DOI:10.2214/AJR.07.3507
AJR 2008; 191:565-568
© American Roentgen Ray Society
Phrenic Nerve Injury Resulting from Percutaneous Ablation of Lung Malignancy
Raymond H. Thornton1,
Stephen B. Solomon1,
Damian E. Dupuy2 and
Manjit S. Bains3
1 Section of Interventional Radiology and Image-Guided Therapies, Department of
Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., Ste. H118,
New York, NY 10021.
2 Department of Diagnostic Imaging, Rhode Island Hospital and the Warren Alpert
Medical School at Brown University, Providence, RI.
3 Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York,
NY.
Received December 6, 2007;
accepted after revision February 21, 2008.
S. B. Solomon is a member of the Scientific Advisory Board of AngioDynamics
(Queensbury, NY).
D. E. Dupuy receives grant support from Endocare (Irvine, CA), Veran
Medical (Nashville, TN), Biotex (Houston, TX), and AblaTx. He has received
honoraria from Covidien.
Address correspondence to R. H. Thornton
(thorntor{at}mskcc.org).
Abstract
OBJECTIVE. The objective of our study was to illustrate the
potential for phrenic nerve injury during percutaneous lung ablation, to
discuss the importance of this complication, and to review the expected
location of the phrenic nerve on chest CT.
CONCLUSION. Knowledge of the expected location of the phrenic
nerve—a structure that is usually not visible on imaging but is
important—is essential for avoiding injury to the nerve during pulmonary
ablation.
Keywords: ablation • diaphragm paralysis • iatrogenic injury • lung cancer • phrenic nerve injury
Introduction
As the major muscle of inspiration, the diaphragm is responsible for
approximately two thirds of vital capacity
[1]. The phrenic nerve provides
the sole motor innervation to the diaphragm. Diaphragm paralysis resulting
from damage to the phrenic nerve can lead to important physiologic
consequences, including hypoxemia, hypercapnia, and up to 20% decrease in
oxygen uptake from the ipsilateral lung
[2]. Because patients referred
for percutaneous ablation of lung tumors often have substantial baseline
abnormalities of pulmonary function, they are at increased risk for morbidity
if phrenic nerve injury results from the procedure. With permission of the
institutional review boards for retrospective review, we present three cases
of lung cancer ablation: two complicated by phrenic nerve injury and a third
in which the potential for phrenic nerve injury was anticipated and avoided.
In addition, we review phrenic nerve anatomy and provide a brief review of
phrenic nerve injury.
Materials and Methods
Case 1
A 69-year-old man with stage IA right upper lobe non–small cell lung
carcinoma (NSCLC) (Fig. 1A) was
referred for radiofrequency ablation after he was deemed not to be a candidate
for thoracic surgery. His medical history was significant for chronic
obstructive pulmonary disease (COPD) with shortness of breath on exertion
requiring multiple inhalers, sleep apnea requiring continuous positive airway
pressure at night, diabetes, and hypertension. The ablation was performed
using a 2-cm radiofrequency electrode (Cooltip, Covidien) in two overlapping
ablations of 12 minutes' duration (Fig.
1B). A radiograph obtained after the procedure showed new
elevation of the right hemidiaphragm (Fig.
1C). Subsequently, the patient required 2 L of oxygen by nasal
cannula to maintain saturations above 92%.
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Fig. 1A —69-year-old man with stage IA right upper lobe
non–small cell lung carcinoma (NSCLC) referred for radiofrequency
ablation. Medical history was significant for chronic obstructive pulmonary
disease with shortness of breath on exertion requiring multiple inhalers,
sleep apnea requiring continuous positive airway pressure at night, diabetes,
and hypertension. Diagnostic inspiratory scan shows right upper lobe
NSCLC.
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Fig. 1B —69-year-old man with stage IA right upper lobe
non–small cell lung carcinoma (NSCLC) referred for radiofrequency
ablation. Medical history was significant for chronic obstructive pulmonary
disease with shortness of breath on exertion requiring multiple inhalers,
sleep apnea requiring continuous positive airway pressure at night, diabetes,
and hypertension. Combination of lower lung volumes during procedure and
posterior displacement of lesion caused by anterior approach substantially
alters relationship of lesion and ablation electrode to superior vena cava and
expected location of phrenic nerve.
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Fig. 1C —69-year-old man with stage IA right upper lobe
non–small cell lung carcinoma (NSCLC) referred for radiofrequency
ablation. Medical history was significant for chronic obstructive pulmonary
disease with shortness of breath on exertion requiring multiple inhalers,
sleep apnea requiring continuous positive airway pressure at night, diabetes,
and hypertension. Chest radiograph obtained after procedure shows differential
elevation of right hemidiaphragm, indicated by arrows.
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Case 2
A 69-year-old man with stage IB NSCLC and severe COPD precluding surgical
resection was referred for external beam radiation therapy and percutaneous
tumor ablation (Fig. 2A).
Because of the size of the mass, three 3.7-cm active-tip microwave antennae
(Vivawave System, Covidien) were inserted and a single 10-minute ablation at
45 W was performed (Fig. 2B).
Immediately after microwave ablation, the patient reported more shortness of
breath than before the procedure and difficulty taking deep breaths. Follow-up
chest radiographs obtained 1 week after microwave ablation
(Fig. 2C) showed mild elevation
of the left hemidiaphragm compared with the scout topogram obtained
immediately before microwave ablation. Chest fluoroscopy revealed paradoxical
diaphragmatic motion.
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Fig. 2A —69-year-old man with stage IB non–small cell lung
carcinoma (NSCLC) and severe chronic obstructive pulmonary disorder precluding
surgical resection was referred for external beam radiation therapy and
percutaneous tumor ablation. Because of size of mass, three 3.7-cm active tip
microwave antennae (Vivawave System, Covidien) were inserted and single
10-minute ablation at 45 W was performed. CT scan shows left upper lobe NSCLC.
Arrow indicates anticipated location of left phrenic nerve.
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Fig. 2B —69-year-old man with stage IB non–small cell lung
carcinoma (NSCLC) and severe chronic obstructive pulmonary disorder precluding
surgical resection was referred for external beam radiation therapy and
percutaneous tumor ablation. Because of size of mass, three 3.7-cm active tip
microwave antennae (Vivawave System, Covidien) were inserted and single
10-minute ablation at 45 W was performed. For adequate coverage of tumor,
anterior microwave antenna is positioned in relatively close proximity to
expected location of phrenic nerve (arrow).
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Fig. 2C —69-year-old man with stage IB non–small cell lung
carcinoma (NSCLC) and severe chronic obstructive pulmonary disorder precluding
surgical resection was referred for external beam radiation therapy and
percutaneous tumor ablation. Because of size of mass, three 3.7-cm active tip
microwave antennae (Vivawave System, Covidien) were inserted and single
10-minute ablation at 45 W was performed. Chest radiograph obtained after
procedure shows elevation of left hemidiaphragm (arrow); this finding
is consistent with left phrenic nerve injury.
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Case 3
An 84-year-old woman who had undergone resection of left lung NSCLC 10
years earlier presented with cough and pneumonia and was subsequently found to
have a solitary PET-positive mass in the right upper lobe abutting the
superior vena cava (Fig. 3A).
Because of the proximity of the mass to the expected location of the right
phrenic nerve, an artificial pneumothorax was created by inserting a needle
(Safe-T-Centesis needle, Cardinal Health) into the right pleural space
(Fig. 3B). Initially 750 mL of
room air was instilled, but the patient's oxygen saturation dropped to 82%.
Therefore, 250 mL of the air was aspirated, leaving enough working space
between the mass and the phrenic nerve while returning the oxygen saturation
to 94%. A single 3.7-cm active-tip microwave antenna (Vivawave System) was
inserted into the mass using CT fluoroscopic guidance, and a single 10-minute
treatment was performed with 45 W of power. The antenna was removed and the
injected air was aspirated. The 6-French Safe-T-Centesis catheter was left in
place overnight to wall suction and was removed the next day. The patient's
breathing remained at baseline without evidence of phrenic nerve injury.
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Fig. 3A —84-year-old woman who had undergone resection of left lung
non–small cell lung carcinoma (NSCLC) 10 years earlier presented with
cough and pneumonia and was subsequently found to have a solitary PET-positive
nodule in right upper lobe abutting superior vena cava. Because of proximity
of nodule to expected location of right phrenic nerve, artificial pneumothorax
was induced using Safe-T-Centesis needle (Cardinal Health). CT scan obtained
before procedure shows close association of cystic, low-attenuation lung tumor
with posterolateral aspect of superior vena cava (arrow).
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Fig. 3B —84-year-old woman who had undergone resection of left lung
non–small cell lung carcinoma (NSCLC) 10 years earlier presented with
cough and pneumonia and was subsequently found to have a solitary PET-positive
nodule in right upper lobe abutting superior vena cava. Because of proximity
of nodule to expected location of right phrenic nerve, artificial pneumothorax
was induced using Safe-T-Centesis needle (Cardinal Health). Because of
proximity of right upper lobe mass to anticipated location of right phrenic
nerve adjacent to superior vena cava (large arrow), pneumothorax was
induced using needle (small arrow) as neuroprotective strategy.
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Anatomy Review
The nondiseased phrenic nerve is typically not seen on cross-sectional
imaging except where its location can be inferred by association with the
course of the pericardiacophrenic arteries. Knowledge of the nerve's location
is essential so that lung ablation procedures can be planned to avoid or
protect this structure (Figs.
4A,
4B,
4C,
4D,
4E, and
4F). Helpful atlases and
descriptions have been previously published
[3,
4].
In the neck, the ventral cervical rami of C3, C4, and C5 coalesce to form
the phrenic nerve on the ventral surface of the anterior scalene muscle,
posterior to the sternocleidomastoid muscle. The nerve courses obliquely,
lateral to medial, across the anterior surface of the anterior scalene,
parallel and posterolateral to the internal jugular vein. At the anterior,
inferomedial border of the anterior scalene, the phrenic nerve courses between
the subclavian artery and subclavian vein into the chest, crossing the
internal mammary artery. Within the thorax, the phrenic nerve initially
parallels the course of the internal mammary arteries and then descends within
the lateral aspect of the middle mediastinum, just deep in relation to the
mediastinal pleura. Some useful landmarks exist to infer the location of the
nerve on the right and the left.
On the right, the phrenic nerve passes posterior to the subclavian vein,
lateral to the brachiocephalic vein and superior vena cava, and anterior to
the right hilum and continues lateral to the pericardial covering of the right
atrium and inferior vena cava before piercing the central tendon of the
diaphragm at or lateral to the caval aperture near the cavoatrial angle. In
patients with an azygous lobe, the right phrenic nerve may travel in the
azygous fissure [5].
On the left, the phrenic nerve is found at the medial aspect of the left
lung apex in a groove between the left common carotid and left subclavian
arteries. It passes lateral to the aortic arch and continues anterior to the
left hilum between the pericardium and mediastinal pleura, passing just
superficial to the left ventricle before entering the diaphragm just lateral
to the left cardiac surface.
Discussion
A wide variety of iatrogenic and pathologic insults to the phrenic nerve
may lead to diaphragm dysfunction or paralysis. The spectrum of physiologic
response to phrenic nerve injury is also heterogeneous, ranging from an
asymptomatic elevated diaphragm to frank respiratory failure requiring
mechanical ventilation [6].
Iatrogenic causes of phrenic nerve injury include cardiac surgery, surgery
involving the aortic arch, mediastinal and lung resections, anterior cervical
spine decompression, catheter ablation of arrhythmogenic pathways in the
heart, and jugular vein puncture. Phrenic nerve injury is also recognized as a
late complication of radiation therapy. Involvement of the phrenic nerve by
tumors of the lung or mediastinum, infections including typhoid and polio, and
blunt trauma are other possible causes
[2]. Phrenic nerve injury may
also occur as a complication of lung tumor ablation.
Phrenic nerve injury is a well-known complication of cardiac surgery.
Cold-induced demyelination injury was previously common when iced slush was
used as a topical myocardial protective strategy. Ischemic, thermal, or
mechanical injury to the nerve can also occur during internal mammary artery
harvest. Although technical modifications—especially the use of phrenic
nerve–insulating pads and avoidance of iced slush—have decreased
the incidence of phrenic nerve injury associated with cardiac surgery, it
remains in the range of 2–31%
[6]. In 60–90% of
patients with phrenic nerve injury after cardiac surgery, the radiographic
abnormality has been noted to resolve within 1 year
[6].
Phrenic nerve injury is increasingly recognized as a complication of
cardiac ablation procedures. Bai et al.
[7] described phrenic nerve
injury in 17 patients treated with cardiac ablation for arrhythmia. Energy
sources that were used included radiofrequency ablation in 13 patients,
cryotherapy in one, ultrasound in two, and laser ablation in another. Of those
17 patients, two had transient abnormalities in diaphragm function that
resolved immediately. Diaphragm function, which was evaluated using chest
radiography and the sniff test, recovered in the remaining 15 patients 8.3
± 6.6 months (mean ± SD) after the procedure. Sacher et al.
[8] described 18 patients who
developed phrenic nerve injury as a result of cardiac radiofrequency ablation
for treatment of atrial fibrillation. In that group, 12 patients had complete
recovery of diaphragm function—three within 24 hours of ablation and
nine within a mean of 4 ± 5 months of ablation. Of the remaining six
patients, three had partial recovery of diaphragm function and three had
persistent diaphragm paralysis.
Phrenic nerve injury has been studied in a dog model using experimental
cardiac radiofrequency ablation at the right superior pulmonary vein.
Radiofrequency ablation to a temperature of > 60°C at that site caused
nerve dysfunction in three dogs, confirming the potential for nerve injury by
heating of adjacent tissue. Direct deposition of radiofrequency energy into
the phrenic nerve produced transient injury in all specimens at 47°C
± 3°C after 38 ± 32 seconds (mean ± SD). Permanent
injury occurred in all dogs after 92 ± 83 seconds of additional energy
delivered at a temperature of 51°C ± 6°C. In five dogs, nerve
function was immediately impacted by the generated current and dysfunction
resolved immediately with discontinuation of radiofrequency deposition. These
findings suggest that a current-mediated electromagnetic effect may also play
a role in the pathogenesis of phrenic nerve injury in addition to thermal
injury when radiofrequency is the energy source
[9].
Because ablation of paramediastinal lung tumors carries risk of injury to
the phrenic nerve, operators must be aware of its anticipated location and
potential neuroprotective strategies. The ability to separate tumors from the
mediastinal pleura—and therefore from the course of the phrenic
nerve—could help to minimize risk while permitting tumor ablation.
Mechanical separation of the phrenic nerve from the heart has been described
by Buch et al. [10], who
interposed an 18 mm x 4 cm balloon catheter between the heart and the
phrenic nerve, thereby eliminating phrenic capture and permitting cardiac
radiofrequency ablation without phrenic nerve injury. Hydrodissection or
creation of a protective or artificial pneumothorax sufficient to separate a
paramediastinal lesion from the anticipated course of the nerve could also
permit safe ablation of such targets. However, protective pneumothoraces may
not be achievable in patients with a history of ipsilateral thoracotomy,
radiation therapy, or other cause of pleural adhesion
[11].
In summary, patients referred for lung tumor ablation often have
substantial underlying pulmonary function abnormalities that may predispose
them to considerable morbidity if the phrenic nerve is injured during
pulmonary ablation procedures. Phrenic nerve injury may be caused by thermal
(both hot and cold) or mechanical injuries and has been seen after a variety
of cardiac ablative techniques including radiofrequency ablation,
cryoablation, ultrasound, and laser ablation. The results of animal studies
indicate that injuries mediated by radiofrequency current directly into or
adjacent to the nerve are seen at ablation temperatures and exposure times
characteristic of routine clinical protocols. Understanding the course of the
phrenic nerve in the thorax as well as potential neuroprotective strategies is
therefore an essential component of safe ablation planning.
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Abstract
Introduction
