A retrospective analysis of the risk factors associated with systemic air embolism following percutaneous lung biopsy
- Authors:
- Published online on: November 18, 2019 https://doi.org/10.3892/etm.2019.8208
- Pages: 347-352
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Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Percutaneous CT-guided lung biopsy has increasingly been adopted as a validated technology in clinical practice. The most common complications of percutaneous CT-guided lung biopsy are pneumothorax and hemoptysis. In general, treatment is not required, except in a small number of serious cases. Systemic air embolism is one of the rare complications of percutaneous CT-guided lung biopsy that may have serious consequences (1–4). If an air embolism occurs in the coronary or cerebral artery, it may lead to acute myocardial or cerebral infarction, or even death (5–8). However, if the complications are identified early, so that timely and effective treatment measures are taken, the rare and serious complications are usually non-fatal. Hyperbaric oxygen therapy is currently recognized as an effective treatment.
As the complications of systemic circulation air embolism frequently occur in the process of puncture or within a short time after puncture (3,5,7), the operator should be well aware of the symptoms that may accompany the complications. Where air embolism is suspected, head and chest CT should be reviewed immediately after the operation, so as to take treatment measures as soon as possible.
In recent years, as understanding of the complications of percutaneous CT-guided lung biopsy has improved, an increasing number of studies have examined air embolism, but few have performed comprehensive analyses of multiple domestic cases (3,7,8). In the present study, risk factors associated with air embolism following lung biopsy were assessed, based on data collected between 2014 and 2018, and the complications and outcomes of 19 patients who developed air embolism were summarized. In addition, the associated risk factors and treatments were discussed to provide insight into and a reference for the prevention, early detection and treatment of systemic air embolism.
Materials and methods
Patients
A total of 2,026 patients (1,155 males and 871 females) with an average age of 58.7±10.6 years (range, 7–86 years) subjected to percutaneous CT-guided lung biopsy between January 2014 and June 2018 at the Affiliated Hospital of Qingdao University (Qingdao, China) were retrospectively enrolled. Each patient provided written informed consent to undergo percutaneous CT-guided lung biopsy. For patients under 18 years of age, their parents or guardians provided written informed consent. All patients underwent routine CT scanning and certain patients underwent enhanced CT scanning.
Equipment and methods
All patients underwent a routine blood test and coagulation test prior to the percutaneous lung biopsy. Patients with frequent cough were administered cough suppressants and received breath-hold training prior to the test. The puncture sites and positions were selected on the basis of previous CT images of the patients.
CT scanning was performed using a 16-slice CT scanner (Brilliance CT, Philips Healthcare). The scanning range was 3–4 cm above and below the lesion center, the scanning slice thickness was 3–5 mm and the interval between slices was also 3–5 mm. A catheter grid surface tag combined with the CT scanner positioning cursor were used to determine the puncture location, depth and direction. Routine disinfection was performed and the syringe was maintained at a site along the direction of puncture after local anesthesia, and an additional CT scan was performed over the puncture area to confirm the puncture path.
The coaxial cannula needle was quickly advanced through the pleura in a predetermined direction under a breath hold, and CT scanning was performed to observe the tip after the needle reached the preset depth. Subsequently, the puncture angle and depth of the needle were adjusted to ensure that all procedures were performed within the pleura. When the needle was inserted in the lesion or at the edge of the lesion, the needle core was withdrawn, and an 18-G or a 20-G biopsy needle (Bard Biopsy; BD Biosciences) was inserted to complete the sampling procedure. The decision to take a second sample was based on the quality of the first sample obtained and the tolerance of the patient.
All patients underwent a chest CT scan after percutaneous lung biopsy, but only those patients with symptoms of a suspected cerebrovascular air embolism or those with an air embolism in the systemic circulation after the chest CT examination underwent a CT scan of the brain. Chest and brain CT scanning were performed after the puncture to determine whether a systemic air embolism had occurred in the cerebrovascular artery, left atrium, left ventricle, coronary artery, aorta or its three branches. A systemic air embolism was confirmed when CT values <-200 Hounsfield units were observed in two sequential images (9). All patients received careful observation and monitoring of vital signs within 2 h after the operation. In addition, all patients who were confirmed to have systemic air embolism underwent brain MRI examination and color Doppler echocardiography one week later to determine whether they had delayed cerebral infarction or myocardial infarction.
Statistical analysis
The factors that may lead to air embolism were divided into three categories: Patient characteristics (e.g. age and sex), puncture process (e.g. location and depth) and the nature of the lesion (e.g. sampling frequency and time). Statistical analyses were performed using SPSS (version 19.0; IBM Corp.). Independent-sample t-tests were used to evaluate the differences between numerical variables. Pearson χ2 was employed to evaluate the differences between categorical variables. P<0.05 was considered to indicate statistical significance.
Results
The incidence and location of systemic air embolism
A total of 19 cases of systemic air embolism were identified among the 2,026 patients who underwent percutaneous CT-guided lung biopsy, with an incidence rate of ~0.9%. Details of the 19 patients with air embolisms are provided in Table I. Among the 19 patients, 3 (15.8%) had obvious symptoms, Fig. 1 shows the CT of a patient with a small quantity of air in the left ventricle, aorta and in the cerebral blood vessels. Fig. 2 shows a patient with a right coronary artery embolism. Three patients with obvious symptoms were treated with high flow inhalation of 100% oxygen, hypertensive drugs and fluid supplementation. The remaining 16 patients without obvious symptoms were treated with inhalation of pure oxygen only. All 19 patients underwent CT 30 min later, which showed that their air embolism had dissipated. The most common site of the air embolism was the left ventricle (17/19, 89.5%), with other sites including the aorta, left atrium, brachiocephalic trunk, cerebrovascular artery, internal carotid and coronary artery. After one week, the 19 patients with systemic air embolism were examined by brain MRI and color Doppler echocardiography, but no delayed myocardial infarction or cerebral infarction was identified.
Risk factors
The factors predicted to influence systemic air embolism occurrence during percutaneous CT-guided lung biopsy are provided in Table II. The relative location of the lesion above the level of the left atrium during puncture and coughing during the puncture procedure significantly influenced the occurrence of air embolism (P<0.05). No statistically significant differences were identified between any of the other factors.
Discussion
Systemic air embolism is a rare complication of percutaneous CT-guided lung biopsy. A 2006 study described the incidence rate of air embolism after percutaneous CT-guided lung biopsy to be 0.061% (2). However, an increased interest and understanding of this condition led to a study in 2012 to report an incidence of 3.8% (9). One potential reason for this difference in incidence rate is that early studies may only have counted cases with severe symptoms, while most asymptomatic patients were ignored (2,9). According to one study, only 26.1% of air embolism cases were detected during or immediately after biopsy (9). In the present study, a general lung and brain CT examination was performed in all 2,026 patients who underwent percutaneous CT-guided lung biopsy and the incidence of air embolism was 0.9%. A small amount of air had entered the circulation in all 19 patients with systemic air embolism, but 16 of them did not have obvious clinical symptoms. The reason for this may be that these patients have less air entering the systemic circulation and had received high-flow 100% oxygen inhalation therapy after air embolism was discovered. Oxygen inhalation therapy with 100% oxygen dissipates the air within embolized bubbles due to accelerated nitrogen resorption and improves oxygenation of ischemic tissue. The most common site of the air embolism was the left ventricle.
When a substantial amount of air enters the systemic or cerebrovascular circulation or the coronary artery, clinical symptoms, including aphasia, hemiplegia, fainting, arrhythmia, cardiac arrest, a decrease in blood pressure and shock, may arise. In such cases, another chest and brain CT should be performed to confirm the air embolism, and once confirmed, the patient should be rapidly placed in a Trendelenburg position or in the right lateral decubitus position and administered 100% high-flow oxygen. Administration of oxygen is an effective treatment for hypoxia and eliminates air bubbles by establishing a diffusion gradient that favors the egress of air from the bubbles (10). The right lateral decubitus position prevents air from entering the systemic circulation, as the left ventricular outflow tract lies inferiorly, and the air within the left ventricle remains in the non-dependent superior aspect and is positioned away from the aorta (11). However, it may be hypothesized that the probability of air entering the left coronary artery is increased in that position, although no better heart and lung recovery rescue position is available. Therefore, timely intervention and the Trendelenburg position may be a better option. Hyperbaric oxygen therapy is currently recognized as an effective treatment for systemic air embolism, as it eliminates air within embolized bubbles by accelerating nitrogen resorption and improves the oxygenation of ischemic tissues (11–13). However, hyperbaric oxygen therapy is contraindicated for patients with severe emphysema, pulmonary bulla or post-operative pneumothorax.
In the present study, air embolisms occurred in the cerebral circulation and the left internal carotid in 3 of 19 affected patients: One patient was asymptomatic and the others presented with symptoms, including hypotension, convulsions and/or unconsciousness. No clinical sequelae were observed after oxygen therapy. In addition, 1 patient had an air embolism in the right coronary artery and exhibited chest pain, tightness and hypotension-associated shock, but no sequelae remained after timely intervention.
Although the prognosis in this group of 19 patients was good, systemic air embolism may potentially have severe consequences. The prognosis is poor, particularly when the embolism is located in the coronary and cerebral arteries, with a mortality rate of as high as 26.3% (4). Thus, patients with an air embolism should receive focused care to improve their prognoses.
In the present study, coughing during the procedure and the relative location of the lesion above the level of the left atrium during percutaneous CT-guided lung biopsy significantly increased the occurrence of air embolism complications. Usually, the pressure in the pulmonary vein is ~10 cm H2O, but the pressure in the lung may sharply increase to ≥180 cm H2O when the glottis is opened during coughing (14). During the biopsy process, coughing may be provoked by bleeding around the vascular injury site caused by the needle. When the pulmonary pressure increases substantially, alveolar air may easily enter the left atrium through a bronchovenous fistula or other air-containing spaces and pulmonary veins, and then travel to the left ventricle to result in a systemic air embolism. If coughing persists after the extraction of specimens, the procedure should be promptly terminated and a chest CT should be performed as soon as possible to evaluate the risk of air embolism; in addition, patients with frequent cough should be administered medicine to relieve their cough. Numerous studies reporting air embolism caused by coughing have been published in the past decade (15–17).
If the location of the lesion is above the level of the left atrium, the venous pressure around the lesion is relatively low. A higher position results in lower pressure and air more easily enters the systemic circulation through the vulnerable blood vessels. A prone position is one of the risk factors for air embolism, according to previous studies (9,18). However, in the present study, there was no significant difference in the incidence of air embolism between two groups in different positions. The reason for adopting a prone position may be that the patient's lesions are located in the dorsal and basal segments of the lower lobe of the lung (9,19,20). The results of the present study suggest that when the prone position is selected for lesions close to the dorsal pleura the location of the lesion is usually higher than the level of the left atrium, which increases the probability of developing an air embolism. Therefore, the puncture position may not be an independent risk factor, whereas the relative location of the lesion above the level of the left atrium during puncture is a risk factor. In addition, a supine position should be selected if possible during the puncture of the basal segment or the lower lobe of the lung to avoid the complication of an air embolism (9).
Of note, the use of a trocar did not affect the occurrence of air embolisms. The amount of air in a 25-cm trocar is only ~0.017 cm3. This small amount of air does not affect the body, even if it enters the circulation, as according to previous experimental studies on dogs, at least 2–3 ml of air must be injected into the pulmonary veins to be fatal (15). In a previous study (17), lesions located near the bottom of the lungs were intractable due to the large movements associated with breathing, resulting in difficulty establishing a successful puncture. Theoretically, a deeper puncture site is more likely to damage the surrounding blood vessels and cause a systemic air embolism. However, according to the statistical analyses performed in the present study, the average depth in the air embolism group was greater than that in the group without air embolism, though the difference was not statistically significant. In previous studies, additional factors, including the coaxial technique, needle size, bleeding, lesion size of <1 cm and frequency of sampling, were also reported as risk factors, although they remain controversial (3,14,17,19,20). In the present study, no significant differences in the other risk factors assessed were observed between the two groups.
The present study has several limitations. As this was a single-center retrospective study there was inevitably bias in the selection of research subjects. Furthermore, the interaction between different factors was not assessed. In addition, the potential risk factors mentioned above, including the application of coaxial technique, needle size, lesion size and frequency of sampling, are not certain to be independent risk predictors. To confirm this will require future multi-factor logistic regression analysis of further large patient cohorts.
In conclusion, in the present study, the incidence of air embolism complications was ~0.9%. Cough and the relative location of the lesion above the left atrium during puncture may be risk factors for systemic air embolism following percutaneous lung biopsy.
Acknowledgements
Not applicable.
Funding
No funding was received.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable requesr.
Authors' contributions
SHL and QF performed the experiments, analyzed the data and wrote the manuscript. HLY and YBH provided technical support during experimentation and were involved in drafting the manuscript. QY, ZXZ and BPZ aquired, analyzed and interpreted the data. CYZ designed the experiments and gave final approval of the version to be published. All authors read and approved the final manuscript.
Ethics approval and consent to participate
The current study was approved by the Ethics Review board of Qingdao University. Written informed consent was obtained from all patients or gaurdains.
Patient consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
References
|
Richardson CM, Pointon KS, Manhire AR and Macfarlane JT: Percutaneous lung biopsies: A survey of UK practice based on 5444 biopsies. Br J Radiol. 75:731–735. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Tomiyama N, Yasuhara Y, Nakajima Y, Adachi S, Arai Y, Kusumoto M, Eguchi K, Kuriyama K, Sakai F, Noguchi M, et al: CT-guided needle biopsy of lung lesions: A survey of severe complication based on 9783 biopsies in Japan. Eur J Radiol. 59:60–64. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Um SJ, Lee SK, Yang DK, Son C, Kim KN, Lee KN and Kim YS: Four cases of a cerebral air embolism complicating a percutaneous transthoracic needle biopsy. Korean J Radiol. 10:81–84. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Ibukuro K, Tanaka R, Takeguchi T, Fukuda H, Abe S and Tobe K: Air embolism and needle track implantation complicating CT-guided percutaneous thoracic biopsy: Single-institution experience. AJR Am J Roentgenol. 193:430–436. 2009. View Article : Google Scholar | |
|
Cheng HM, Chiang KH, Chang PY, Chou YF, Huang HW, Chou AS and Yen PS: Coronary artery air embolism: A potentially fatal complication of CT-guided percutaneous lung biopsy. Br J Radiol. 83:83–85. 2010. View Article : Google Scholar | |
|
Kodama F, Ogawa T, Hashimoto M, Tanabe Y, Suto Y and Kato T: Fatal air embolism as a complication of CT-guided needle biopsy of the lung. J Comput Assist Tomogr. 23:949–951. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Ghafoori M and Varedi P: Systemic air embolism after percutaneous transthoracic needle biopsy of the lung. Emerg Radiol. 15:353–356. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Mokhlesi B, Ansaarie I, Bader M, Tareen M and Boatman J: Coronary artery air embolism complicating a CT-guided transthoracic needle biopsy of the lung. Chest. 121:993–996. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Freund MC, Petersen J, Goder KC, Bunse T, Wiedermann F and Glodny B: Systemic air embolism during percutaneous core needle biopsy of the lung: Frequency and risk factors. BMC Pulm Med. 12:22012. View Article : Google Scholar : PubMed/NCBI | |
|
Van Liew HD, Conkin J and Burkard ME: The oxygen window and decompression bubbles: Estimates and significance. Aviat Space Environ Med. 64:859–865. 1993.PubMed/NCBI | |
|
Hare SS, Gupta A, Goncalves AT, Souza CA, Matzinger F and Seely JM: Systemic arterial air embolism after percutaneous lung biopsy. Clin Radiol. 66:589–596. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Ashizawa K, Watanabe H, Morooka H and Hayashi K: Hyperbaric oxygen therapy for air embolism complicating CT-guided needle biopsy of the lung. AJR Am J Roentgenol. 182:1606–1607. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Ohashi S, Endoh H, Honda T, Komura N and Satoh K: Cerebral air embolism complicating percutaneous thin-needle biopsy of the lung: Complete neurological recovery after hyperbaric oxygen therapy. J Anesth. 15:233–236. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Agostoni E and Rahn H: Abdominal and thoracic pressures at different lung volumes. J Appl Physiol. 15:1087–1092. 1960. View Article : Google Scholar : PubMed/NCBI | |
|
Ishikawa Y, Matsuguma H, Nakahara R, Ui A, Suzuki H and Yokoi K: Arterial air embolism: A rare but life-threatening complication of percutaneous needle biopsy of the lung. Ann Thorac Surg. 87:16222009. View Article : Google Scholar : PubMed/NCBI | |
|
Kau T, Rabitsch E, Celedin S, Habernig SM, Weber JR and Hausegger KA: When coughing can cause stroke-a case-based update on cerebral air embolism complicating biopsy of the lung. Cardiovasc Intervent Radiol. 31:848–853. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Ishii H, Hiraki T, Gobara H, Fujiwara H, Mimura H, Yasui K, Doke T, Mukai T, Kurokawa H, Ando Y, et al: Risk factors for systemic air embolism as a complication of percutaneous CT-guided lung biopsy: Multicenter case-control study. Cardiovasc Intervent Radiol. 37:1312–1320. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Muth CM and Shank ES: Gas embolism. N Engl J Med. 342:476–482. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Bhatia S: Systemic air embolism following CT-guided lung biopsy. J Vasc Interv Radiol. 20:709–711. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Arnold BW and Zwiebel WJ: Percutaneous transthoracic needle biopsy complicated by air embolism. AJR Am J Roentgenol. 178:1400–1402. 2002. View Article : Google Scholar : PubMed/NCBI |
