Michael Curtis, MD
University of California, San Francisco
Lung transplantation remains only a class IIb indication for intraoperative monitoring via transesophageal echocardiography (TEE) in existing guidelines.1 However, some have suggested that TEE should become routine during these procedures2, given the multiple and varied impacts to the cardiovascular system throughout such a case (e.g., pulmonary artery clamping, reperfusion injury, air embolization, etc.) TEE may also be able to quickly detect obstruction at the pulmonary artery (PA) anastomosis at the pulmonary arteries and making immediate intraoperative revision possible if needed. While no society guidelines exist for diagnosing such a life-threatening complication on intraoperative TEE, there are many recommendations one may use to guide their evaluation.
Incidence and Related Complications
Obstruction of a pulmonary artery anastomosis is rare – it was reported in approximately 3% of lung transplantations reviewed in a recent meta-analysis by Kumar et al.3 A multitude of etiologies have been implicated, including donor-recipient size mismatch, external compression from surrounding tissue, twisting and/or kinking, thrombosis, and suture obstruction.3,4 Those with restrictive lung disease and females also appear to be at higher risk of PA obstruction. Finally, obstruction at the pulmonary arterial sites is generally accepted to be more common than at their venous counterparts, which is thought to result from differences in the surgical technique required at the different anastomotic sites.4,5
Although relatively rare, such obstruction at a pulmonary artery anastomosis cannot be taken lightly: once diagnosed, the rate of mortality approaches nearly 25%.3 There are also associated complications that may result, such as graft failure, persistent hypoxemia, prolonged need for mechanical ventilation, and right-heart failure.3,5 These potentially devastating consequences highlight the importance of having high index of suspicion for such a lesion. For example, early clinical signs may be hemodynamic instability, pulmonary hypertension, a diminished capnography tracing, or unexplained hypoxemia or acidosis should all be concerning to providers.6,7
Role of Transesophageal Echocardiography
With regards to objective testing, pulmonary angiography is regarded as being the gold standard for diagnosis of stenosis at the pulmonary artery anastomosis, given its imaging quality and ability to immediately intervene on the findings with catheter-based techniques.4 However, intraoperative TEE is able to provide much earlier insight into possible complications with an anastomotic site, allowing for immediate surgical revision and avoidance of any related post-operative complications.
Unfortunately, consensus guidelines on the diagnosis of obstruction at a PA anastomosis by echocardiography do not exist. However, multiple measures have been proposed (Table 1), including the intraluminal narrowing of the pulmonary artery graft to 75% or less of the diameter of the native, ipsilateral PA, as put forth by Hausmann et al. in their 1992 publication.8 Other suggested measures that should be concerning are a mean velocity through the pulmonary artery of 2.6 m/s or greater, a gross PA diameter of less than 0.8 cm, the presence of turbulent flow on color doppler, and elevated pressure gradients across the anastomosis.3 What precisely constitutes an elevated gradient at the PA anastomosis itself lacks wide-agreement, though some having put forth using the American Society of Echocardiography (ASE) guidelines for pulmonary valve stenosis as a guide7, while others recommend that gradients should be of concern once 57 mm Hg or higher.3
Interrogation of related structures by echo, such as the pulmonary veins, may also provide hints as to the functioning of the pulmonary arteries. For example, impaired flow as demonstrated by doppler (e.g., blunted S or D waves) or thrombosis due to stasis in the ipsilateral pulmonary veins may also be concerning for PA anastomotic obstruction.7 Similarly, evidence of increased perfusion through the contralateral pulmonary veins (e.g., increased velocities) may be a sign that a significantly greater proportion of right-heart output is going through one pulmonary artery due to the other being obstructed.
Unfortunately, evaluation by the pulmonary arteries with TEE is inherently limited by anatomy. For example, the relative inability to evaluate the left pulmonary artery due to interference from the adjacent left mainstem bronchus. The relative orientation of the pulmonary arteries to the echo probe may also make it challenging to line up a doppler beam and obtain accurate velocities or pressure gradients. If concerned, other options that may be used intraoperatively include epipulmonary artery ultrasonography (i.e., direct, external contact with an ultrasound probe manipulated by surgical team), which one study has shown to be superior for imaging the left pulmonary artery than TEE itself.9 The surgeon may also directly cannulate the pulmonary artery of concern and measure a true pressure gradient by pullback technique.
Post-Operative Endovascular Interventions
Given that intraoperative diagnosis by TEE can be challenging, and that nearly 75% of patients diagnosed with PA obstruction post-operatively require some sort of procedural intervention3, it is fortunate that options exist now outside of open surgical techniques. For example, multiple reports of successful endovascular stenting have been published.10-12 Although balloon angioplasty alone is regarded as less useful in high-grade stenosis due to arterial elastic recoil10, it has still been shown to be successful in some cases.13
Although use of intraoperative TEE is not yet the standard of care during lung transplantation, it may provide information both critical to the hemodynamic management of the patient, as well as possible complications in the surgical procedure. Specifically, obstruction at a pulmonary artery anastomosis – a rare complication with high morbidity and mortality – may be caught early enough with thorough echocardiographic investigation to revise intraoperatively. However, it is important to remember inherent limitations of TEE prevent it from being a panacea for lesions at this location, and that sometimes it must be supplemented with alternative intraoperative or post-operative techniques when there is sufficient concern.
|Table 1 – Signs Suggestive of Pulmonary Artery Anastomosis Obstruction on Transesophageal Echocardiography (TEE)|
|Gross Inspection of the Pulmonary Artery||· Presence of an obstructive mass (e.g., thrombus)|
|Intraluminal Diameter||· ≤ 75% of the native, ipsilateral pulmonary artery
· < 0.8 cm intraluminal diameter
|Pulmonary Artery Mean Velocity||· ≥ 2.6 m/s|
|Color Doppler||· Evidence of turbulent flow|
|Peak Pressure Gradient||· No widespread agreement – however, suggestions to use gradients ≥ 57 mm Hg or ASE guidelines for grading pulmonary valve stenosis (i.e., mild < 36 mm Hg, moderate 36-64 mm Hg, and severe > 64 mm Hg)14 as a framework
|Ipsilateral Pulmonary Veins||· Evidence of diminished flows (e.g., blunted S or D waves) or stasis (e.g., presence of thrombus)
|Contralateral Pulmonary Veins||· Evidence of significantly increased flows (e.g., elevated velocities)
* American Society of Echocardiography (ASE)
- Cheitlin MD, Armstrong WF, Aurigemma GP, Beller GA, Bierman FZ, Davis JL, et al. ACC/AHA/ASE 2003 guideline update for the clinical application of echocardiography: summary article: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (ACC/AHA/ASE Committee to Update the 1997 Guidelines for the Clinical Application of Echocardiography). Circulation. 2003;108(9):1146-62. Epub 2003/09/04. doi: 10.1161/01.CIR.0000073597.57414.A9. PubMed PMID: 12952829.
- Iyer MH, Bhatt A, Kumar N, Hussain N, Essandoh MK. Transesophageal Echocardiography for Lung Transplantation: A New Standard of Care? J Cardiothorac Vasc Anesth. 2020;34(3):741-3. Epub 2019/11/11. doi: 10.1053/j.jvca.2019.10.025. PubMed PMID: 31706852.
- Kumar N, Hussain N, Kumar J, Essandoh MK, Bhatt AM, Awad H, et al. Evaluating the Impact of Pulmonary Artery Obstruction After Lung Transplant Surgery: A Systematic Review and Meta-analysis. Transplantation. 2021;105(4):711-22. Epub 2021/03/25. doi: 10.1097/TP.0000000000003407. PubMed PMID: 33760790.
- Siddique A, Bose AK, Ozalp F, Butt TA, Muse H, Morley KE, et al. Vascular anastomotic complications in lung transplantation: a single institution’s experience. Interact Cardiovasc Thorac Surg. 2013;17(4):625-31. Epub 2013/06/22. doi: 10.1093/icvts/ivt266. PubMed PMID: 23788195; PubMed Central PMCID: PMCPMC3781793.
- Clark SC, Levine AJ, Hasan A, Hilton CJ, Forty J, Dark JH. Vascular complications of lung transplantation. Ann Thorac Surg. 1996;61(4):1079-82. Epub 1996/04/01. doi: 10.1016/0003-4975(96)00003-3. PubMed PMID: 8607660.
- Tan Z, Roscoe A, Rubino A. Transesophageal Echocardiography in Heart and Lung Transplantation. J Cardiothorac Vasc Anesth. 2019;33(6):1548-58. Epub 2019/02/03. doi: 10.1053/j.jvca.2019.01.005. PubMed PMID: 30709594.
- Abrams BA, Melnyk V, Allen WL, Subramaniam K, Scott CD, Mitchell JD, et al. TEE for Lung Transplantation: A Case Series and Discussion of Vascular Complications. J Cardiothorac Vasc Anesth. 2020;34(3):733-40. Epub 2019/10/02. doi: 10.1053/j.jvca.2019.09.005. PubMed PMID: 31570240.
- Hausmann D, Daniel WG, Mugge A, Heublein B, Hamm M, Schafers HJ, et al. Imaging of pulmonary artery and vein anastomoses by transesophageal echocardiography after lung transplantation. Circulation. 1992;86(5 Suppl):II251-8. Epub 1992/11/01. PubMed PMID: 1424008.
- Felten ML, Michel-Cherqui M, Sage E, Fischler M. Transesophageal and contact ultrasound echographic assessments of pulmonary vessels in bilateral lung transplantation. Ann Thorac Surg. 2012;93(4):1094-100. Epub 2012/03/06. doi: 10.1016/j.athoracsur.2012.01.070. PubMed PMID: 22387146.
- Waurick PE, Kleber FX, Ewert R, Pfitzmann R, Bruch L, Hummel M, et al. Pulmonary artery stenosis 5 years after single lung transplantation in primary pulmonary hypertension. J Heart Lung Transplant. 1999;18(12):1243-5. Epub 1999/12/28. doi: 10.1016/s1053-2498(99)00091-1. PubMed PMID: 10612386.
- Grubstein A, Atar E, Litvin S, Belenky A, Knizhnik M, Medalion B, et al. Angioplasty using covered stents in five patients with symptomatic pulmonary artery stenosis after single-lung transplantation. Cardiovasc Intervent Radiol. 2014;37(3):686-90. Epub 2014/02/11. doi: 10.1007/s00270-013-0758-0. PubMed PMID: 24510277.
- Berger H, Steiner W, Schmidt D, Forst H, Dienemann H. Stent-angioplasty of an anastomotic stenosis of the pulmonary artery after lung transplantation. Eur J Cardiothorac Surg. 1994;8(2):103-5. Epub 1994/01/01. doi: 10.1016/1010-7940(94)90102-3. PubMed PMID: 8172715.
- Shoji T, Hanaoka N, Wada H, Bando T. Balloon angioplasty for pulmonary artery stenosis after lung transplantation. Eur J Cardiothorac Surg. 2008;34(3):693-4. Epub 2008/07/22. doi: 10.1016/j.ejcts.2008.06.005. PubMed PMID: 18639464.
- Baumgartner H, Hung J, Bermejo J, Chambers JB, Evangelista A, Griffin BP, et al. Echocardiographic assessment of valve stenosis: EAE/ASE recommendations for clinical practice. J Am Soc Echocardiogr. 2009;22(1):1-23; quiz 101-2. Epub 2009/01/10. doi: 10.1016/j.echo.2008.11.029. PubMed PMID: 19130998.