Electromyography of respiratory muscles in amyotrophic lateral sclerosis

Abstract

We reviewed the records of 52 amyotrophic lateral sclerosis (ALS) patients examined between 1995 and 2000 who had needle electromyography (EMG) of their respiratory muscles, including the diaphragm, at or near the time of their diagnosis. With respiratory function testing, patients with abnormal diaphragmatic EMG at diagnosis (Group 1, n=23) had significantly lower forced vital capacity (FVC), lower daytime arterial PO₂ and higher PCO₂ measurements (p<0.05) than patients with normal diaphragmatic EMG (Group 2, n=29). Twenty-eight percent of the patients without symptoms or signs of respiratory insufficiency at the time they were examined had an abnormal diaphragm EMG. Mean survival of Groups 1 and 2 were similar. However, sub-analysis of patients within each group, comparing those treated with non-invasive positive pressure ventilation (NIPPV) with those not treated, showed that treated patients in Group 1 (abnormal diaphragm EMG) survived significantly longer (p<0.05) than untreated patients. They also started NIPPV earlier than treated patients in Group 2. We conclude that respiratory muscle EMG was simply and safely performed on ALS patients at or around the time of diagnosis. The procedure can detect sub-clinical respiratory muscle dysfunction. The technique used for EMG of the respiratory muscles, its pitfalls and contraindications are also reviewed.

Introduction

Respiratory failure is the most common cause of death from amyotrophic lateral sclerosis (ALS) [1], [2], [3]. Occasionally, ALS may present with acute respiratory failure [4], [5] that invariably results from denervation of respiratory muscles. In non-respiratory onset ALS, clinical signs and symptoms of respiratory insufficiency at its earliest stage can be subtle, and easily overlooked in the face of other, more obvious disease-related challenges. Conventional methods of respiratory function testing may not detect early respiratory muscle dysfunction, and can be difficult to interpret in patients with established bulbar deficits[6], [7], [8]. At the same time, there is accumulating evidence that intervention with non-invasive positive pressure ventilation (NIPPV) improves quality of life and may increase survival in some patients [9], [10]. Detecting early respiratory dysfunction in ALS is therefore paramount, but is proving to be problematical. Needle electromyography (EMG) of the respiratory muscles is occasionally recommended in ALS electrodiagnostic protocols[11], but usually for patients with clinically apparent respiratory dysfunction. We propose that needle EMG of respiratory muscles may be of more value prior to this point.

Assessment of respiratory muscles using needle EMG is usually not a routine component of, or adjunct to, conventional electrodiagnostic protocols followed during the diagnosis and follow-up of patients with ALS. This may be due in part to fear of harming the patient [12], [13], [14], or to sparse published data supporting the utility of the procedure. However, at least one method for respiratory muscle EMG is proven to be simple and safe to perform in patients with neuromuscular disease [12], [15], [16].

In this paper, we report retrospective results of respiratory muscle EMG performed in 52 patients with ALS seen between 1995 and 2000. The results as they relate to other tests of respiratory function, use of NIPPV, and survival, are discussed.

There are three known methods for EMG study of the diaphragm, the principal, primary muscle of inspiration. The costal portion of the muscle can be studied substernally by inserting the needle beneath and along the posterior surface of the xyphoid process [17], or subcostally under the costal cartilage of the eighth, ninth or tenth rib [13], [14], as indicated in Fig. 1A. The most rigorously reviewed technique is that developed by Bolton [12], [15], [18], in which the costal diaphragm is accessed through the lower intercostal spaces which lie below the inferior border of the lung and pleura (Fig. 1A and B). A technique very similar to Bolton's was described more than 40 years ago in some of the first electrophysiologic studies on human respiratory muscle function [19]. All three methods require penetration of superficial, abdominal wall muscles which have important respiratory functions namely, but not exclusively, clearing of the airways and cough [20], [21]. However, only Bolton's technique provides information on the intercostal muscles, important for expanding and contracting the rib cage during resting and labored breathing [20], [22].

Respiratory muscle EMG using Bolton's intercostal technique is not without its challenges. The costal diaphragm is thin, approximately 3–4 mm, as it abuts the lower rib cage. This increases the potential for contamination, or “cross-talk”, from overlying muscles in the thoracoabdominal wall [23]. The continuous shortening and lengthening of the diaphragm with resting breathing, combined with the thinness of the muscle, makes stabilizing needle position and recording baseline somewhat more challenging. However, use of a modified high-pass filter (100–500 Hz) may help in selectively recording from each of the thin, overlapping muscle layers and in reducing baseline artifact [24], and in the authors' experience, without preventing recording of abnormal, spontaneous activity. Motor unit potentials in the diaphragm are of shorter duration, smaller amplitude, and are more numerous than in other muscles. In addition, partial voluntary contraction of the muscle is not possible. This makes analysis of MUP morphology and recruitment somewhat difficult [16], [25].

Substernal and subcostal techniques for diaphragm EMG may be more challenging due to the thickness of the anterior abdominal muscles and overlying subcutaneous tissue. In addition, placement of the needle in the diaphragm can be awkward as it must be advanced more or less parallel to the posterior surface of the sternum or rib cage. These techniques also require the electromyographer to apply continuous pressure to the abdomen with their free hand in order to keep major abdominal organs away from the path of the needle [13], [14].

Any of the techniques for needle EMG of the diaphragm are relatively contraindicated in patients with marked abdominal obesity or distention, local infection, marked chronic obstructive pulmonary disease (COPD), hepatomegaly, coagulopathies, frequent coughing or hiccups, or in patients who are unable to be positioned supine [26]. Bolton [12] reports only two cases of pneumothorax in over 1000 procedures, both occurring in patients with severe COPD and on ventilators.