases.6 In the present study, a higher location of the lesion relative to the LA was also a risk factor. We thus believe that biopsies of the lesions at higher distance from the LA should be avoided or at least planned carefully.

In addition to these issues, changes in intra-alveolar pressure should be another factor that may plan an important role. Regarding the increase in the pressure of intra-alveolar space, coughing and positive-pressure ventilation are some of the well-known important risk factors.16 Presence or absence of coughing and hemoptysis was unfortunately not precisely recorded throughout our series of cases and was not included in the analyses. Although alveolar hemorrhage is known to be a risk factor for air embolism as a factor related to cough and hemoptysis,5,7 it was not significant in this study. Considering about factors influencing intra-alveolar pressure, breath holding during the procedure could be also important. Han et al24 reported that CT-guided lung biopsy under free breathing is effective method with high diagnostic performance and no air embolism case. In this study, most procedures were performed under inspiratory breath holding. The CT fluoroscopic images shown in Figure 2 were obtained on a single inspiratory breath hold. Breath holding after inspiration allows better visualization of the needle tip and the tumor position under CT fluoroscopy,25 but intra-alveolar pressure could be increasing during this process. Some case reports have argued that Valsalva maneuver increased the risk of air embolism.26,27 Valsalva maneuver is defined as forced exhalation against a closed airway, usually performed after a normal or full inspiration.28 Thus, the Valsalva maneuver and breath holding after inspiration are not exactly the same, but they can be similar in terms of increasing alveolar pressure. There is currently not yet any consensus on the optimum way of breath holding during advancement of the biopsy needle, including inspiratory breath holding, expiratory breath holding, or free breathing. We also believe that the relationship between air embolism and the way of breath holding should be considered in the future study.

In most previous studies of air embolism cases using coaxial needles, extracorporeal air migration through the inner lumen of the needle was not negligible as one of the causes in situations where air could easily enter because of risk factors reported in the past. Although we did not use coaxial needles, radiological incidence of air embolism was relatively higher than expected that in cases using coaxial needles.4,6,9 From the results of this study, it is conceivable that the alveolar-pulmonary venous fistula formation could be the main cause of air migration. In addition, it is necessary to consider changes of pressure balance between the pulmonary vein and alveolar space during lung biopsy.

The present study has a few limitations. First, this was a retrospective study in a small number of patients within a single institution. Small sample size led to inclusion of only a few cases of air embolism, and therefore, multivariable statistical analysis could not be performed. Second, we did not directly compare the results between the coaxial and noncoaxial needles. Third, the exact duration of breath holding was not recorded and thus was not taken into account in this study. In addition, we did not compare needle advancement during inspiration, expiration, and free breathing. Further study is needed to investigate the influence of breath holding on air embolism.


In CT fluoroscopy–guided lung biopsy using the noncoaxial automatic needle in this study, the radiological incidence of air embolism on retrospective evaluation of whole-chest CT was almost 4%, including asymptomatic cases. Careful evaluation of air in the left cardiac system and aorta on post biopsy CT before reposition is important to detect asymptomatic air embolism. The risk factors were alveolar-pulmonary venous fistula formation by penetration of pulmonary veins around the lesion, as well as higher intra-alveolar pressure associated with higher lesion locations relative to the LA. It is necessary to avoid these factors during CT fluoroscopy–guided lung biopsy.


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air embolism; automatic needle; complication; CT-guided lung biopsy; noncoaxial needle; CT - computed tomography; GGO - ground glass opacity; LA - left atrium; LV - left ventricle

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