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Unexpected vocal cord paralysis and myasthenia gravis in a patient with squamous cell lung cancer.

Francesca De Iuliis 1, Lucrezia Amoroso2, Luciana Blasi1, Stefania Vendittozzi2, Ludovica Taglieri1, Gerardo Salerno 1, Rosina Lanza3, Susanna Scarpa1.

1Experimental Medicine Department, 2 Radiology-Oncology and Anatomo-pathology Department, 3Gynecology and Obstetrics Department, Viale Regina Elena 324, University of Rome 'Sapienza', 00161 Roma, Italy.





To whom correspondence should be sent: Susanna Scarpa, 
Experimental Medicine Department 
Viale Regina Elena 324, University of Rome 'Sapienza', 00161 Roma, Italy.
e-mail: susanna.scarpa@uniroma1.it                           phone: +393395883081



ABSTRACT 
Vocal cord paralysis is a voice disorder that occurs when one or both the vocal cords don�t open or don�t close properly. This often determines difficulty in swallowing and coughing in the patient, because food or liquids slip into the trachea and the lungs. Vocal cord paralysis may be caused by trauma, malignancy, surgery, or intubation and has been sometimes described to follow vinca alkaloid treatment. Myasthenia gravis is an autoimmune disorder which can represent a paraneoplastic syndrome in cancer patients.
We report a 55-years-old male with non small cell lung cancer presenting�an�unilateral vocal cord paralysis�immediately after the treatment with gemcitabine, and myasthenia gravis one week after.
To date, there aren�t any data in the literature describing causal relationships between non small cell lung cancer and myasthenia gravis; here we suggest that myasthenia gravis simultaneous to lung cancer might be a rare form of paraneoplastic syndrome. Whereas it is impossible to find a single cause for the vocal cord paralysis, we suggest a multifactorial pathogenesis, not excluding the possibility of a single rare paraneoplastic syndrome that includes both myasthenia gravis and vocal cord paralysis.

Key words:  non small cell lung cancer (NSCLC); vocal cord paralysis; paraneoplastic syndrome; myasthenia gravis; quality of life; lung cancer.





INTRODUCTION

Advanced lung cancer is one of the most aggressive neoplasias and one of the less responsive to treatments. The primary goal of management of these patients is to improve their quality of life, since this is often compromised as a result of underlying disease and side effects of chemotherapy  (1). Neurological complications frequently occur in patients with cancer as side effects of medication, compression or tumor invasion of nerves or lymph nodes. In 20% of lung cancer cases, neurological symptoms can be associated with various paraneoplastic syndromes  (encephalomyelitis, sensory neuropathy, myasthenia). Several antineoplastic drugs (cisplatin, taxanes, vinca alkaloids) widely used in the treatment of lung cancer can cause neurological toxicity related to impaired nerve transmission, especially in predisposed patients or patients with neurological comorbidities.Lambert-Eaton myasthenic syndrome (LEMS) and myasthenia gravis (MG) are well known classical paraneoplastic syndromes of small cell lung carcinoma (SCLC), but not of NSCLC.
We report a clinical case of a 55 years-old patient with diabetes mellitus in absence of neurological deficit, that was treated for a locally advanced squamous cell carcinoma of the lung. Hepresented dysphonia and aphonia at the end of the first infusion of gemcitabine, and developed a MG after one week.


CASE REPORT

A 55-year-old man, with�40 pack-year history�of�smoking, was referred to our hospital because of� sharp chest pain that spread to the left side of the chest for a week and weight loss in two months. The pain was not associated with cough and physical exercise and it didn�t change location. He complained of hemoptysis, hoarseness and dyspnea, swelling of the lower extremities and loss of appetite.  His medical history was significant for myocardial infarction, diabetes mellitus and hypertension. Blood tests were normal except for hemoglobin (Hb = 9.5 g/dl); serum tumor markers (CEA, CA125, CA19.9) were negative. A chest CT revealed a 4.5 cm circumscribed mass in the left lung hilum that infiltrated the middle and posterior mediastinum, the left pulmonary artery and the left main bronchus, with lymphadenopathy in the hilum and aortopulmonary window (Fig.1).   The diagnosis of poorly differentiated squamous cell carcinoma was performed on the bronchoscopic biopsy.
Bone scintigraphy was negative; after cardiological evaluation and echocardiogram (ejection fraction was 45%), the patient underwent 3 cycles of carboplatin (AUC 5) + vinorelbine 30 mg/mq d1, 8 q21. The patient didn�t report any side effect from the chemotherapy. 
At the end of the chemiotherapy, a CT scan showed an increase of the left lesion and other small lesions in the lung left lower lobe. So the patient underwent three cycles of docetaxel 75 mg/mq d1 q21 without significant toxicity. Unfortunately, a CT scan assessment showed progression of lung disease. 
Considering the good general conditions of the patient and the absence of side effects associated with the treatment, the patient was submitted to a third-line chemotherapy with gemcitabine 1000 mg/mq  d 1, 8 , 15 q28.
At the end of the first infusion, the patient developed hoarseness and stridor, progressing to nearly total aphonia. A flexible fiber optic endoscope showed the left vocal cord in abducted position with loss of movement. Otolaryngology evaluation and flexible laryngoscopy confirmed the diagnosis of unilateral irreversible left vocal cord paralysis (VCP). 
He had neither previous clinical symptoms nor positive history for inherited neuropathy, and neurological examination did not reveal any deficiency or peripheral neuropathy. 
A contrast enhanced CT scan of soft tissue neck was normal and ruled out a metastatic compression from adenopathy along the course of the recurrent laryngeal nerve, while the images of the chest confirmed enlargement of the lung cancer and metastatic nodes in the aortopulmonary window (Fig. 2).  
Complete blood chemistry, electrolytes and serum proteins were normal. Tests to detect the presence of any anti-lue antibody were performed in order to rule out any lue-correlated paralysis and they resulted negative. At that time the patient had been recommended to have further investigations but he refused any procedure (laryngeal electromyography, thyroid ultrasonography, esophageal transit, MRI of the neck). After one week he described symptoms of muscle weakness, diplopia, dysphagia, and fatigue; also a bilateral asymmetric ptosis was noted. A new neurologic examination was performed, which confirmed bilateral ptosis, moderate weakness in proximal muscles and low weakness in distal muscles, normal reflexes and normal sensory function. A test with 2 mg of intravenous edrophonium was performed, and it was positive. Serum antibodies against acetylecholine receptor (AChR-MG) and muscle-specific receptor tyrosine-kinase (MuSK-MG) were negative; while autoantibodies against the muscle proteins titin (positivity range 0.6-1.5 ng/ml) and ryanodin receptor (positivity range 0.3-20 ng/ml) have been detected. We suggested to the patient to perform a standard repetitive nerve stimulation (RNS) test, which is one of the most sensitive diagnostic test in patients with presynaptic neuromuscular junction (NMJ) disorders, to evaluate patient's muscle weakness and to confirm the diagnosis of myasthenia gravis. Taking the obtained data together and considering also the absence of a thymoma, the diagnosis of myasthenia gravis was determined. The patient refused any kind of examination and treatment, therefore a supportive care was proposed to him. After 3 months, a CT scan showed liver metastasis and disease progression (fig. 3), the patient had a progressive deterioration of general medical conditions, and�he died two weeks later.

DISCUSSION
Vocal cord paralisys (VCP) is a common disorder. The severity of voice and swallowing problems depend on the position where the nerve damage occurs and symptoms can range from mild to life threatening. It can be due to head and neck injuries, viral infections, neck or chest tumors, complications from endotracheal intubation, neurologic insults such as a stroke, or neurologic diseases such as multiple sclerosis or Parkinson�s disease. In many cases, however, the cause is unknown (2-3).
Metabolic diseases, such as diabetes mellitus, can cause VCP; however our patient�s diabetes was totally controlled by therapy, without showing any side effect, as demonstrated by blood tests and glycosylated haemoglobin, that were normal.
Treatment of VCP may include voice therapy, bulk injections, surgery or a combination of treatments. In some cases, the voice returns without treatment during the first year after damage. For this reason, doctors often delay corrective surgery for at least a year, to be sure that the voice does not recover spontaneously. During this time, the suggested treatment is usually voice therapy, which may involve exercises to strengthen the vocal cords or improve breath control during speech.  The surgery technique adds bulk to the paralyzed vocal cord or changes its position. 
Rare side effects of cisplatin and vincristine (4-6) therapy can be the one-sided paralysis of the vocal cord and this has never been described for other chemotherapeutic agents, not even for the gemcitabine.
Gemcitabine is an antimetabolite, mainly responsible for haematological (thrombocytopenia, neutropenia) and gastrointestinal (nausea, vomiting, diarrhea) toxicities. Neurotoxic side effects have not been described in relation to gemcitabine, except rare cases of reversible CNS symptoms (7).  In addition, our patient previously treated with carboplatin and vinorelbine, showed good tolerance and no neurological deficits.
We can�t exclude a paraneoplastic syndrome that is frequently associated with lung cancer (8-11). Paraneoplastic neurological syndromes (PNS) are rare and occur as a remote effect of tumors, not directly caused by mass lesions, metastases, infections, nutritional factors or anti-tumor treatment.  Small cell lung cancers (SCLC) are the tumors most frequently associated with PNS, while paraneoplastic syndrome is rarely correlated to NSCLC  (12-14).
 Our patient had a left lung collapse due to an enlarged mass in the left hilum, with an evidence of metastatic node in in the aortopulmonary window near the pathway of the left recurrent laryngeal nerve which may justify VCP, but not its fast onset. The neoplastic compression of laryngeal nerve is a theory that remains valid (15-17), although no diagnostic evidence was performed, but the most interesting feature was the sudden appearance of dysphonia immediately after the end of the infusion of chemotherapy. The suddenness of this dysphonia suggests an acute event (paraneoplastic syndrome?) rather than the result of a much slower invasive process. MG is an autoimmune neuromuscular disorder, considered as a paraneoplastic syndrome when associated with thymoma (in 15% of cases) or other malignancies.  The manifestations of MG are muscle fatigability and weakness, caused by antibody-mediated reaction against the nicotinic acetylcholine receptor (AChR) at the neuromuscular junction (18). The first clinical signs of MG are diplopia and ptosis, characteristic of the ocular form of the disease. In generalized MG, the weakness extends to bulbar muscles (with consequent dysarthria, dysphonia, chewing and swallowing difficulties), trunk muscles (respiratory difficulties), and limb muscles.  A recent paper has described the VCP as the first and only manifestation of MG in some patients (19). The Myasthenia Gravis Foundation of America Clinical Classification divides MG into 5 main classes and several subclasses (20). Our patient corresponded to Class IIa:  predominantly affected limbs, axial muscles and lesser involvement of oropharyngeal muscles. Many factors may trigger or worsen exacerbations of MG, and we suggest that chemotherapy may have permitted the onset of a paraneoplastic myasthenia-like syndrome in our patient. The patient did not agree to have further investigations, so it was impossible to perform an efficient investigation for the lack of compliance.  Whether the patient should have made a therapy with pyridostigmine, he could have quickly improved myasthenic symptoms, as demonstrated by the positive test with edrophonium. The steroid therapy should have been  proposed only at low doses and with strict control of blood glucose, considering the diabetes. The lack of compliance had worsened significantly the clinical outcome. Patients with lung cancer are very heterogeneous, and this case report demonstrates how the presence of a disabling health condition can have a serious impact on compliance and outcomes. Seemingly, severe symptoms, as in our case, can often determine a psychological distress and a consequent poor quality of life. 

CONCLUSION
The presence of disabilities parallel to a neoplasia often determines the impairment of quality of life and of compliance. Both VCP and MG have had a negative impact on the clinical history of our patient. To date, literature doesn�t describe any causal relationship between NSCLC and MG, so we suggest that simultaneous MG with lung cancer might be a rare form of paraneoplastic syndrome.
Whereas it is impossible to find a single cause for the VCP, we suggest a multifactorial pathogenesis, not excluding the possibility of a single rare paraneoplastic syndrome that also includes the MG.


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Figure legends
FIG. 1:  Contrast-enhanced CT prior to vocal cord paralysis demonstrates a 4,5 cm circumscribed mass in left lung hilum
FIG. 2:  CT after development of left vocal cord paralysis shows enlargement of the lung cancer and metastatic nodes in the aortopulmonary window.
FIG. 3: Liver metastasis








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