Phrenic nerve and diaphragmatic dysfunction has been assumed to be the cause of respiratory failure in hereditary motor and sensory neuropathy, type 1 (HMSN I). In order to determine the relationship between phrenic nerve and pulmonary function in this disease, 25 patients underwent a 4-step evaluation process consisting of: (1) bilateral phrenic nerve conduction study; (2) median, peroneal, and tibia1 motor conduction studies; (3) measurement of forced vital capacity (FVC) and maximal inspiratory and expiratory pressures (MIP, MEP); and (4) pulmonary-focused history and physical. Phrenic nerve motor latency was abnormally prolonged in 22 of the 23 (96%) subjects when a response was obtained. All had slowed velocity or absent peripheral motor conduction responses. Vital capacity was abnormally reduced in 6 of the 25 (24%) subjects. Eight (32%) had an abnormally reduced MIP, while 19 (76%) had an abnormally reduced MEP. Only 2 (8%) subjects had clinical evidence of pulmonary dysfunction. None of the dependent variables (FVC, MIP, MEP, peripheral nerve conduction, or clinical examination) correlated with phrenic nerve latencies. Although phrenic nerve latencies are markedly prolonged in HMSN I, these values are not useful in predicting respiratory dysfunction. Key words: phrenic nerve hereditary motor and sensory neuropathy, type I pulmonary function Charcot-Marie-Tooth disease neuromuscular disease MUSCLE & NERVE 15:459-462 1992
EVALUATION OF PHRENIC NERVE AND PULMONARY FUNCTION IN HEREDITARY MOTOR AND SENSORY NEUROPATHY, TYPE I GREGORY T. CARTER, MD, DAVID D. KILMER, MD, H. WILLIAM BONEKAT, DO, JAMES S. LIEBERMAN, MD, and WILLIAM M. FOWLER, JR., MD
Hereditary motor and sensory neuropathy, type I (HMSN l), is a slowly progressive disease resulting in distal muscle weakness and atrophy, as well as impaired ~ e n s a t i o n . ~ ' ~Restrictive '" lung disease, common in many neuromuscular disorders, is not a predominant feature of HMSN I. Recently, however, there have been several case reports of From the Departments of Physical Medicine and Rehabilitation (Drs. Carter, Kilmer. Lieberman. and Fowler) and Internal Medicine, Division of Pulmonary Medicine (Dr Bonekat), University of California, Davis, California. Acknowledgments. Supported by Research and Training Center Grant H133880016-03and Research Training Grant G0087C2005 from the National Institute on Disability and Rehabilitation Research (NIDRR), United States Department of Education. The authors thank Merete Glick, RPT for her technical assistance with data collection in this study. Address reprint requests Gregory T. Carter, MD, University of California, Davis, Medical Center, Department of Physical Medicine and Rehabilitation, 4301 "X" Street, Room 2030, Sacramento, CA 95817. Accepted for publication April 24, 1991 CCC 0148-639X1921040459-04$04 00 0 1992 John Wiley & Sons, Inc.
Phrenic Nerve and Pulmonary Function in HMSN I
respiratory dysfunction in HMSN I, with some patients requiring mechanical ventilatory support.228718 Diminished maximal static airway pressures have also been reported, presumably due to impaired dia hra matic and chest-wall muscle function."*14" It ghas been assumed that the phrenic nerve may be involved and could account for the respiratory One report noted microscopic neuropathic changes in the phrenic nerve that were identical at autopsy to the histologic changes in the peripheral nerves in a 69year-old woman with HMSN I who died of respiratory failure. l o Despite these case reports, no investigation has prospectively determined the extent of phrenic nerve involvement and respiratory dysfunction in a cross-section of patients with HMSN I. Our study was designed to assess phrenic nerve function in patients with HMSN I, and determine its relationship to (1) vital capacity and maximal static respiratory pressures; (2) clinical signs and symp-
MUSCLE & NERVE
April 1992
459
toms of respiratory dysfunction; and (3) peripheral nerve function. MATERIALS AND METHODS
All 30 patients with HMSN I in the neuromuscular disease clinic at our institution were invited to participate in the study. Twenty-five agreed and signed a detailed consent form that outlined the research protocol as approved by the University Human Subjects Approval Committee. There were 12 female and 13 male subjects, with an average age of 39 years (range 11 to 65 years). Patients underwent an evaluation consisting of ( 1) pulmonary-focused history and physical examination, (2) pulmonary function tests (PFTs) consisting of forced vital capacity (FVC), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP); (3) bilateral phrenic nerve motor conduction studies; and (4) median, peroneal, and tibia1 nerve motor conduction studies. The history included questions related to shortness of breath with ambulation, at rest, and during sleep. Physical examination included auscultation of the heart and lungs and examination for thoracoabdominal paradoxical breathing in the supine position. FVC was measured using a Cybermedic Moose spirometer (Cybermedic Inc., Louisville, CO). MIP and MEP were measured near residual volume (RV) and total lung capacity (TLC) respectively, according to the technique described by Black and Hyatt.' A Boehringer direct reading dial gauge force meter (Boehringer Laboratories, Inc., Wynnewood, PA) was used for these measurements. Three technically satisfactory measurements were obtained, and the maximum reading recorded. Phrenic nerve conduction studies were performed using the technique described by Davis.4 Peripheral nerve conduction studies were performed in the standard fashion described by Ma and Liveson.I5 All phrenic and peripheral nerve conduction data was recorded, analyzed, and printed using a Teca Mystro EMG unit ('Teca Corp., Pleasantville, NY). Normal age- and sex-matched predicted values for FVC were obtained from the Intermountain Thoracic Society." FVC was defined as abnormal if less than 80% of the predicted value. MIP and MEP age- and sex-matched normal predicted values were obtained from Black and Hyatt.' Four subjects were under 20 years of age, and for this group we used the available MIP and MEP values for adults 20 years of age. Values for MIP and MEP were expressed as a percentage of the lower
460
Phrenic Nerve and Pulmonary Function in H M S N 1
limit of the normal predicted value range. Thus, any value 47 m/s) (Table 1). Both subjects without median nerve responses had marked thenar wasting and no voluntary movement of the thumb. Peroneal nerve responses were obtainable in 5 Peripheral
M U S C L E & NERVE
April 1992
Table 1. Electrophysiologic and pulmonary function data in the 25 subiects. Median Right MCV phrenic MIP MEP FVC Patient (misec) latency (ms) (% pred) (% pred) (% pred) 1 2 3 4 5 6 7
a 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
20 30 6 24 23 27 28 15 21 17 22 NR 19 33
ia 21 28 13 NR 40 16 21 19 15 41
20.6 15.0 11.5 7.7 19.3 11.6 11.5 15.0 11.8 13.5 20.8 17.1 15.4 11.0 24.7 16.5 15.0 15.0 23.0 12.4
NR NR 15.0 23.0 10.2
145 165 130 22 1 1a9 1a6 142 189 86 150 94 169 49 132 1a5 43 64 98 101 a4 113 35 162 126 156
67 115 53 117 90 120 79 1oa 86 107 60 a1 58 a9 a1 29 48 72 66 45 90 60 101 77
a8
113 92 104 103 100 107 a9 101 107 87 1oa 89 54 60 96 106 92 63 69 45 95 40 a4 103 80
mls = meters per second; ms, = milliseconds; % pred = percent predicted, NR = no response. Normal median MCV > 47 mls, phrenic latency < 9.2 ms.
subjects, with velocities ranging from 10 to 32 m/s (normal >40 m/s). Tibia1 nerve responses were obtainable in 9 subjects. Velocities ranged from 9 to 32 m/s (normal >40 mh). A tibia1 nerve response was present in every subject with a recordable peroneal nerve response. Using the guidelines of D y ~ kall , ~subjects met the electrodiagnostic criteria for HMSN I. Relationship Between Phrenic Latency and Peripheral Motor Conduction. T o determine if the ex-
tent of peripheral conduction slowing corresponded to prolongation of the phrenic latency, we correlated the phrenic motor response with rnedian motor conduction velocity. No relationship existed between these 2 variables (r = 0.36, P > 0.1). Relationship Between Phrenic Latency and Pulmonary Function Variables. In a similar fashion, we
determined the relationship between phrenic latency slowing and MIP, MEP, and FVC. No signif-
Phrenic Nerve and Pulmonary Function in HMSN I
icant correlation existed between phrenic latency and MIP ( r = -0.08, P > O . l ) , MEP (r = -0.11, P > O . l ) , or FVC ( r = -0.28, P > 0.1). DISCUSSION
Our findings indicate that the phrenic nerve is involved in HMSN I. However, electrical evidence of phrenic nerve dysfunction did not correlate with common indices of pulmonary function (FVC, MIP, MEP), clinical signs and symptoms of respiratory insufficiency, or peripheral nerve motor conduction velocity. T h e data indicate that prolongation of phrenic nerve latency does not necessarily imply clinical evidence of pulmonary dysfunction. T h e lack of correlation between FVC, MIP, MEP and phrenic nerve latency may be due to an insensitivity of these pulmonary function tests. In previous case reports of respiratory failure in HMSN I, dia hra matic weakness was the presumed cause. '03''"A more sensitive measure of diaphragmatic function, such as transdiaphragmatic pressure measurement, l 3 may identify abnormalities not found on routine tests and yield a stronger association. Interestingly, MEP values were abnormal in a much higher percentage of patients (76%) than were MIP values (32%). This observation has been noted in previous studies of HMSN I."," In addition, all patients with reduced FVC or MIP had a reduced MEP. While MIP is primarily generated by the diaphragm, MEP reflects abdominal and external intercostal muscle strength. This suggests that the expiratory musculature is at least as affected, if not more so, than the inspiratory musculature in HMSN I. However, since expiration is primarily a passive action, if the inspiratory muscles are adequate, a reduced MEP is seldom a cause of respiratory failure unless complications arise from retained secretions secondary to an ineffective cough.3 Clinical observation of weakness bears little relationship to peripheral motor conduction velocit^.^ Thus, it is not surprising that phrenic nerve latency and MIP values were not related. Assessment of axonal loss is not possible with phrenic nerve stimulation due to the wide variation in the amplitude of the evoked motor response, even in Lack of correlation between median and phrenic nerve function may be due to differential involvement of distal and proximal motor nerves. Although this disorder is known to cause relatively uniform slowing of motor conduction in
8
MUSCLE & NERVE
April 1992
461
distal nerve^,^-^ it is not known if this holds for proximal nerves as well. Although our study demonstrates that the phrenic nerve is involved in HMSN I, phrenic nerve latency does not have a significant relationship to routine pulmonary function testing, peripheral nerve function, or clinical evaluation. It
would be useful to study more symptomatic HMSN I patients using sensitive, quantitative measures of diaphragmatic function to better elucidate the causes of respiratory dysfunction. In addition, longitudinal studies may delineate which variables, if any, can best serve as predictors of respiratory compromise and failure.
REFERENCES 1. Black LF, Hyatt RE: Maximal respiratory pressures: normal values and relationship to age and sex. A m Rev Respir Dis 1969;99:696-702. 2. Chan CK, Mohsenin V, Loke J, Virgulto J , Sipski ML, Ferranti R: Diaphragmatic dysfunction in siblings with hereditary motor and sensory neuropathy (Charcot- MarieTooth disease). Chest 1987;91:567-570. 3. Clausen JL: Maximal inspiratory and expiratory pressure, in Clausen JL (ed): Pulmonary Function Testing Guidelines and Controversies. New York, Academic Press, 1982, p p 187- 191. 4. Davis JN: Phrenic nerve conduction in man. J Neurol Neurosurg Psychiatry 1967;30:420. 5. Dyck PJ: Inherited neuronal degeneration and atrophy af-
fecting peripheral motor, sensory, and autonomic neurons, in Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds): Peripheral Neuropathy (2 ed). Philadelphia, WB Saunders, 1984, V O ~2, p p 1600- 1655. 6. Dyck PJ, Karnes JL, Lambert EH: Longitudinal study of neuropathic deficits and nerve conduction abnormalities in hereditary motor and sensory neuropathy type 1. Neurology 1989;39:1302- 1308. 7. Dyck PJ, Lambert EH: Lower motor and primary sensory
neuron diseases with peroneal muscular atrophy. I. Neurologic, genetic, and electrophysiologic findings in hereditary polyneuropathies. Arch Neurol 1968; 18:603- 6 19. 8. Dyer EL, Callahan AS: Charcot- Marie-Tooth disease and respiratory failure (letter). Chest 1988;93:221. 9. Eichacker PQ, Spiro A, Sherman M, Lazar E, Reichel J , Dodick F: Respiratory muscle dysfunction in hereditary motor sensory neuropathy, type I . Arch Intern Med
10. Gilchrist D, Chan CK, Deck JH: Phrenic involvement in Charcot- Marie-Tooth disease: a pathologic documentation. Chest 1989;96:1197-1199. 11. Hardie R, Harding AE, Hirsch N, Gelder C, Macrae AD, Thomas PK: Diaphragmatic weakness in hereditary motor and sensory neuropathy. J Neurol Neurosurg Psychiatry 1990;53:348-350. 12. Harding AE, Thomas PK: T h e clinical features of heredi-
tary motor and sensory neuropathy types I and 11. Brain 1980; 1031259- 280. 13. Laporta D, Grassino A: Assessment of transdiaphragmatic pressure in humans. J Appl Physiol 1985;58: 1469- 1476. 14. Laroche CM, Carroll N, Moxham J, Stanley NN, Evans RJ,
Green M: Diaphragm weakness in Charcot-Marie-Tooth disease. Thorax 1988;43:478- 479. 15. Ma DM, Liveson JA: Cervical plexus, in Ma DM, Liveson JA (eds): Nerve Conduction Handbook. Philadelphia, FA Davis, 1983, p p 41-44. 16. Morris AH, Kanner RE, Crapo RO, Gardner RM: Table of reference values for lung function in adult women and men, in Morris AH, Kanner RE, Crapo RO, Gardner RM (eds): Clinical Pulmonary Function Testing: A Manual of Uniform Laboratory Procedure (2 ed). Salt Lake City, U'T, Intermountain Thoracic Society, 1984, pp 103- 151. 17. Nathanson BN, Ding-Guo Y, Chan K: Respiratory weakness in Charot- Marie-Tooth disease. Arch Intern Med 1989; 149: 1389- 1391. 18. Varlotta GP, Feinberg JH, Yang GW, Wilner M, Alba AS:
Pulmonary rehabilitation, including artificial ventilation in hereditary motor sensory neuropathy, type I. Arch Phys Med Rehabil 1990;71:760.
1988; 148: 1739- 1740.
462
Phrenic Nerve and Pulmonary Function in HMSN I
MUSCLE & NERVE
ADril 1992
EVALUATION OF PHRENIC NERVE AND PULMONARY FUNCTION IN HEREDITARY MOTOR AND SENSORY NEUROPATHY, TYPE I GREGORY T. CARTER, MD, DAVID D. KILMER, MD, H. WILLIAM BONEKAT, DO, JAMES S. LIEBERMAN, MD, and WILLIAM M. FOWLER, JR., MD
Hereditary motor and sensory neuropathy, type I (HMSN l), is a slowly progressive disease resulting in distal muscle weakness and atrophy, as well as impaired ~ e n s a t i o n . ~ ' ~Restrictive '" lung disease, common in many neuromuscular disorders, is not a predominant feature of HMSN I. Recently, however, there have been several case reports of From the Departments of Physical Medicine and Rehabilitation (Drs. Carter, Kilmer. Lieberman. and Fowler) and Internal Medicine, Division of Pulmonary Medicine (Dr Bonekat), University of California, Davis, California. Acknowledgments. Supported by Research and Training Center Grant H133880016-03and Research Training Grant G0087C2005 from the National Institute on Disability and Rehabilitation Research (NIDRR), United States Department of Education. The authors thank Merete Glick, RPT for her technical assistance with data collection in this study. Address reprint requests Gregory T. Carter, MD, University of California, Davis, Medical Center, Department of Physical Medicine and Rehabilitation, 4301 "X" Street, Room 2030, Sacramento, CA 95817. Accepted for publication April 24, 1991 CCC 0148-639X1921040459-04$04 00 0 1992 John Wiley & Sons, Inc.
Phrenic Nerve and Pulmonary Function in HMSN I
respiratory dysfunction in HMSN I, with some patients requiring mechanical ventilatory support.228718 Diminished maximal static airway pressures have also been reported, presumably due to impaired dia hra matic and chest-wall muscle function."*14" It ghas been assumed that the phrenic nerve may be involved and could account for the respiratory One report noted microscopic neuropathic changes in the phrenic nerve that were identical at autopsy to the histologic changes in the peripheral nerves in a 69year-old woman with HMSN I who died of respiratory failure. l o Despite these case reports, no investigation has prospectively determined the extent of phrenic nerve involvement and respiratory dysfunction in a cross-section of patients with HMSN I. Our study was designed to assess phrenic nerve function in patients with HMSN I, and determine its relationship to (1) vital capacity and maximal static respiratory pressures; (2) clinical signs and symp-
MUSCLE & NERVE
April 1992
459
toms of respiratory dysfunction; and (3) peripheral nerve function. MATERIALS AND METHODS
All 30 patients with HMSN I in the neuromuscular disease clinic at our institution were invited to participate in the study. Twenty-five agreed and signed a detailed consent form that outlined the research protocol as approved by the University Human Subjects Approval Committee. There were 12 female and 13 male subjects, with an average age of 39 years (range 11 to 65 years). Patients underwent an evaluation consisting of ( 1) pulmonary-focused history and physical examination, (2) pulmonary function tests (PFTs) consisting of forced vital capacity (FVC), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP); (3) bilateral phrenic nerve motor conduction studies; and (4) median, peroneal, and tibia1 nerve motor conduction studies. The history included questions related to shortness of breath with ambulation, at rest, and during sleep. Physical examination included auscultation of the heart and lungs and examination for thoracoabdominal paradoxical breathing in the supine position. FVC was measured using a Cybermedic Moose spirometer (Cybermedic Inc., Louisville, CO). MIP and MEP were measured near residual volume (RV) and total lung capacity (TLC) respectively, according to the technique described by Black and Hyatt.' A Boehringer direct reading dial gauge force meter (Boehringer Laboratories, Inc., Wynnewood, PA) was used for these measurements. Three technically satisfactory measurements were obtained, and the maximum reading recorded. Phrenic nerve conduction studies were performed using the technique described by Davis.4 Peripheral nerve conduction studies were performed in the standard fashion described by Ma and Liveson.I5 All phrenic and peripheral nerve conduction data was recorded, analyzed, and printed using a Teca Mystro EMG unit ('Teca Corp., Pleasantville, NY). Normal age- and sex-matched predicted values for FVC were obtained from the Intermountain Thoracic Society." FVC was defined as abnormal if less than 80% of the predicted value. MIP and MEP age- and sex-matched normal predicted values were obtained from Black and Hyatt.' Four subjects were under 20 years of age, and for this group we used the available MIP and MEP values for adults 20 years of age. Values for MIP and MEP were expressed as a percentage of the lower
460
Phrenic Nerve and Pulmonary Function in H M S N 1
limit of the normal predicted value range. Thus, any value 47 m/s) (Table 1). Both subjects without median nerve responses had marked thenar wasting and no voluntary movement of the thumb. Peroneal nerve responses were obtainable in 5 Peripheral
M U S C L E & NERVE
April 1992
Table 1. Electrophysiologic and pulmonary function data in the 25 subiects. Median Right MCV phrenic MIP MEP FVC Patient (misec) latency (ms) (% pred) (% pred) (% pred) 1 2 3 4 5 6 7
a 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
20 30 6 24 23 27 28 15 21 17 22 NR 19 33
ia 21 28 13 NR 40 16 21 19 15 41
20.6 15.0 11.5 7.7 19.3 11.6 11.5 15.0 11.8 13.5 20.8 17.1 15.4 11.0 24.7 16.5 15.0 15.0 23.0 12.4
NR NR 15.0 23.0 10.2
145 165 130 22 1 1a9 1a6 142 189 86 150 94 169 49 132 1a5 43 64 98 101 a4 113 35 162 126 156
67 115 53 117 90 120 79 1oa 86 107 60 a1 58 a9 a1 29 48 72 66 45 90 60 101 77
a8
113 92 104 103 100 107 a9 101 107 87 1oa 89 54 60 96 106 92 63 69 45 95 40 a4 103 80
mls = meters per second; ms, = milliseconds; % pred = percent predicted, NR = no response. Normal median MCV > 47 mls, phrenic latency < 9.2 ms.
subjects, with velocities ranging from 10 to 32 m/s (normal >40 m/s). Tibia1 nerve responses were obtainable in 9 subjects. Velocities ranged from 9 to 32 m/s (normal >40 mh). A tibia1 nerve response was present in every subject with a recordable peroneal nerve response. Using the guidelines of D y ~ kall , ~subjects met the electrodiagnostic criteria for HMSN I. Relationship Between Phrenic Latency and Peripheral Motor Conduction. T o determine if the ex-
tent of peripheral conduction slowing corresponded to prolongation of the phrenic latency, we correlated the phrenic motor response with rnedian motor conduction velocity. No relationship existed between these 2 variables (r = 0.36, P > 0.1). Relationship Between Phrenic Latency and Pulmonary Function Variables. In a similar fashion, we
determined the relationship between phrenic latency slowing and MIP, MEP, and FVC. No signif-
Phrenic Nerve and Pulmonary Function in HMSN I
icant correlation existed between phrenic latency and MIP ( r = -0.08, P > O . l ) , MEP (r = -0.11, P > O . l ) , or FVC ( r = -0.28, P > 0.1). DISCUSSION
Our findings indicate that the phrenic nerve is involved in HMSN I. However, electrical evidence of phrenic nerve dysfunction did not correlate with common indices of pulmonary function (FVC, MIP, MEP), clinical signs and symptoms of respiratory insufficiency, or peripheral nerve motor conduction velocity. T h e data indicate that prolongation of phrenic nerve latency does not necessarily imply clinical evidence of pulmonary dysfunction. T h e lack of correlation between FVC, MIP, MEP and phrenic nerve latency may be due to an insensitivity of these pulmonary function tests. In previous case reports of respiratory failure in HMSN I, dia hra matic weakness was the presumed cause. '03''"A more sensitive measure of diaphragmatic function, such as transdiaphragmatic pressure measurement, l 3 may identify abnormalities not found on routine tests and yield a stronger association. Interestingly, MEP values were abnormal in a much higher percentage of patients (76%) than were MIP values (32%). This observation has been noted in previous studies of HMSN I."," In addition, all patients with reduced FVC or MIP had a reduced MEP. While MIP is primarily generated by the diaphragm, MEP reflects abdominal and external intercostal muscle strength. This suggests that the expiratory musculature is at least as affected, if not more so, than the inspiratory musculature in HMSN I. However, since expiration is primarily a passive action, if the inspiratory muscles are adequate, a reduced MEP is seldom a cause of respiratory failure unless complications arise from retained secretions secondary to an ineffective cough.3 Clinical observation of weakness bears little relationship to peripheral motor conduction velocit^.^ Thus, it is not surprising that phrenic nerve latency and MIP values were not related. Assessment of axonal loss is not possible with phrenic nerve stimulation due to the wide variation in the amplitude of the evoked motor response, even in Lack of correlation between median and phrenic nerve function may be due to differential involvement of distal and proximal motor nerves. Although this disorder is known to cause relatively uniform slowing of motor conduction in
8
MUSCLE & NERVE
April 1992
461
distal nerve^,^-^ it is not known if this holds for proximal nerves as well. Although our study demonstrates that the phrenic nerve is involved in HMSN I, phrenic nerve latency does not have a significant relationship to routine pulmonary function testing, peripheral nerve function, or clinical evaluation. It
would be useful to study more symptomatic HMSN I patients using sensitive, quantitative measures of diaphragmatic function to better elucidate the causes of respiratory dysfunction. In addition, longitudinal studies may delineate which variables, if any, can best serve as predictors of respiratory compromise and failure.
REFERENCES 1. Black LF, Hyatt RE: Maximal respiratory pressures: normal values and relationship to age and sex. A m Rev Respir Dis 1969;99:696-702. 2. Chan CK, Mohsenin V, Loke J, Virgulto J , Sipski ML, Ferranti R: Diaphragmatic dysfunction in siblings with hereditary motor and sensory neuropathy (Charcot- MarieTooth disease). Chest 1987;91:567-570. 3. Clausen JL: Maximal inspiratory and expiratory pressure, in Clausen JL (ed): Pulmonary Function Testing Guidelines and Controversies. New York, Academic Press, 1982, p p 187- 191. 4. Davis JN: Phrenic nerve conduction in man. J Neurol Neurosurg Psychiatry 1967;30:420. 5. Dyck PJ: Inherited neuronal degeneration and atrophy af-
fecting peripheral motor, sensory, and autonomic neurons, in Dyck PJ, Thomas PK, Lambert EH, Bunge R (eds): Peripheral Neuropathy (2 ed). Philadelphia, WB Saunders, 1984, V O ~2, p p 1600- 1655. 6. Dyck PJ, Karnes JL, Lambert EH: Longitudinal study of neuropathic deficits and nerve conduction abnormalities in hereditary motor and sensory neuropathy type 1. Neurology 1989;39:1302- 1308. 7. Dyck PJ, Lambert EH: Lower motor and primary sensory
neuron diseases with peroneal muscular atrophy. I. Neurologic, genetic, and electrophysiologic findings in hereditary polyneuropathies. Arch Neurol 1968; 18:603- 6 19. 8. Dyer EL, Callahan AS: Charcot- Marie-Tooth disease and respiratory failure (letter). Chest 1988;93:221. 9. Eichacker PQ, Spiro A, Sherman M, Lazar E, Reichel J , Dodick F: Respiratory muscle dysfunction in hereditary motor sensory neuropathy, type I . Arch Intern Med
10. Gilchrist D, Chan CK, Deck JH: Phrenic involvement in Charcot- Marie-Tooth disease: a pathologic documentation. Chest 1989;96:1197-1199. 11. Hardie R, Harding AE, Hirsch N, Gelder C, Macrae AD, Thomas PK: Diaphragmatic weakness in hereditary motor and sensory neuropathy. J Neurol Neurosurg Psychiatry 1990;53:348-350. 12. Harding AE, Thomas PK: T h e clinical features of heredi-
tary motor and sensory neuropathy types I and 11. Brain 1980; 1031259- 280. 13. Laporta D, Grassino A: Assessment of transdiaphragmatic pressure in humans. J Appl Physiol 1985;58: 1469- 1476. 14. Laroche CM, Carroll N, Moxham J, Stanley NN, Evans RJ,
Green M: Diaphragm weakness in Charcot-Marie-Tooth disease. Thorax 1988;43:478- 479. 15. Ma DM, Liveson JA: Cervical plexus, in Ma DM, Liveson JA (eds): Nerve Conduction Handbook. Philadelphia, FA Davis, 1983, p p 41-44. 16. Morris AH, Kanner RE, Crapo RO, Gardner RM: Table of reference values for lung function in adult women and men, in Morris AH, Kanner RE, Crapo RO, Gardner RM (eds): Clinical Pulmonary Function Testing: A Manual of Uniform Laboratory Procedure (2 ed). Salt Lake City, U'T, Intermountain Thoracic Society, 1984, pp 103- 151. 17. Nathanson BN, Ding-Guo Y, Chan K: Respiratory weakness in Charot- Marie-Tooth disease. Arch Intern Med 1989; 149: 1389- 1391. 18. Varlotta GP, Feinberg JH, Yang GW, Wilner M, Alba AS:
Pulmonary rehabilitation, including artificial ventilation in hereditary motor sensory neuropathy, type I. Arch Phys Med Rehabil 1990;71:760.
1988; 148: 1739- 1740.
462
Phrenic Nerve and Pulmonary Function in HMSN I
MUSCLE & NERVE
ADril 1992
