Clin Physiol Funct Imaging (2010) 30, pp107–115
doi: 10.1111/j.1475-097X.2009.00911.x
Electromyographic tools to assess hemidiaphragm paralysis Yves Jammes1,2, Ce´cile Budin-Poirier1,2 and Fabienne Bre´geon1,2 1
UMR MD2 (P2COE), Jean Roche Institute, Faculty of Medicine, University of Me´diterrane´e, and 2Lung Function Laboratory, North Hospital, Assistance Publique-Hoˆpitaux de Marseille, Marseille, France
Summary Correspondence
Non-invasive measurements of the phrenic nerve conduction time (CT) and diaphragmatic electromyographic response to voluntary inspiratory efforts may help to document an abnormal diaphragmatic function in the presence of hemidiaphragm elevation on chest radiographs. Twenty-one patients were addressed for the diagnosis of abnormal placement and motion of the right (13) or left (8) cupola on chest radiographs. CT was measured by recording the diaphragmatic M-wave evoked Accepted for publication by electrical transcutaneous phrenic nerve stimulation. The integrated diaphragmatic Received 12 June 2009; surface electromyogram (Edi) was recorded during sniff and Mu¨ller manoeuvres. accepted 15 October 2009 Four patients were followed up during the next 8–16 months. Among the twentyKey words one patients, five (24%) had a lengthened or absent CT. A right-to-left peak Edi diaphragm electromyogram; diaphragm paralysis; asymmetry was measured in fourteen (67%), including those having abnormal CT. maximal inspiration; phrenic nerve; sniff Agreement between side-related radiographic abnormalities and Edi asymmetry was high in the cases of an elevation of the right cupola (12 ⁄ 13, 92%) but poor when Abbreviations the left cupola was suspected (1 ⁄ 8, 13%). Long-term follow-up of Edi asymmetry ANOVA, analysis of variance; CT, phrenic nerve showed a partial or total recovery. Thus, the combination of measurements of conduction time; Edi, integrated diaphragmatic electromyogram; EMG, surface electromyogram; phrenic nerve CT and Edi recordings during voluntary inspiratory efforts confirmed FEV1, forced expiratory volume in 1 s; FVC, forced 67% of the radiographic suspicion of diaphragmatic dysfunction. Pr. Yves Jammes, UMR MD2 (P2COE), Jean Roche Institute, Faculty of Medicine, University of Me´diterrane´e, Marseille, France E-mail:
[email protected];
[email protected]
vital capacity; M-wave, evoked compound muscle action potential; PaCO2, arterial partial pressure of carbon dioxide; PaO2, arterial partial pressure of oxygen; PImax, maximal inspiratory mouth pressure; TLC, total lung capacity; VC, vital capacity.
Introduction The causes, clinical manifestations and exploration of diaphragmatic dysfunction are widely documented (Laghi & Tobin, 2003). Diaphragmatic dysfunction may result from the reduction or the suppression of the motor command through a phrenic nerve compression or section or neuronal lesions at the spinal or supraspinal level. They may also result from an impaired muscle contractility, accompanying inflammatory, infectious or haemorrhagic pleurisy (Malucelli & Mariano, 1980; Zifko et al., 2002) or simply result from a mechanical impairment of the diaphragmatic motion (through a disruption of the muscle structure or a decreased compliance of the surrounding tissues) (Laghi & Tobin, 2003). In routine medical practise, diaphragmatic dysfunction is often simply called diaphragm paralysis and suspected from hemidiaphragm elevation on chest radiographs. The radiographic and radioscopic criteria for diaphragmatic cupolae abnormality are well defined (Tarver et al., 1989; Laghi & Tobin, 2003; Verhey et al., 2007). Although more appropriate (Laghi & Tobin, 2003), ultrasonography is rarely primarily used to explore diaphrag-
matic function in our country, because of the higher cost and because it requires a trained practitioner. For about four decades, physiologists have developed noninvasive means to explore the motor command to the diaphragm using electrical or magnetic stimulation of the phrenic motoneurones (cervical stimulation) or the supraspinal structures (transcranial stimulation). The contractile diaphragmatic response is then assessed from recordings of the twitch mouth or trans-diaphragmatic pressure (Laroche et al., 1988), or the evoked electromyographic (EMG) potential called the M-wave (Newsom Davis, 1967; De Troyer & Vanderhoeft, 1982; Markand et al., 1984; McKenzie & Gandevia, 1985; Mier et al., 1987; Similowski et al., 1989, 1997; Chen et al., 1995; Zifko et al., 1996; Verin et al., 2002; Demoule et al., 2003; Glerant et al., 2006; Resman-Gaspersc & Podnar, 2008). However, twitch pressure changes or M-wave recordings have been rarely reported as diagnostic tools to complete the exploration of a diaphragmatic dysfunction (Newsom Davis, 1967; Moorthy et al., 1985; Gandevia, 1987; Mier et al., 1987; Wilcox & Pardy, 1989; Chetta et al., 2005). There is a dearth of data in the literature on the ability of physiological tools to explore the
2009 The Authors Journal compilation 2009 Scandinavian Society of Clinical Physiology and Nuclear Medicine 30, 2, 107–115
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108 EMG assessment of diaphragmatic dysfunction, Y. Jammes et al.
diaphragm complementary to X-rays assessments. We found two studies where the diaphragm M-wave recording was used to attest diaphragmatic dysfunction after surgical damage of the phrenic nerve (Newsom Davis, 1967; De Troyer & Vanderhoeft, 1982) or in patients with idiopathic diaphragmatic weakness (Moorthy et al., 1985; Mier et al., 1987). Recordings of twitch pressure changes or M-wave elicited by direct or indirect phrenic nerve stimulation are interesting tools that cannot prejudge on an altered recruitment of motor units during voluntary efforts because of myogenic disorders. As in skeletal muscles (Basmajian, 1962, 1980), the electrophysiological assessment of the diaphragmatic function might combine both M-wave recordings with the measurement of the conduction time (CT) and a quantitative EMG analysis during voluntary inspiratory efforts. Given our previous published works comparing patients with Steinerts myotrophic dystrophy (Jammes et al., 1985) with healthy controls (Badier et al., 1993, 1994), our team has the expertise of several electrophysiological diagnostic tools, including the recording of integrated diaphragmatic EMG (Edi) during Mu¨ller manoeuvres, that is a maximal inspiratory effort against an infinite resistance, and sniff manoeuvres. The aim of the present retrospective observational study was to assess the precise contribution of electrophysiological tools to explore the diaphragmatic or phrenic nerve function in patients referred to our lung function laboratory with unexplained dyspnoea, radiographic and radioscopic signs of an altered placement and motion of the diaphragmatic cupolae. We measured the M-wave CT, Edi in response to maximal voluntary efforts (sniff and Mu¨ller manoeuvres), and the maximal inspiratory mouth pressure (PImax) recorded during Mu¨ller efforts.
Material and methods Study subjects This 2-year retrospective study was carried out in twenty-one patients referred to our laboratory because of unexplained persistent dyspnoea at rest. Standard chest radiographs and radioscopy indicated alterations of placement and motion of a diaphragmatic cupola. Mean values of their age and weight are indicated in Table 1. Details on the possible causes of suspected diaphragmatic dysfunction are given in Table 2. Altered diaphragmatic function was suspected to be right in 13 patients and left in
eight patients. The risk factors for diaphragmatic dysfunction were a chest trauma caused by car accident (n = 6) or surgery (n = 2), neurological disorder (hemiplegia: n = 2; axonal polyneuropathy: n = 3; cervical arthritis: n = 2; Parkinson disease: n = 1), or acute pneumopathy with pleurisy (n = 1), but none could be specified in the four remaining subjects (idiopathic phrenic nerve paralysis). Chest radiographs and radioscopic examinations were performed by different experienced practitioners who followed the recommendations by Tarver et al. (1989). Data were compared to those measured in a control group of 10 healthy subjects (three females; mean age: 41 ± 13 year; mean weight: 69 ± 9 kg) initially explored to determine normal values of CT and mostly of right-to-left asymmetry in CT values and amplitude of integrated diaphragmatic electromyograms during voluntary manoeuvres. Their characteristics are shown in Table 3. The procedures were carried out with the adequate understanding and written consent of each subject. In parallel with pulmonary function measurements, all patients underwent the same protocol routinely used in our laboratory to examine the diaphragmatic function (Jammes et al., 1985; Badier et al., 1993, 1994). Our protocol of EMG examination of the diaphragm was approved by our Institutional Ethics Committee, which authorized the initial series of measurements in healthy volunteers 3 years ago. Study design We obtained standard face and profile chest radiographs and the written interpretation of the radiologist that attested to diaphragmatic motion abnormalities when present. In our laboratory, the pulmonary function was measured at rest using spirometry and plethysmography. Blood gases were also measured. Then, an EMG assessment of the diaphragmatic function was performed during which the patient was asked to perform sniff and Mu¨ller manoeuvres with recording of the inspiratory mouth pressure. Methods Lung function tests To evaluate the functional consequences of diaphragmatic dysfunction, spirometry with measurement of total pulmonary
Table 1 Characteristics of patients with abnormal chest radiographs and data on pulmonary function. Age year 60 18
Weight kg
FEV1 % pred
FEV1 ⁄ FVC % pred
TLC % pred
VC % pred
PaO2 mmHg
PaCO2 mmHg
81 23
65 27*
78 32*
72 23*
66 32
77 23
40 14
FEV1 (forced expiratory volume in 1 s), ratio between FEV1 and FVC (forced vital capacity), TLC (total lung capacity) and VC (vital capacity) expressed in percentage of predicted values (Quanjer, 1983). Arterial partial pressures of oxygen (PaO2) and carbon dioxide (PaCO2). Values are mean ± standard error (SD). Asterisks indicate significant modifications compared to predicted values (*P
