Abstract
In current practice, it is not well-known whether the development of air bubbles spontaneously in the heart during routine transthoracic echocardiography examination has a clinical consequence. Even though there have been published case reports regarding the formation of air bubbles due to iatrogenic reasons, we could not find a case of a patient demonstrating spontaneous air bubbles formation due to only coughing. Thus, in this report, we present a case of an adult patient who had unexpected air bubbles in the heart after coughing. Furthermore, the patient experienced a catastrophic cerebrovascular accident after diagnosing such an event in the same day. We thought that spontaneously occurring air bubbles in the heart might have resulted in cerebrovascular accident by passing through patent foramen ovale, which we have diagnosed after we had seen that the spontaneously occurred air bubbles had also appeared in left chambers. To our knowledge, this might be the first case of such a patient in the literature.
<Learning objective: The appearance of cough-induced air bubbles in the left heart might be a precursor to peripheral air embolism, and thus, predictive of very poor prognosis. Thus, medical workers should be aware of this poor finding.>
Keywords: Cough, Air bubble, Cerebrovascular accident
Introduction
Appearance of spontaneous air bubbles due to cough in the heart during routine transthoracic echocardiography examination is a very rare finding and the importance of this finding in clinical practice has not been well reported. In the literature, a few case reports have been published; but all of them were only due to iatrogenic reasons [1]. Thus, in this case, we describe an adult patient who had unexpected air bubbles in the heart after coughing. Moreover, the patient had a poor prognosis owing to cerebrovascular accident after diagnosing such an event. As far as we know, there is no similar case in the literature regarding this issue.
Case report
A 74-year-old male patient with a history of coronary artery by-pass grafting (CABG) and idiopathic pulmonary fibrosis consulted our clinic for the evaluation of progressive dyspnea. Upon physical examination, it was noted that there was a pretibial edema on both sides of the legs. Also, the patient had difficulty in breathing and frequent attacks of cough. The patient's rhythm was normal sinus rhythm. In addition, he was prophylactically anticoagulated with low-molecular-weight heparin. On transthoracic echocardiography (TTE), it was observed that the left ventricle (LV) was normally contracting and the right ventricular systolic function was severely depressed with severe tricuspid regurgitation (Fig. 1A,B, Video 1). During TTE examination, the patient was experiencing cough attacks. We observed that there appeared to be air bubbles in the right atrium (RA), followed by the right ventricle (RV) (Fig. 2A, Videos 2, 3), such that it was fully filled with air bubbles. After a couple of beats, the same bubbles were seen in the left atrium (LA) and LV, suggesting an accompanying patent foramen ovale (PFO) or a small atrial septal defect (ASD) with right-to-left shunt (Fig. 2B, Video 4). Interestingly, these air bubbles disappeared after the cessation of the cough attack. The same finding was confirmed during other spontaneously developed or instructed cough attacks. The diagnosis of PFO was based upon the finding that the air-bubbles appeared in the left heart just two-to-three beats after they had appeared in the RA. We considered that the patient's status was not good enough to perform either transesophageal echocardiography or magnetic resonance imaging for proving the presence of PFO. During the intensive care unit follow-up, the patient started to experience myoclonic contractions just after a cough attack in the evening hours of the same day, and later he developed a cardiac arrest. The patient was successfully resuscitated and intubated. Afterwards, the patient consulted our neurology department, and he was diagnosed with a cerebrovascular accident. Due to the patient's critical status and vegetative state, he could not undergo magnetic resonance or computerized tomography examination. The patient passed away on the 22nd day after the TTE examination.
Fig. 1.
A. Transthoracic echocardiography image showing normal left ventricle diameter and function. B. Transthoracic echocardiography image showing severely dilated right ventricle and D-shape interventricular septum. IVS, interventricular septum; LA, left atrium; LV, left ventricle; RV, right ventricle.
Fig. 2.
A. Transthoracic echocardiography image showing the formation of spontaneous air bubbles in the right atrium and right ventricle. B. Transthoracic echocardiography image showing passing of air bubbles in the left ventricle through patent foramen ovale. LV, left ventricle; RA, right atrium; RV, right ventricle.
Discussion
The appearance of air in an air-free area can result from two ways; air leakage, which can be defined as the appearance of air due to passing from a normally air-filled cavity, or as a result of the gas dissolved in the liquid becoming insoluble due to a sudden pressure decrease [1,2]. In this patient, air-leak at the level of lung is unlikely because the air-bubbles should have firstly appeared in the left heart if it was the case. Although the most common cause of air leakage is pneumothorax, it may also develop due to other reasons, such as idiopathic pulmonary fibrosis and CABG, which were also present in our patient [2], [3], [4]. However, the severity of the interstitial fibrosis was not so high to cause an air leakage and the air leakage associated with CABG is expected to occur in the early postoperative course. Therefore, we do not think that the air bubbles seen in our patient are due to one of them. Pneumothorax is also unlikely to be responsible in this case because there were no other signs and symptoms of pneumothorax, such as chest pain, or rapidly deteriorating clinical status.
The mechanism, but not the cause, of the bubbles in this case might be that the sudden pressure changes during the cough attack might have resulted in the gas in the intrathoracic veins becoming insoluble. According to Boyle's law, a sudden decrease in the pressure causes enlargement of tiny bubbles and makes them visible by ultrasound devices [5]. Veins are more sensitive to pressure changes around them due to their thinner walls. Furthermore, because the patient had right heart failure, the right atrial pressure might have increased to such a level (higher than that of the LA) that the air bubbles came from the venous system directly and passed to the LA without any additional maneuver such as Valsalva. Although we think that “a PFO with spontaneous right-to-left shunt” is more appropriate to define this defect, a small ASD with right-to-left shunt cannot be excluded by only TTE examination. Another diagnosis would be “a stretched PFO which behaves like an ASD due to increased right atrial pressure”. The possibility of PFO may also suggest platypnea-orthodeoxia syndrome. However, we do not think such a diagnosis because the dyspnea in this syndrome occurs when the patient is upright and resolves with recumbent position. This feature is just opposite to that of our case.
Actually, the cause of the air bubbles in our case is open to many possibilities and none of them can be confirmed or entirely excluded because the diagnostic modalities were limited to reach such a conclusion. However, we think that the causal relationship may be in two ways; I-) The bubbles may have caused the event; II-) The bubbles may have resulted from the same event that had caused the catastrophic event. We think that the first one is more likely because the cerebrovascular event occurred just after a cough attack. What we really think that is important and educative about this case is that cough-induced air bubbles coupled with PFO may be predictive of a poor prognosis rather than the cause of the air bubbles. The air bubbles might have coalesced after passing into the aorta (we did not see any big air bubble in the heart) and resulted in cerebrovascular accident. A thromboembolism might also be responsible but this is more unlikely because the patient was under proper parenteral anticoagulation throughout the hospitalization. Moreover, the history obtained from the patient did not reveal such a fatal cerebrovascular event. It is likely that it had not happened before.
As far as we could find, this is the first clinical entity that bubbles spontaneously occurred after a thoracic maneuver, passed into the arterial system through PFO, or a small ASD, and caused cerebrovascular accident without any iatrogenic reason. We think that the appearance of cough-induced air bubbles in the left heart might be a precursor to peripheral air embolism, and thus, predictive of very poor prognosis.
Funding
None.
Declaration of Competing Interest
None to declare.
Acknowledgments
None.
Footnotes
Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.jccase.2021.04.019.
Appendix. Supplementary materials
Video 1. Video image showing normal contraction of the left ventricle and severely depressed and dilated right ventricle. LA, left atrium; LV, left ventricle; RV, right ventricle.
Videos 2, 3. Video image showing the formation of air bubbles in the right atrium and right ventricle due to coughing. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.
Video 4. Video image showing passing of air bubbles in the left ventricle through patent foramen ovale. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.
References
- 1.Shintani Y., Funaki S., Ose N., Kawamura T., Kanzaki R., Minami M., Okumura M. Air leak pattern shown by digital chest drainage system predict prolonged air leakage after pulmonary resection for patients with lung cancer. J Thorac Dis. 2018;10:3714–3721. doi: 10.21037/jtd.2018.05.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Blasco V., Visintini P., Antonini F., Leone M., Albanese J., Martin C. Embolie gazeuse secondaire à une fistule pleuroveineuse [Venous gas embolism from pleurovenous fistula] Ann Fr Anesth Reanim. 2007;26:242–244. doi: 10.1016/j.annfar.2006.10.001. [DOI] [PubMed] [Google Scholar]
- 3.Mukundakrishnan K., Ayyaswamy P.S., Eckmann D.M. Bubble motion in a blood vessel: shear stress induced endothelial cell injury. J Biomech Eng. 2009;131 doi: 10.1115/1.3153310. [DOI] [PubMed] [Google Scholar]
- 4.Vik A., Jenssen B.M., Brubakk A.O. Arterial gas bubbles after decompression in pigs with patent foramen ovale. Undersea Hyperb Med. 1993;20:121–131. [PubMed] [Google Scholar]
- 5.Jones M.W., Brett K., Han N., Wyatt H.A. StatPearls [Internet] StatPearls Publishing; Treasure Island, FL: 2021. Hyperbaric physics. [Updated 2020 Oct 27]https://www.ncbi.nlm.nih.gov/books/NBK448104/ Available from: [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Video 1. Video image showing normal contraction of the left ventricle and severely depressed and dilated right ventricle. LA, left atrium; LV, left ventricle; RV, right ventricle.
Videos 2, 3. Video image showing the formation of air bubbles in the right atrium and right ventricle due to coughing. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.
Video 4. Video image showing passing of air bubbles in the left ventricle through patent foramen ovale. LA, left atrium; LV, left ventricle; RA, right atrium; RV, right ventricle.


