Symptomatic pain treatments (carbamazepine and gabapentin) were tried and had only a transient and incomplete effect on the severe pain syndrome.
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1 Laurencin 1 Appendix e-1 Supplementary Material: Clinical observations Patient 1 (48-year-old man) This patient, who was without a notable medical history, presented with thoracic pain and cough, which led to the performance of a thoracic scan. The scan revealed a mediastinal tumor. The biopsy revealed a malignant thymoma. No myasthenia was associated. Three weeks later, before the onset of treatment for the malignant thymoma, he presented with diffuse fasciculations, cramps, excessive sweating and insomnia. He complained of severe pain in his hands and feet, with burning and electric discharge sensations. Clinical examination showed symmetrical thermal and pinprick hypoesthesia, with allodynia in his hands and feet. There was no autonomic disorder other than hyperhidrosis. Anti-CASPR2 antibodies were detected in serum but not in the CSF (cerebrospinal fluid). Electroneuromyogram (EMG) confirmed the presence of neuromyotonia (NM) with fasciculations and myokymic discharges. Motor and sensory nerve conduction studies were normal. The patient showed a pathological hypersensitivity to the laser stimuli during laser evoked potentials (LEPs). Average scalp-recorded responses to repeated runs of 15 laser stimuli applied to both feet and the left hand were reduced and time-dispersed, with preserved peak latencies. The N2/P2 latencies were 260/320 ms for the left upper limb. No reproducible N2/P2 component was visible in the single-trial responses after foot stimulation, and the N2/P2 complex was absent in the averaged waveform (Figure 1). The cutaneous sympathetic response (CSR) was absent at all stimulated sites. Skin biopsy revealed no abnormalities in intra-epidermal fiber nerve density (IEFND) at the proximal and distal sites. Polysomnography recording showed a reduced total sleep time (215 min). Nevertheless, global sleep macro- and microarchitecture were preserved, except for REM sleep latency, which was increased, most likely due to the ongoing pain relief and antidepressant treatment. According to the patient, the night wakings were related to pain and NM. Brain and spinal magnetic resonance imaging did not reveal any abnormalities. The malignant thymoma was treated with chemotherapy (4 cycles of cisplatin, Adriamycin, and cyclophosphamide) and then thymectomy 6 months after the diagnosis. Symptomatic pain treatments (carbamazepine and gabapentin) were tried and had only a transient and incomplete effect on the severe pain syndrome. The Morvan syndrome (MoS) was treated with steroids, immunoglobulins (IVIg) and plasmapheresis concomitantly, but the pain persisted, so compassionate treatment with
2 Laurencin 2 rituximab was undertaken. This treatment resulted in rapid and dramatic improvement within a few weeks, with a strong reduction in the pain sensations. Both the clinical examination and EMG results returned to normal after treatment. Anti-CASPR2 antibodies were no longer detected 12 months later. Patient 2 (41-year-old man): This patient, who was without a notable medical history, developed a swallowing disorder at the age of 40 years and presented suddenly with an acute respiratory distress coma, leading to the diagnosis of myasthenia. In this context, a thoracic scan was performed, and a thymic mass was also discovered. The biopsy led to the diagnosis of malignant thymoma. Chemotherapy (4 cycles of carboplatin and Taxol) was given, while a polyvalent immunoglobulin treatment was used to control the myasthenia. Then, mediastinal tumor surgery was performed. The patient received a final dose of 54 Gy of radiotherapy. The cancer treatment was completed 8 months after the initial symptoms. In addition, immunosuppressive treatment with CellCept was introduced to better control the myasthenia symptoms. One year later, he presented with diffuse fasciculations, myokymia, excessive sweating and insomnia. He complained of severe pain in his hands and feet, with a burning sensation. Clinical examination showed allodynia in his hands and feet. There was no autonomic disorder other than hyperhidrosis. Anti-CASPR2 antibodies were detected in serum but not in the CSF. EMG confirmed the presence of NM (myokymic discharges and prolonged motor unit discharge after M-waves). LEPs showed normal averaged scalp-recorded responses to stimuli applied to the hands, whereas responses to stimuli applied to the feet were time-dispersed, with preserved peak latencies. The N2/P2 latencies were 234/328 ms for the right upper limb, 246/328 ms for the left upper limb, 262/328 ms for the right lower limb and 289/371 ms for the left lower limb. All of the potentials exhibited amplitude of between 9 and 10 µvolts. The CSR was smaller at the feet than at the thighs. The patient had pathological hyposensitivity to the laser stimuli. Skin biopsy revealed a decrease in IEFND at the proximal and distal sites with no proximal/distal gradient, suggesting non-length-dependent small fiber neuropathy. Polysomnographic recording showed severe insomnia (total sleep time = 132 min), with no REM sleep and no slow-wave sleep, a notable index of microarousal (= 36) and no circadian organization of the vigilances stages. Sleep spindles had disappeared. Brain and spinal magnetic resonance imaging did not reveal any abnormalities.
3 Laurencin 3 He underwent IVIg and steroids to treat the MoS, but these treatments had only a transient and incomplete effect on the severe pain syndrome and insomnia, so rituximab treatment was added. This addition resulted in dramatic improvement within a few weeks, with a strong reduction in the pain sensations and insomnia. Patient 3 (29-year-old man): At the age of 27 years, this patient presented with a diplopia, revealing myasthenia gravis. A thoracic scan revealed a mediastinal tumor. The biopsy revealed a malignant thymoma. The patient was treated with neoadjuvant chemotherapy (cisplatin, cyclophosphamide and doxorubicin) for 2 months, followed by thymectomy 4 months later. Six months after this treatment, the thymoma relapsed, and a complementary metastasectomy had to be performed. The myasthenia gravis was treated with IVIg, pyridostigmine and, occasionally, plasmapheresis. One year after the onset of the myasthenia gravis, he presented with diffuse fasciculations, cramps, distal neuropathic pain, excessive sweating and insomnia. He complained of severe pain in his feet, with a burning sensation. Clinical examination showed allodynia in his feet. There was no autonomic disorder other than hyperhidrosis. Anti-CASPR2 antibodies were detected in serum but not in the CSF. EMG confirmed the presence of NM (fasciculation and myokymic discharges). Motor and sensory nerve conduction studies were normal. LEPs showed normal averaged scalp-recorded responses to stimuli applied to his hands, whereas the responses to stimuli applied to his feet were time-dispersed, with preserved peak latencies. The N2/P2 latencies were 195/250 ms for the right upper limb, 203/297 ms for the left upper limb, 234/328 ms for the right lower limb and 227/324 ms for the left lower limb. All of the potentials exhibited normal amplitude. The CSR was absent at all stimulated sites. Skin biopsy revealed normal IEFND but an abnormal ratio between the proximal and the distal site. Polysomnographic recording showed reduced total sleep time (510 min), with a notable index of microarousal (=56) but no circadian organization of the vigilances stages. Slow-wave sleep was reduced (9%), and sleep spindles were absent. Brain and spinal magnetic resonance imaging did not reveal any abnormalities. The MoS was treated with IVIg with only a transient effect on the severe pain syndrome, so rituximab treatment was added. It resulted in dramatic improvement within a few weeks, with
4 Laurencin 4 a strong reduction in pain sensations and a decrease in insomnia. Patient 4 (62-year-old woman): This patient developed myasthenia gravis at the age of 52 years. A thoracic scan was performed, and a mediastinal mass was discovered. The biopsy revealed a malignant thymoma. She was treated with thymectomy and chemotherapy (ifosfamide, etoposide, and cisplatin); 3 years later, she relapsed, and metastasectomy and radiotherapy were required. The myasthenia gravis was treated with IVIg, pyridostigmine, and azathioprine. Ten years later, when she was 62 years old, she presented with diffuse myokymia, excessive sweating and insomnia. She complained of severe pain in her feet, with burning and electric discharge sensations. Clinical examination showed allodynia in her feet. There were autonomic signs, such as excessive sweating and orthostatic hypotension. Anti-CASPR2 antibodies were detected in serum but not in the CSF. EMG confirmed the presence of NM (fasciculation and myokymic discharges). Quantitative thermal sensory tests showed abnormalities linked to C fibers in the two feet, while the hands were normal. LEPs revealed no signs of small fiber dysfunction, except for the absence of CSR and hyposensitivity to the laser stimuli. The N2/P2 latencies were 207/289 ms for the right upper limb, 175/269 ms for the left upper limb, 226/308 ms for the right lower limb and 226/320 for the left lower limb. All of the potentials exhibited a normal amplitude. Skin biopsy revealed a decrease in IEFND at the distal leg compared to the proximal thigh. Polysomnographic recording showed a reduction of total sleep (total time of sleep = 430 min) and an increased microarousal index (= 69), with no circadian organization of the vigilances stages. Slow-wave sleep was reduced (7%), and sleep spindles were absent. Brain magnetic resonance imaging revealed white matter abnormalities. She received partially effective symptomatic pain treatment with pregabalin, morphine, clomipramine and IVIg. The neuropathic pain was still present but was less intense and fluctuating. She died suddenly at home due to a suspected pulmonary embolism.
5 Laurencin 5 Figure 1: HEK 293 cells expressing CASPR2 protein react with serum from patient 1 (A). This reactivity co-localizes (C) with the reactivity of a rabbit antibody against CASPR2 (B). No reactivity was observed with the serum from a control healthy patient (D, G). In panels C and F, the cell nuclei were visualized with 4,6-diamidino- 2-phenylindole (DAPI). In panels B and E, CASPR2 was labeled with a rabbit anti- CASPR2 antibody (ab33994, Abcam, Paris, France).
6 Laurencin 6 Figure 2: Laser-evoked potentials in patient 1 A. Nociceptive potentials evoked by laser stimulation of the left hand and left foot in patient 1 (48 years old) and in a 49-year-old control subject. Vertex (Cz) to nose derivation. In each panel: - Upper traces: superimposition of 10 single-trial responses - Lower trace: averaged waveform In the patient, the negative and positive (N2/P2) responses to hand stimulation were poorly reproducible and absent in several single trials. The N2 and P2 voltages were reduced in the averaged waveform (latencies of ms). No reproducible N2/P2 component was visible in the single-trial responses after foot stimulation, and the N2/P2 complex was absent in the averaged waveform. In the control, the main N2 and P2 components of the LEP were clearly visible in single-trial responses to hand and foot stimulation, peaking at latencies of
7 Laurencin 7 ms and ms after hand and foot stimulation, respectively. The amplitude of the averaged waveform was 23 μv for hand stimulation and 12 μv for foot stimulation. B. The cutaneous sympathetic responses to foot stimulation in the patient and the control. There was no response in the patient and a normal response in the control. Figure 3: Skin biopsies 20x, immunohistochemistry, intra-epidermal nerve immunostaining with a PGP 9.5 antibody. A: Patient 2, proximal biopsy, intra-epidermal nerve fiber density = 2.95/mm (normal > 5.2). B: Control, intra-epidermal nerve fiber density = 8.41/mm.
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