From Targeted Fascicular Biopsy of Major Nerve to Targeted Cutaneous Nerve Biopsy: Implementing Clinical Anatomy Can Catalyze a Paradigm Shift

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1 Clinical Anatomy 31: (2018) EDITORIAL From Targeted Fascicular Biopsy of Major Nerve to Targeted Cutaneous Nerve Biopsy: Implementing Clinical Anatomy Can Catalyze a Paradigm Shift TOMAS MAREK, 1 B. MATTHEW HOWE, 2 KIMBERLY K. AMRAMI, 2 AND ROBERT J. SPINNER 1 * 1 Department of Neurologic Surgery, Mayo Clinic, Rochester, Minnesota 2 Department of Radiology, Mayo Clinic, Rochester, Minnesota TARGETED FASCICULAR BIOPSY OF MAJOR NERVES Over the past fifteen years, our group has introduced a technique targeted fascicular biopsy (Capek et al., 2015; Laumonerie et al., 2017) in order to diagnose patients with unknown progressive neuropathy and MRI abnormalities of major nerves not diagnosed with noninvasive tests. The noninvasive diagnostic studies include neurologic evaluation, electrophysiological testing, and high resolution MR imaging (PET- CT is often performed in addition to MR when malignancy is suspected). During this time period, we have successfully performed targeted fascicular biopsy of a proximal nerve in >300 patients at our institution. The inspiration for the targeted fascicular biopsy was stereotactic biopsy, a technique where neurosurgeons three-dimensionally target an intracranial lesion seen on imaging. Analogously, peripheral nerve surgeons can use a minimally invasive technique to target an MRI abnormality using anatomic coordinates and perform an open procedure through a 6 8 cm incision to harvest at least a 6 cm fascicular biopsy (a longitudinal segment of nerve of similar size as that often obtained in distal cutaneous nerve biopsies). Previous non-targeted distal cutaneous nerve biopsy (i.e., sural nerve) as a part of a diagnostic algorithm was of relatively low yield. The explanation was simple: not every disease affects the whole course of a peripheral nerve (Spinner et al., 2010). Diagnostic yields of targeted fascicular biopsy have been 74% (Laumonerie et al., 2017) and 85%(Capek et al., 2015) while (non-targeted) distal cutaneous nerve have ranged from 20% to 50% (Hart et al., 2013). A wide variety of diagnoses have been made utilizing a targeted approach, including inflammatory and neoplastic lesions and the accurate diagnosis led to targeted treatment. Therapy with steroids or intravenous immunoglobulin (IVIG) was initiated in patients where inflammatory process was an underlying cause. In patients with malignancies, appropriate chemotherapy, radiotherapy, or hormonal therapy was administered. With this technique, new deficits have been rarely experienced and have typically been minor and transient; new permanent or increased deficits were reported in <5% of the patients (Capek et al., 2015; Laumonerie et al., 2017). TARGETED CUTANEOUS NERVE BIOPSY A targeted cutaneous nerve biopsy can be envisioned as a safer and easier technique to perform than a targeted fascicular biopsy to establish a correct diagnosis. First, biopsy of cutaneous nerves is safer procedure for patients because of lower risk of serious consequences such as permanent neurologic deficits. Second, performing a biopsy of superficial cutaneous nerve(s) is less invasive than a fascicular biopsy of a major nerve (i.e., brachial plexus). Lastly, the procedure is faster and perhaps more cost effective. Case Illustrations We illustrate this technique with four patients with idiopathic brachial plexopathy to demonstrate the utility of this technique. These cases had radiologic abnormalities involving the brachial plexus, and on closer review, the cutaneous nerves as well. Instead of targeting the pathology in the brachial plexus, the great auricular (Figs. 1 3) or supraclavicular (Fig. 4) nerve was biopsied. Three cases were done through small open incisions, and one with a mass and suspected malignancy, underwent a percutaneous Conflict of interest: None *Correspondence to: Robert J. Spinner, M.D., Mayo Clinic, Gonda 8-214, Rochester, MN 55905, USA. spinner.robert@mayo.edu Received 27 November 2017; Accepted 3 December 2017 Published online 30 January 2018 in Wiley Online Library (wileyonline library.com). DOI: /ca VC 2018 Wiley Periodicals, Inc.

2 Editorial 617 Fig. 1. A 37-year-old woman presented to our institution in March 2002 for further evaluation of her complex neurologic issues occurring for 6 years. MRI of the head and neck revealed lobulated enhancing masses extending along the cervical and upper thoracic nerves and also extending to the brachial plexus bilaterally. The differential diagnosis included neurofibromatosis, schwannomatosis, and CIDP. Biopsy of the left great auricular nerve was performed. A histopathologic diagnosis of CIDP was confirmed. A: An axial fat-saturated fast spin echo (FSE) image demonstrates lobulated hyperintense masses extending along the course of the cervical nerves. Lesions can be traced extending medially from the neural foramina and laterally into the proximal brachial plexus (arrows); B: An axial FSE image shows a markedly abnormal lobulated hyperintense left great auricular nerve (arrow) that matches the pathology of the cervical nerves and brachial plexus; C: An operative photograph shows the edematous appearing great auricular nerve (GAN). Fig. 2. A 48-year-old woman with a history of melanoma in the angle of the right jaw previously excised was evaluated in our institution in 2014 for atrophy of the right neck muscles, a palpable painful mass in the right neck area, and progressive right brachial plexopathy. MRI revealed radiological changes in cervical plexus and its branches (i.e., great auricular, transverse cervical) as well as in the brachial plexus consistent with features found in perineural spread of a tumor. The patient underwent an open biopsy of the great auricular and transverse cervical nerves. Pathologic examination confirmed melanoma (Restrepo et al., 2015). A: Coronal T1-weighted fat-saturated gadolinium enhanced image demonstrating enhancement of C4 and C5 nerves extending into the upper trunk of the brachial plexus (arrowheads); B: Axial T1 weighted fat-saturated gadolinium enhanced image demonstrates enlargement and enhancement of the great auricular nerve (arrow) at the level of C2. C: An operative photograph showing GAN and discolored nodular lesion within the nerve (arrowhead).

3 Fig. 3. A 79-year-old man with a 23-year long history of melanoma presented to our institution with a progressive right brachial plexopathy in April MRI imaging revealed radiological features consistent with perineural spread of tumor from great auricular and/or lesser occipital nerve to the brachial plexus. Fine-needle aspiration of subcutaneous nodularity corresponding with a site where a junction of great auricular nerve and transverse cervical nerve is located was performed. Pathology revealed melanoma. A: Axial T1-weighted fat-saturated gadolinium enhanced image demonstrating enhancement of the right C4 (hollow arrowhead) and C5 (arrow) nerves. Enhancement corresponding with cutaneous branch of C3 is noted (arrowhead); B: A coronal spoiled gradient recalled echo (SPGR) fat-saturated image demonstrating post gadolinium enhancement and enlargement of the right C5 nerve (arrow) and linear enhancement extending into the subcutaneous tissue (arrowheads); C: US image showing biopsy site (dashed circle) and aspiration needle (arrow) during the biopsy. Fig. 4.

4 Editorial 619 Fig. 5. Based on clinical anatomy (Left), the pathogenesis of skin cancers of scalp and neck can be understood. A road map for perineural spread is presented (Middle). The cervical plexus is depicted as a hub of the cutaneous nerves represented with solid lines (anterior rami); dashed lines are used for the posterior rami, which pass indirectly to the cervical plexus. A targeted cutaneous nerve biopsy can be considered based on the improved understanding of the pathogenesis (Right) (with permission, Mayo Foundation, 2017). fine-needle aspiration with ultrasound guidance. One case confirmed an inflammatory condition (CIDP) and three, perineural spread of a previously treated skin cancer. The case illustrated in Figure 4 had no radiological abnormalities of cutaneous nerves. In this particular case, cutaneous nerves (i.e., supraclavicular nerves) were targeted based mainly on previous history of the disease and rigorous physical examination. Institutional Review Board approval was obtained for this work as well as patient consents. A PARADIGM SHIFT: AN EVOLUTION OF A TECHNIQUE In the past, we performed distal cutaneous nerve biopsies exclusively. With improved imaging over the past two decades we have been targeting nerve pathologies more proximally within major nerves to improve diagnostic yields (Capek et al., 2015; Laumonerie et al., 2017). Is it time to consider targeted cutaneous nerve biopsies in selected cases? If we Fig. 4. An 82-year -old woman with a history of cutaneous squamous cell carcinoma presented to our institution in August 2017 because of progressive symptoms including neck and shoulder pain, right arm weakness, and sensory loss and shortness of breath. The patient s MR imaging was suggestive of perineural spread of tumor. The right supraclavicular nerves and the subclavius nerve were biopsied. Histopathologic examination revealed squamous cell carcinoma in all specimens. A: Sagittal oblique fat saturated post gadolinium MR image demonstrates abnormal central enhancement of the supraclavicular brachial plexus (arrow); B: A coronal fat saturated gadolinium enhanced image demonstrates asymmetric enhancement of the right brachial plexus (arrow); C: An operative photograph depicting open biopsy of supraclavicular nerves (arrowheads). D: An operative photograph showing the same open biopsy. Biopsied subclavius nerve (arrowhead) is visible as well as the upper trunk of the brachial plexus (UT).

5 620 Marek et al. (Restrepo et al., 2015) in patients with skin cancer from cutaneous nerves to major nerves whether following a path of least resistance or tropism. Understanding the pathogenesis of skin cancers in the neck region, we propose a road map based on knowledge of clinical anatomy for possible sites for diagnostic biopsy (Figs. 5 and 6). With further refinements, we believe it is time to consider moving from the deep biopsy (inside) back to the superficial (outside) in selected cases. Improved technology with high resolution MR imaging, and increasing experience of radiologists in peripheral nerve pathology has led to the appreciation and visualization of abnormalities affecting smaller, more superficial nerves. We recognize that subtle abnormalities affecting small nerves may not be visualized with current technologies (exemplified in Case 4 where the pathway was suspected clinically, but could not be confirmed radiologically). With further development of technology and with radiologists becoming more experienced in peripheral nerves evaluation we can predict that subtle changes on imaging of peripheral nerves will become easier to appreciate. With more experience comes knowledge and then new ideas (Fig. 7). The pendulum is changing. We Fig. 6. Diagnostic biopsy sites are shown illustrating the techniques of targeted cutaneous nerve biopsy and targeted fascicular biopsy. Blue dots represent spread of a disease (with permission, Mayo Foundation, 2017). understand the path of nerves and pathology affecting them, we can selectively target minor cutaneous branches that are connected to the affected major nerves. For example, inflammatory conditions (e.g., CIDP) can affect both proximal major nerves (i.e., brachial plexus) and distal cutaneous nerves. Neoplastic processes can extend by perineural spread Fig. 7. The evolution of these techniques for nerve biopsy (with permission, Mayo Foundation, 2017).

6 Editorial 621 introduce this new technique based on maturation of ideas. CONCLUSION We have become aware of the importance of neural highways in disease processes, including recent advances related to benign entities such as intraneural ganglion cysts or malignant ones such as perineural spread of malignancy (Spinner and Capek, 2017). Armed with precise knowledge of clinical anatomy and pathophysiology of diseases affecting peripheral nerves and an understanding of three-dimensional anatomy on imaging, we are able to appreciate the path of the disease and abnormalities involving smaller cutaneous nerves not previously considered or evaluated on MR imaging exams. In carefully selected patients, we are able to offer less invasive and safer procedure in order to establish correct diagnosis. REFERENCES Capek S, Amrami KK, Dyck PJ, Spinner RJ Targeted fascicular biopsy of the sciatic nerve and its major branches: Rationale and operative technique. Neurosurg Focus 39:E12. Hart MG, Santarius T, Trivedi RA Muscle and nerve biopsy for the neurosurgical trainee. Br J Neurosurg 27: Laumonerie P, Capek S, Amrami KK, Dyck PJ, Spinner RJ Targeted fascicular biopsy of the brachial plexus: Rationale and operative technique. Neurosurg Focus 42:E9. Restrepo CE, Spinner RJ, Howe BM, Jentoft ME, Markovic SN, Lachance DH Perineural spread of malignant melanoma from the mandible to the brachial plexus: Case report. J Neurosurg 122: Spinner RJ, Capek S Adapting findings from rare peripheral nerve disorders can lead to broad applications in neurosurgery. Neurosurgery 64: Spinner RJ, Amrami KK, Dyck PJB Targeted fascicular biopsy: A surgical perspective. In: Dyck PJ, Dyck PJB, Engelstad JK, Low PA, Amrami KK, Spinner RJ, Klein CJ, editors. Companion to Peripheral Neuropathy: Illustrated Cases and New Developments. Philadelphia: Saunders Elsevier. p