DOI 10.1378/chest.88.2.211 1985;88;211-214Chest

 S S Moorthy, O N Markand, Y Mahomed and J W Brown mechanical ventilation.severe respiratory insufficiency requiring Electrophysiologic evaluation of phrenic nerves in

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CHEST I 88 I 2 I AUGUST, 1985 211

Electrophysiologic Evaluation of PhrenicNerves in Severe Respiratory InsufficiencyRequiring Mechanical Ventilation*S. S. Moorthy, M.D. , F.C.C.P;t Omkar N. Markand, M.D.4

Yousuf Mahomed, M. D. , F. C. C. P ;� andJohn W Brown, M. D. , F. C. C. P §

Diaphragmatic paralysis in patients with respiratory insuf-

ficiency compounds the problems in the management. Inthe presence oflower lobe atelectasis, pleural effusion, or apatient’s poor respiratory effort, fluoroscopic examination is

often not a reliable way to diagnose diaphragmatic paral-ysis. We observed that transcutaneous phrenic nerve slim-ulation in the neck and recording the diaphragmatic poten-

tials from electrodes placed on the lower part ofthe chest is

C ontraction of the diaphragm produces 60 percent

of the tidal volume in normal supine individuals

at rest.’ Evaluation ofdiaphragmatic function is, there-

fore, important in patients with respiratory insuffI-

ciency. Paralysis ofthe diaphragm is usually diagnosed

by an elevated diaphragm on the chest x-ray film and

paradoxic movement of the diaphragm observed with

inspiration during fluoroscopic examination. The radi-

ologic diagnosis is difficult in the presence of lower

lobar atelectasis, pleural effusion, or with poor respira-

tory effort of the patient. It may also be difficult

sometimes to transport a critically ill patient to the

radiology unit for fluoroscopic study. We observed that

electrophysiologic studies of phrenic nerves provide a

useful technique for diagnosing diaphragmatic dys-

function in critically ill patients.

MATERIALS AND METHODS

Because of our interest in the electrophysiologic studies of the

diaphragm, we were asked to evaluate 21 patients who had respira-

tory insufficiency of recent onset requiring mechanical ventilation.

Fourteen patients developed respiratory dysfunction in the

postoperative period following a surgical procedure, usually a

thoracotomy. An elevated diaphragm on the chest x-ray film,

persistent lower lobe atelectasis, inability to wean from ventilatory

support, and suspicion of phrenic nerve damage during surgery

prompted the anesthesiologist and the surgeon to seek a study of

phrenic nerve conduction in these patients. One patient had

traumatic quadriplegia due to a high cervical cord injury. The

remaining six patients had decreased respiratory effort on the basis of

severe polyradiculoneuropathy of the Guillain-Barr#{233} type (five

patients) or myasthenia gravis (one patient).

*From Indiana University School of Medicine, Indianapolis.

tDepartment of Anesthesia.Wepartment of Neurology.§Section of Cardiovascular Surgery.Manuscript received November 29; revision accepted January 17.Reprint requests: Mr James May, Department ofNeurology, EM125,545 Barnhill Drive, Indianapolis 46223

a simple, reliable, and noninvasive technique to diagnose

diaphragmatic dysfunction at the bedside in critically illpatients. In 14 postoperative patients and one with cervicalspinal cord injury with respiratory failure, we found tenpatients who showed phrenic nerve dysfunction. Besidesdiagnostic utility, the electrophysiologic evaluation ofphrenic-diaphragmatic function provides critical informa-tion needed for therapy.

With the patient lying supine and the head in midline, we

stimulated the right and left phrenic nerves transcutaneously behind

the sternocleidomastoid muscle at the level of the upper border of

thyroid cartilage by conventional bipolar stimulating electrodes

(TECA Corp) The cathode was placed close to the clavicle. A disk

electrode over the manubrium sterni acted as a ground electrode.

Suprathreshold square-wave pulses ofO.1 to 0.5 msec at a rate of Jlsec

were delivered. The frequency response of the amplifier was set at

1.6 Hz to 32 kHz (- 3 dB). By adjusting the position of the

stimulating electrodes, the phrenic nerve could be selectively

stimulated with minimal brachial plexus stimulation.

The diaphragmatic evoked potentials were recorded from two

surface disk electrodes 8 mm in diameter; one was placed at the

seventh intercostal space (7ICS) close to the costochondral junction

and the other over the xiphoid process (XP). The electrodes were

held to the skin by electrolyte paste (Grass) and further secured with

cloth tape (Scotch). The ipsilateral 7ICS electrode was connected to

the input terminal 2 (red terminal) and the XP electrode to the input

terminal 1 (black terminal) of the electromyograph (TECA-TE42).

Using this XP-7ICS derivation, positivity at the 7ICS electrode

yielded an upgoing waveform. The details of the technique are

reported by Markand et al.’

The upper limits of the phrenic nerve conduction time in normal

adults is less than 9.75 msec (mean ± 2.5 SD). The amplitude of the

diaphragmatic potential is greater than 0.4 mV. In children the

latency is shorter (4.3 to 4.9 msec) and is dependent on the length of

the chest. The amplitude ratio of left and right responses are

normally over 0.6 and less than 1.6.

RESULTS

All patients with polyradiculoneuropathy (Guillain-

Barr#{233}syndrome) had abnormal electrophysiologic

studies of the diaphragm, the details of which have

been previously described.2 The amplitude of the

diaphragmatic response was significantly decreased

bilaterally. In two, the phrenic nerves were totally

inexcitable during the height ofthe illness. When the

diaphragmatic responses were elicitable, the latencies

were usually prolonged. Two patients had serial studies

starting less than a week from the onset of Guillain-

 © 1985 American College of Chest Physicians by guest on July 11, 2011chestjournal.chestpubs.orgDownloaded from

Phrenic Nerve Studyt

Patient, Right LeftSex, Precipitating Cause �-�------� �-�---�

Age (yr) of Respiratory Failure* Radiologic Fmdingst Amp Let Amp Let

1, M, 61 CABG LLL atel; L p1 eff; � L hemidiaphragm 0.28 9.0 NR ...

2, M, 3 mo Repair of coarctation of aorta R lung inf/atel; LUL inf/atel; � L

hemidiaphragm

0.90 4. 1 NR ...

3, M, 73 CABG 5 yr ago; recent cholecystectomy L hemidiaphragm NR . . . NR ...4, F, 9 mo Repair ofcongenital MI RUL atel/inf; bil perthilar inf;

paradoxical movement of R

diaphragm (?)

0.80 4.5 1.00 4.0

5, M, 37 Ca of testes; thoracotomy for metastases R hemidiaphragm NR . . . 0.38 ...6, F, 4 Repair of artrioventricular canal RUL atellinf; bil LL inf 0.55 4.3 0.40 4.4

7, F, 4 Repair of congenital VSD R p1 eff; bil pulmonary inf; t L

hemidiaphragm

0.55 4.9 0.60 4.9

8, F, 71 CABG LLL atel; L p1 eff 0. 18 8.5 NR ...9, M, 62 CABG Bibasilar atellinf; bil p1 eff 0.45 9.5 0.65 9.5

10, F, 54 Right upper lobeetomy for Ca oflung RUL inf; R eff; L inf; fluoroparadoxical

movement R

NR . . . 1.30 8.0

11, M, 62 Colectomy for Ca and resection of

metastases in left lung

LLL inf/atel; L p1 eff 1. 10 8.5 NR ...

12, M, 3 mo Repair oftruncus arteriosus LLL atel/infand p1 eff 1.25 6.2 NR ...13, M, 12 Crouwn�s disease LLL atel/inf; RUL inf 0.70 6.0 0.25 10.2

14, F, 78 AV and MV replacement LLL inflate!; bil p1 eff 0.50 8.2 NR ...15, M, 7 Fracture ofcervical spine LUL atellinf; RUL atel 0. 10 6.5 NR ...

mitral valve.

tLLL, Left lower lobe; atel, atelectasis; L, left; p1, pleural; eff, effusion;

upper lobe; bil, bilateral; and LL, lower lobe.

tAmp, Amplitude; Let, latency; and NR, no response.

*CABG, Coronary arterial bypass graft; MI, mitral incompetence; Ca, carcinoma; VSD, ventricular septal defect; AV, aortic valve; and MV,

t , elevated; R, right; inf infiltrate; LUL, left upper lobe; RUL, right

Table 1-Phrenic Nerve Conduction in 14 Postoperative and One Post-traumatic Patient with Respiratory Insufficiency

212 Phrenic Nerves in Severe Respiratory Insufficiency (Moorthy et a!)

Barr#{233}syndrome. In both, the diaphragmatic potential

regained normal amplitude over several weeks parallel

with the improvement in the patient’s ventilation; how-

ever, the latencies of the diaphragmatic responses

remained prolonged. The only patient with my-

asthenia gravis in this series had his diaphragmatic

responses decreased in amplitude bilaterally, but the

latencies were normal.

The data on 14 patients who developed respiratory

insufficiency after a surgical procedure (usually cardiac

or thoracic) are shown in Table 1. Four patients (cases 4,

6, 7, and 9) had normal phrenic studies; their respira-

tory difficulties were apparently due to atelectasis or

infiltrates bilaterally (Fig 1). One patient (case 3) had no

recordable diaphragmatic potential on stimulation of

either phrenic nerve. He required mechanical ventila-

tion until his death three months later. Unilateral

diaphragmatic paresis or paralysis was demonstrated in

six patients (four with inexcitable left phrenic nerve,

one with inexcitable right phrenic nerve, and one with

lower amplitude response with left phrenic stimula-

tion), with the diaphragmatic responses being totally

normal on the other side (Fig 2). Three patients had

evidence of bilateral but asymmetric involvement. In

one, the right phrenic nerve was inexcitable, but the

left-sided response was present at a reduced ampli-

tude. The remaining two had paralysis of the left

hemidiaphragm, with paresis of the right side.

One patient with traumatic quadriplegia due to high

cervical cord injury showed evidence of total paralysis

on the left with severe paresis of the right hemi-

diaphragm. The diaphragmatic-evoked response on

stimulation of the right phrenic nerve was 0.1 mV,

which was believed to be unsatisfactory for dia-

phragmatic pacing.

DIsCuSsIoN

In patients with severe respiratory insufficiency,

diaphragmatic paralysis may constitute an important

contributing factor to respiratory failure and difficulty

in weaning from mechanical ventilatory support. Dia-

phragmatic contraction contributes 60 percent of the

normal minute’ ventilation, and its paralysis is associ-

ated with reduction ofvital capacity, maximum volun-

tary ventilation, forced expiratory volume in one

second, and functional residual capacity, and an in-

creased ventilation-perfusion mismatch.� In our study

of2l patients with respiratory failure requiring assisted

ventilation, 17 showed electrophysiologic evidence of

unilateral or bilateral diaphragmatic palsy.

Detection of phrenic nerve paralysis in the past has

been largely by radiologic investigations. An elevated

 © 1985 American College of Chest Physicians by guest on July 11, 2011chestjournal.chestpubs.orgDownloaded from

�J 500

6 msec

FIGURE 1. Normal and symmetric diaphragmatic potentials evoked by right and left phrenic nerve

stimulation in four-year-old child four days after repair of congenital heart disease (case 7).

RT. PHRENIC STIM. LT. PHRENIC SlIM.

CHEST I 88 I 2 I AUGUST, 1985 213

F � � :� � / I I / / / I I / / I / :r i : : � ; ; � :�

hemidiaphragm on the chest x-ray film with atelectasis

or infiltrates of the lower lobe on the affected side

suggests unilateral phrenic paralysis . Fluoroscopic

examination ofthe chest demonstrating reduced excur-

sion of the hemidiaphragm and paradoxic motion is

considered diagnostic ofdiaphragmatic paralysis.6 Un-

fortunately, fluoroscopic study may be delayed due to

the difficulties in transportation of the critically ill

patient to the radiology unit. Furthermore, the radi-

ologic findings are not pathognomonic ofphrenic palsy.

Similar findings may also occur with eventration of the

diaphragm, local pulmonary conditions (infiltrates,

atelectasis, effusion, etc), and subphrenic pathologic

abnormalities.7 The radiologic diagnosis of dia-

phragmatic weakness is, therefore, difficult and often

impossible in the presence of coexisting pulmonary

pathologic abnormalities. Such a complicating situa-

tion is commonly encountered in patients with respira-

tory failure in the postoperative period following a

surgical procedure on the chest (eg, coronary arterial

bypass graft). These patients not only show severe

pulmonary infiltrates or atelectasis, but are also at risk

RI. PHRENIC STIM.

to develop phrenic nerve damage secondary to surgical

trauma, traction, or hypothermia.8 In two of our

patients, radiologic studies raised the suspicion of

diaphragmatic paralysis, but electrophysiologic stud-

ies indicated normal phrenic-diaphragmatic function.

Although electrophysiologic techniques for study-

ing phrenic nerves and diaphragmatic function have

been available since the original work ofDavis9 in 1967,

they have not been widely employed in critically ill

patients due to lack ofa standardized, noninvasive, and

reliable technique of phrenic nerve stimulation and

recording. The availability of portable electrophysio-

logic instruments and experience with transcutaneous

phrenic stimulation and recording of diaphragmatic

potential make this technique feasible and reliable and

simple to perform in the intensive care unit. We found

that stimulation of the phrenic nerve by surface elec-

trodes was effective and without discomfort. The

invasive technique of stimulation through a needle

electrode placed close to the phrenic nerve as pro-

posed by some’#{176}is not necessary.

Both latency and amplitude of the diaphragmatic

LI. PHRENIC SlIM.

_j 500 �sv

10

FIGURE 2. Absence ofdiaphragmatic potential on left phrenic stimulation in 78-year-old patient two weeks

following aortic and mitral valvular repairs. Diaphragmatic response is normal to right phrenic stimulation

(case 14).

 © 1985 American College of Chest Physicians by guest on July 11, 2011chestjournal.chestpubs.orgDownloaded from

214 Phrenic Nerves in Severe Respiratory Insufficiency (Moorthy et a!)

potential are important for the diagnosis of dia-

phragmatic dysfunction. Prolongation of the latency

provides unequivocal evidence of slowed conduction

along the phrenic nerve, a common finding in poly-

radiculoneuropathies and in some patients with in-

traoperative injuries ofthe phrenic nerves. The ampli-

tude ofthe diaphragmatic potential, on the other hand,

provides a measure of the number of diaphragmatic

muscle fibers activated by phrenic nerve stimulation.

Abnormalities of amplitude may be the sole evidence

of diaphragmatic paresis in patients who develop

respiratory insufficiency on the basis of myasthenia

gravis and motor neuron disease and also in patients

with intraoperative phrenic nerve injuries in the

thorax.

Diagnosis of phrenic palsy is not only helpful in

understanding the pathophysiology, but also in plan-

ning therapy in patients with respiratory insufficiency.

Patients with bilateral phrenic dysfunction are likely to

need continued positive-pressure ventilation or con-

tinuous positive airway pressure for their respiratory

support. “-‘� Unilateral diaphragmatic paralysis causes

respiratory insufficiency only if there are other com-

plicating factors such as intrinsic pulmonary or pleural

pathologic abnormalities. Correction of these compli-

cations is, therefore, crucial in restoring normal yen-

tilation. In patients with diaphragmatic paralysis,

plication of diaphragm is useful.’3 In patients with

traumatic quadriplegia with respiratory insufficiency

due to cervical cord injury, phrenic studies are crucial

in deciding if diaphragmatic pacing (electrophrenic

respiration) would have a place in the management of

the ‘#{176}If phrenic nerve stimulation elicits more

or less normal diaphragmatic responses, it can be

assumed that the anterior horn cells and their axons

innervating the diaphragm are intact. Diaphragmatic

pacing would be indicated in such patients. On the

other hand, if phrenic stimulation produces no re-

sponse or a low-amplitude response, diaphragmatic

pacing would not be beneficial, as was the case in our

patient with high cervical cord injury with quadri-

plegia.

We conclude that transcutaneous phrenic stimula-

tion with surface recording ofthe diaphragmatic poten-

tial is a noninvasive and reliable technique for diag-

nosis of diaphragmatic dysfunction. The test can be

performed easily at the bedside ofa critically ill patient

with pulmonary insufficiency. Electrophysiologic eval-

uation of phrenic nerves must be included in the

assessment of all patients who develop respiratory

insufficiency. When performed with customary radi-

ologic investigation, such evaluation provides useful

diagnostic and therapeutic information in such pa-

tients.

REFERENCES

1 Wang CS, Josenhans WI Contribution ofdiaphragmaticlabdom-

inal displacement to ventilation in supine man. J Appl Physiol

1971; 31:576-80

2 Markand ON, Kincaid JC, Pourmand BA, Moorthy 55, King

RD, Mohamed Y, et al. Electrophysiologic evaluation of dia-

phragm by transcutaneous phrenic nerve stimulation. Neurology

1984; 34:604-14

3 McCredie M, Lovejoy FW Jr. Kaltreider NL. Pulmonary func-

tion in diaphragmatic paralysis. Thorax 1962; 17:213-17

4 Arborelius M Jr, Lilja B, Senykj. Regional and total lung function

studies in patients with hemidiaphragmatic paralysis. Respira-

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5 Easton PA, Fleetham JA, DeLaRocha A, Anthonisen NR. Respi-

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11 Robotham JL, Chipps BE, Shermeta DW. Continuous positive

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12 Robotham JL. A physiological approach to hemidiaphragm

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13 Haller BJ Jr. Pickard LR, Tepas JJ, Rogers MC, Robotham JL,

Shorter N, et al. Management of diaphragmatic paralysis in

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ative plication. J Pediatr Surg 1979; 14:779-85

14 Sivak ED, Razavi M, Groves LK, Loop FD. Long-term manage-

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DOI 10.1378/chest.88.2.211 1985;88; 211-214Chest

S S Moorthy, O N Markand, Y Mahomed and J W Browninsufficiency requiring mechanical ventilation.

Electrophysiologic evaluation of phrenic nerves in severe respiratory

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