Ann Thorac Surg 2006;82:1870-1875
© 2006 The Society of Thoracic Surgeons
Original Articles: General Thoracic
Surgical Anatomy of the Accessory Phrenic Nerve
Marios Loukas, MD, PhDa,b,*,
Christopher R. Kinsella, Jr, MSa,
Robert G. Louis, Jr, MDa,
Sagar Gandhi, MSc,
Brian Curry, PhDa
a Department of Anatomical Sciences, St. George's University School of Medicine, Grenada, West Indies
b Department of Education and Development, Harvard Medical School, Boston, Massachusetts
c Department of Anatomy, American University of the Caribbean, Saint Maarten, the Netherlands Antilles
Accepted for publication May 18, 2006.
* Address correspondence to Dr Loukas, Department of Anatomical Sciences, St. George's University School of Medicine, Grenada, West Indies. (Email: edsg2000{at}yahoo.com; mloukas{at}sgu.edu).
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Abstract
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BACKGROUND: Reports place the frequency of phrenic nerve injury after cardiac operations between 10% and 85%, emphasizing the importance of an accurate anatomic description of the diaphragm's innervating nerves to reduce iatrogenic injury, length of hospitalization, and associated costs. The aim of our study was to explore the anatomic variations of the accessory phrenic nerve and relate these findings to phrenic nerve injury.
METHODS: Eighty adult formalin-fixed cadavers were dissected, resulting in 160 nerve specimens. Fifty nerve specimens were also examined laparoscopically with findings later confirmed through gross dissection. All nerves contributing to the phrenic nerve after crossing the anterior scalene were considered to be accessory phrenic nerves.
RESULTS: The phrenic nerve was present in all specimens, and 99 (61.8%) also had an accessory phrenic nerve. The accessory phrenic nerve arose from the nerve to subclavius in 60 specimens (60.6%), ansa cervicalis in 12 (12.1%), and nerve to sternohyoid in 7 (7%). The accessory phrenic nerve joined with the phrenic nerve in the thorax anterior to the subclavian vein in 45 (45.5%) specimens and posterior in 17 (22.2%). A phrenic-accessory phrenic nerve loop was found around the subclavian vein in 45 (35 on the right, 10 on the left) specimens and around the internal thoracic artery in 38 (31 on the right, 7 on the left).
CONCLUSIONS: To reduce injuries to the diaphragm, the presence of an accessory phrenic nerve should be considered before mobilization and skeletonization of the internal thoracic artery above the second rib.
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Introduction
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Although the surgical anatomy of the phrenic nerve (PN) has been well described [1, 2], recent reports concerning PN injury (PNI) associated with myocardial revascularization [3–5] and high mobilization of the internal thoracic artery (ITA) [6, 7] emphasize the clinical importance of identifying potential risk factors. The morbidity associated with PNI after coronary artery bypass grafting (CABG) has also been shown to increase in patients with chronic obstructive pulmonary disease (COPD) [7].
Previous studies have focused on high mobilization of the ITA [6, 7], devascularization of peri-PN blood vessels [8], surgical manipulations of the PN [6, 9], and cardioplegia from saline slush application [4] as risk factors for PNI. The presence of an accessory PN (APN), which has received less attention, may increase the risk associated with any injury to the PN. Specifically, mobilization and skeletonization of the ITA above the second rib may damage the blood supply of the APN or sever its connection with the PN.
Standard anatomy texts describe the APN as containing fibers from C5 to the diaphragm through the nerve to subclavius [1, 2] or C3 fibers through the ansa cervicalis [2]. Although there is consensus that the APN will join the PN at the root of the neck at the level of the first rib or within the thorax [1, 2], descriptions of its course differ. The APN is described as more often lying posterior [2] or only anterior [1] to the subclavian vein.
The aim of this study was to explore and describe the range of all the previously mentioned observations and provide a comprehensive picture of the anatomy of the APN across a broad range of specimens to help reduce the frequency of iatrogenic injury.
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Material and Methods
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The institutional review board approved this study (IRB/06014). Individual consent was waived because data collection (age and patient history) was obtained from cadaver records. The anatomy of the APN and PN was examined in 80 adult cadavers (160 specimens) during gross anatomy courses at the American University of the Caribbean (25), Harvard Medical School (45), and St. George's Medical School (10) during 2004 to 2005. The mean age of the cadavers was 69 years (range, 55 to 86 years); 48 were male and 32 were female. All of the cadavers had been fixed in formalin-phenol-alcohol solution. None of the specimens revealed any evidence of previous surgical procedures, traumatic lesions, or gross pathologies to the neck and thorax.
The cadavers at the American University of the Caribbean were also examined using a Stryker laparoscopic unit including a Stryker Quantum 4000 light source, Stryker 3-chip camera system (Stryker Endoscopy, San Jose, CA) and a Wolf 5-mm x 30-cm 0° laparoscope. Images were recorded with image capture software (Endoscopy Support Services, Inc. Brewster, NY) as previously described [10]. The primary incision for the entrance of the endoscope and the laparoscopic scissors and forceps (Wolf, 5 mm) was superior to the subclavian vein at the root of the neck at the parasternal line.
The purpose of introducing and exploring the APN laparoscopically before gross dissection was to identify and appreciate any variations significant to the ITA before removing the chest wall. After laparoscopic investigation, the variations of the APN with the ITA were anticipated and preserved grossly. The clavicles were removed and the specimens were dissected in the traditional manner to expose the entire anatomy of the APN. All nerves contributing to the PN after it had crossed the anterior scalene were considered to be APNs.
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Results
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The PN was found bilaterally in all 80 cadavers (160 PNs) and an APN was associated with 99 of the PNs (61.8%), with bilateral occurrence in 31 cadavers (38.8%). Bilateral symmetrical origin of the APN, from the nerve to subclavius, was observed in only 10 cadavers. The APN varied in its origin, course, and point of communication with the PN (Tables 1 and 2).
The most frequent origins of the APN were from the nerve to subclavius in 60 (60.6%), ansa cervicalis in 12 (12.1%), and nerve to sternohyoid in 7 (7.1%) (Fig 1). The APN also originated from the supraclavicular nerve in 4 (4%), spinal accessory nerve in 4 (4%), hypoglossal nerve in 2 (2%; Fig 2), C5 in 2 (2%), C4 in 5 (5.1%), and C3 in 3 (3%; Fig 3). Ninety APN lay lateral to the PN and 9 lay medial (Table 1).
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Fig 1. Drawing illustrates the different points of origin of the accessory phrenic nerve. These are ansa cervicalis, nerve to sternohyoid, and nerve to subclavius. Arrows indicate the structures from which the accessory phrenic nerves originate, and circles indicate the accessory phrenic nerves.
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Fig 2. Drawing illustrates the different points of origin of the accessory phrenic nerve. These are hypoglossal nerve, spinal accessory nerve, and supraclavicular. Arrows indicate the structures from which the accessory phrenic nerves originate, and circles indicate the accessory phrenic nerves.
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Fig 3. Drawing illustrates the different points of origin of the accessory phrenic nerve. These are C3, C4, and C5, nerves. Arrows indicate the structures from which the accessory phrenic nerves originate, and circles indicate the accessory phrenic nerves.
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The APN joined the PN at varying levels. These included connections at the root of the neck, at the level of the second rib inferior to the subclavian vein, and inferior to the subclavian vein at the root of the lung (Table 2, Fig 4). Thirty-two APNs (32.3%) joined the PN at various points in the root of the neck. Because of the large variability of connections within the neck, it was not possible to group these findings.
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Fig 4. Drawing illustrates the different points that the accessory phrenic nerve joins the phrenic nerve in the thorax. Circle 1 demonstrates an accessory phrenic nerve that joins the phrenic nerve just inferiorly and anteriorly to the subclavian vein. Circle 2 demonstrates an accessory phrenic nerve that joins the phrenic nerve inferiorly and anteriorly to the subclavian artery looping around the internal thoracic artery. Circle 3 demonstrates an accessory phrenic nerve that joins the phrenic nerve inferiorly and anteriorly to the subclavian artery at the root of the lung.
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When joining within the thorax, the APN and PN formed a loop around the subclavian vein in 45 specimens (45.5%; Figs 5 and 6).
This loop encircled either the right or the left ITA (RITA, LITA) in 38 (38.4%; Fig 7). When traveling posteriorly to the subclavian vein, the APN formed a loop with the PN at the level of the subclavian vein in 8 specimens (8.1%) and formed a loop involving an ITA in 7 (7 7.1%; Fig 8,
Table 2). Finally, the APN joined the PN inferior to the subclavian vein near the pulmonary hilum in 13 specimens (13.1%).
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Fig 5. The communication of the accessory phrenic nerve with the phrenic nerve in the thorax anterior to the subclavian vein is shown.
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Fig 6. Two specimens dissected laparoscopically are demonstrated. In both specimens, the connection of the accessory phrenic nerve with the phrenic nerve between the mediastinal pleura and pericardium is evident.
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Fig 7. The communication of the accessory phrenic nerve with the phrenic nerve in the thorax anterior to the subclavian vein forming a loop with the right internal thoracic artery is shown.
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Fig 8. The communication of the accessory phrenic nerve with the phrenic nerve in the thorax posterior to the subclavian vein forming a loop with the left internal thoracic artery is shown.
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Laparoscopically, APNs were clearly identified below the subclavian vein forming loops around the LITA or RITA. All the results obtained laparoscopically were later confirmed through gross dissection. We found no differences in the prevalence of APNs with respect to race or gender.
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Comment
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The frequency of certain variations in origin, course, and communication between the PN and APN in our study differs from previous reports and includes a description of an APN/PN loop around the ITA with incidence reported for both left and right sides. Previous descriptions of APN frequency vary considerably between cadaveric and surgical studies [11]. In 1930, Aycock and Habliston, as reported by Kelley [11], performed the largest cadaveric study and found a 65% incidence in 130 cadavers. The largest surgical study, by Greenfield and Curtis in 1942, included 119 operations with an incidence of 24.4%, as reported by Kelley [11].
Kelley was the first to address the differing reports of frequency with a physiologic definition for the APN: if the PN is paralyzed and the ipsilateral diaphragm continues to move, it is assumed that an APN exists; if a second nerve is severed resulting in ipsilateral paralysis of the diaphragm, this is proof that the APN is identified [11]. Using these criteria, he reported conclusive proof of an APN in 80.9% of 309 surgical cases.
In the current study, which is concerned with anatomic variation, it was important to have consistent criteria for identifying APNs. We decided that all nerves contributing to the PN after it had crossed the anterior scalene would be considered as APNs. Although it is not clear whether previous authors of anatomic studies used a similar criterion for identifying APNs, our reported frequency of 61.8% agrees closely with the results of Aycock and Habliston as reported by Kelley [11].
The results of our study agree with texts describing the nerve to subclavius as the major origin of the APN [1, 2]. We also found that the ansa cervicalis and nerve to sternohyoid are the next most common origins of an APN. Several texts [1, 2] describe the course and communication of the APN with respect to the PN, although little information is available about their variations. Previous descriptions place the APN strictly lateral to the PN [2], but we found the APN descending medial to the main trunk in 9 specimens (9.1%). The connection between the PN and APN is described as occurring posterior to (or forming a loop around) the subclavian vein [1]; however, without reports on the frequency of the APN/PN connection it was not possible to compare results.
The frequency of an APN warrants inclusion in descriptions of normal anatomy and justifies considerations of its clinical significance. In 1973, Talbot [12] considered the anatomy of the PN and APN when trying to account for transient PN paralysis and diaphragmatic palsy after subclavian venipuncture. He reported an APN in 45% of his specimens, with the APN crossing the subclavian vein anteriorly in every instance. He listed local anesthetic and trauma from the cannulating needle as possible causes of injury. This study found the APN traveling anterior to the subclavian vein in 28.1% of all specimens, half of Talbot's reported 45% incidence.
Transient paralysis of the diaphragm has also been linked to supraclavicular nerve block [13]. Neal and colleagues [13] reported that supraclavicular nerve block was associated with a 50% incidence of hemidiaphragmatic paresis that was not accompanied by clinical evidence of respiratory compromise. The contributions from the brachial plexus to the PN via the APN may account for this finding. Gray's Anatomy [1] states that when avulsing the PN to immobilize the diaphragm, if it is part of an APN/PN loop, damage to the subclavian vein may occur. We found such loops in 45.5% of our specimens.
Studies have shown that CABG procedures have associated PNI [3–5], with levels of morbidity after iatrogenic injury varying across patient types [7]. Cohen and colleagues [7] showed that patients with COPD and PNI after CABG had significantly worse survival than patients with only COPD or PNI undergoing the same procedure [7]. Surviving patients with COPD and PNI also had more complications, readmissions, and a worse quality of life compared with other groups [7]. High mobilization of the ITA [6, 7], devascularization of peri-PN blood vessels [8], surgical manipulations of the PN [6, 9], and cardioplegia from saline slush application [4] put the PN at risk during cardiac procedures.
When sensitive tests are used after cardiac surgery, PNI has a reported frequency of 10% to 85% [9, 13–17]; however, these studies do not take into account the role that the APN may play. This is understandable considering the extensive surgical dissection required to uncover the range of APNs contributing to the PN and the APN's obscurity. It is our opinion that all in cases where injury to the PN is considered, injury to the APN should also be considered.
This study found APN/PN loops around the RITA in 31 specimens (31.3%) and around the LITA in 7 (7.1%). These findings may complicate the surgical picture involved with ITA harvest. High mobilization and skeletonization of the ITA may place the APN at risk for increased PNI [6, 8]. Based on our study, we propose the use of the second as a surgical landmark for locating the APN around the RITA and LITA.
Deng and colleagues [6] attribute differences in the incidence of PNI after LITA and RITA harvesting to the differences between the left and right PN's relationship to the neighboring vasculature [6]. O'Brien and colleagues [8] showed in a swine model that high LITA mobilization decreased left PN perfusion by 71%, with resultant impaired nerve function, but that only minimal changes were associated with high RITA mobilization. Our study found APNs to be more frequent on the right side (75.8%) than the left (24.2%). The higher frequency of right-sided APNs found in our study, along with the right PN's close course with the RITA [1], may contribute to the difference in frequency of left and right PNI by offering protection to the right hemidiaphragm through split innervation.
A common diagnostic criterion is needed to describe accurately the incidence of injury to the PN and APNs. The current criterion for classifying a PNI varies across reports [3, 4, 10] but generally rests upon the clinical finding of diaphragmatic hemiparesis rather than direct observation of nerve transection. Because the hemiparesis may be due to a PNI or an accessory PNI, it may be helpful to classify this clinical symptom under "diaphragmatic dysfunction" unless specific nerve transection is observed intraoperatively. This distinction may help to include the APN in discussions of the causes of transient and permanent diaphragmatic dysfunction.
Based on the clinical findings of others, our study assumes that the APN contains motor fibers. Although physiologic investigations of the innervation of the diaphragm have been conducted over the years, a study specific for the APN has not been repeated since Kelley [11]. This leaves open the question of what specific fibers the APN carries, and what variation is seen in motor and sensory contribution based on the origin of the APN and the level at which it joins the PN. Additional studies could prove useful in establishing the electrophysiologic properties of the APN.
We hope that this study will provide valuable data to clinicians, researchers, and anatomists alike by adding to the specific description of the APN. For the clinician in particular, procedures involving thoracic structures call for extensive knowledge of all the possible anatomic variations. It is conceivable that the application of this data will prove useful in the discussion and reduction of phrenic nerve lesions and diaphragmatic dysfunction after thoracic procedures, with subsequent decreases in hospitalization and total cost of patient care.
A limitation of the study is that it was not possible to do a physiologic investigation of the APN, as pioneered with Kelley's criteria [11], because it was strictly anatomic. This limitation has left open the question of the nature of those fibers carried by the APN. Furthermore, it was beyond the scope of this study to investigate the distances from the origin of the APN to its communication with the PN across the variation of APNs.
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Acknowledgments
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We would like to acknowledge Dr Stephen Clinch for his valuable comments.
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References
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Abstract
Introduction
