Repetitive Peripheral Inductive Stimulation In

Comprehensive Physiotherapeutic Approach

- A Case Study
Žarković D., Department of Anatomy and Biomechanics,
Faculty of Sport and Physical Education, Charles University Prague
Presented at the XXIII. Meeting of Society of Rehabilitation and Physical Medicine,
May, 2016, Luhačovice, Czech republic

Abstract
Background:
Repetitive peripheral inductive stimulation (rPIS) uses high intensity electromagnetic field, which interacts
with the human body and causes depolarization of the neuromuscular tissue. This can be used to achieve
different therapeutic effects, such as to strengthen weakened muscles or relieve the pain.

Aim:
Aim of the case study was to evaluate the efficacy of the rPIS in a 4-week protocol of comprehensive
rehabilitation, which consisted of strengthening of breathing muscles and treatment of musculoskeletal
disorders in central motor impairment.

Methods:
To compare patient´s condition ´before and after´, spirometry and kinesiology evaluation were performed. In
comprehensive rehabilitation protocol, the BTL-6000 Super Inductive System was incorporated.

Results:
After 4-week intensive rehabilitation protocol, significant improvement of spirometric parameters as well as
amelioration of patient´s musculoskeletal system were observed.

Conclusion:
rPIS can be effectively integrated in comprehensive physiotherapy treatment and cover various therapeutic
effects.

Key words:
BTL-6000 Super Inductive System, spirometry, kinesiology, physiotherapy

Introduction
Comprehensive rehabilitation usually consists of physiotherapeutic methods as well as physical therapy. By combination
of different methods, we can tailor therapy to our patients needs and improve their quality of life. One of possibilities
certainly is a repetitive peripheral inductive stimulation (rPIS), which seems very promising from many aspects. rPIS
uses high intensity electromagnetic field, passing through neural tissue in which, electric current causing change in action
potential is induced. As the currents are carrying an electric signal to the muscle, muscle contraction is achieved. rPIS is a
method covering multiple therapeutic effects and can be indicated in treatment of various conditions of musculoskeletal
and neural system. According to specific therapeutic parameters, such as frequency and intensity of stimulation, you
can relieve pain, strengthen muscles or release joint blockage. In this paper, we propose how to integrate rPIS in a
comprehensive physiotherapeutic approach.
Materials and methods
Herein, we present a 29-year-old man, who was seriously Therapy consisted of 2 parts – preparatory and active phase.
injured in a car accident in early childhood. Due to the In both phases, the BTL-6000 Super Inductive System
accident, he has persistent postraumatic respiratory and (SIS) and a hand-held focused field applicator were used.
musculoskeletal disease even in adult age (see Picture Preparatory phase was important to optimize the condition
1). We integrated him into a 4-week comprehensive of soft tissues, relieve the pain, eliminate trigger points or
rehabilitation program. Patient was assessed by release joint blockage in the thoracic spine (see Picture 2).
spirometry to evaluate his ventilation parameters. Results For this purpose, BTL-6000 Super Inductive System and
of spirometry evaluation confirmed a combination of combination of manual techniques were used. This process
restrictive and obstructive respiratory disease. Due to facilitated further relearning of motor patterns such as
respiratory muscles weakness, values of ventilation optimal breathing pattern.
parameters, such as slow vital capacity (SVC); force vital
In the active phase, stimulation of breathing muscles with
capacity (FVC) or maximal voluntary volume (MVV)
BTL-6000 Super Inductive System was performed only on
were below the normal threshold.
the patient´s affected side. Consequently, active relearning
In the kinesiology evaluation, the right-sided hemiparesis
of the new breathing pattern was performed in various
was the most obvious clinical problem from many
postural positions (see Picture 3). Intensity of the therapy
aspects. On one hand, hemiparesis leads to discoordinated
with BTL-6000 Super Inductive System was set to above
and efficient breathing pattern. On the other hand, it leads
the sensitivity up to above the motor threshold.
to asymmetry of his shoulder and pelvic girdle resulting
into scoliosis. These evaluations were performed ´before
and after´ to compare his condition.
Subjectively, patient reports breathing difficulties,
especially during inspiration. He feels limitation even
more during physical activity (e.g. jogging). His
assymetric posture and efficient breathing pattern lead to
back pain, especially in thoracic and lumbar area, joint
blockages and discoordination of the trunk muscles.

Picture No. 2:
Thoracic spine mobilization with SIS

Picture No.1:
Patient affected by right-sided hemiparesis
Aim of therapy was to improve his ventilation parameters
as well as to eliminate problems in his musculoskeletal
system (numerous trigger points, joint blockages etc.),
which secondary affect breathing pattern.
Patient underwent a therapeutic protocol comprised of total
16 therapies. He attended therapies up to 4 times a week. Picture No.3:
Duration of one therapy was 60 minutes. Stimulation of the breathing muscles with SIS
Results
The 4-week protocol, in which BTL-6000 Super
Inductive System was incorporated, resulted into
improvement of spirometric parameters. Significant
improvements were observed mainly in SVC
parameters, which report the maximum volume of
air that can be exhaled slowly after slow maximum
inhalation. The most obvious was 45% amelioration
of the IRV parameter. In FVC, mostly PEF parameter
was improved about 12 %. This parameter is
reporting the speed of air flow. MVV profile was
improved about 9 %. This parameter reports the Table No.1:
maximum amount of air that can be inhaled and Results of spirometry evaluation
exhaled within one minute (see Table 1).
A positive effect of the therapy was also observed in
patient´s musculoskeletal system, where numerous
painful muscle spasms, leading to scoliotic trunk
assymetry were eliminated. This positively reflects
on the patient´s posture (Picture 4).
From patient´s subjective evaluation, he reported
effortless inspiration and more comfort during
physical activity, where he has almost no breathing
limitation.

Discussion
We consider that distinguishing the ´preparatory´
and ´active´ phase were determining for
the therapy results. Firstly, to optimize the
condition of patient´s thorax and soft tissues
and consequent muscle stimulation resulted into
the improvement of ventilation parameters. The
improvement of patient´s ventilation parameters
was mainly observed in SVC parameters. These
parameters and evaluation are performed slowly.
When slowly inhaling and exhaling, patient is
able to control his breathing pattern and breathe
more efficiently. In therapy, stimulation of both
inspiration and expiration muscles was performed Picture No.4:
as well as muscle coordination was trained. Patient´s uprighted posture after therapies

Conclusion
In this case study we suggest that rPIS can be effectively integrated in comprehensive physiotherapy treatment
and covers various therapeutic effects. Although, the study represents only one case, significant changes in
patient´s respiratory and musculoskeletal system were observed.

Functional Magnetic Stimulation
in Patients With Tetraplegia
Vernon WH. Lin, MD, PhD, Harwinder Singh, MD, Rajinder K. Chitkara, MD, Inder Perkash, MD
ABSTRACT. Lin VWH, Singh H, Chitkara RK, Perkash I.
Functional magnetic stimulation for restoring cough in patients
with tetraplegia. Arch Phys Med Rehabil 1998;79:517-522.
Objective: To evaluate the usefulness of functional magnetic
stimulation (FMS) as a noninvasive method for assisting cough
in patients with tetraplegia.
Design: A prospective before-after trial.
Setting: The functional magnetic stimulation laboratory of a
spinal cord injury (SCI) service.
Participants: Thirteen male SC1 patients, with injury levels
between C4 and C7.
Intervention: A commercially available magnetic stimulator
with a round magnetic coil (MC) was used. Expiratory muscle
activation was achieved by placing the MC along the lower
thoracic spine.
Main Outcome Measure: The planned major outcome
measures were the maximal expired pressure (MEP), expiratory
reserve volume (ERV), and forced expiratory flow rate (FEF)
by FMS compared with voluntary maximal efforts. Another
outcome was the optimal MC placement and stimulation
intensity that would result in highest expired pressure.
Results: The mean (iSEM) MEP, ERV, and FEF generated
by FMS were 66.40 t 6.69cmHz0, .77 2 .14L, and 5.28 F
.42L/sec, respectively. They were 118%, 169%, and 110% of
voluntary maximum efforts. MC placement at the TlO to Tll
spinous process and stimulation intensity at 80% produced the
highest MEP and FEE
Conclusion: FMS of the expiratory muscles produced signifi-
cant expired pressures, volumes, and flow rates when compared
with voluntary maximum efforts; therefore, FMS can be used as
an effective method to restore cough in tetraplegic patients.
0 1998 by the American Congress of Rehabilitation Medi-
cine and the American Academy of Physical Medicine and
Rehabilitation
P ULMONARY COMPLICATIONS are a major cause of
morbidity and mortality in patients with spinal cord injury
(SCI); their reported incidence has varied from 36% to 83%,
with respiratory insufficiency, pneumonia, and atelectasisbeing
the most common complications.‘” These complications arise
From the Functional Magnetic Stimulation Laboratory, Spinal Cord Injury Service
(Drs. Lin, Singh, Perkash), and Pulmonary Diseases Section, Medical Service (Dr.
Chitkara), VA Palo Alto Health Care System, Palo Alto; and Division of Physical
Medicine and Rehabilitation, Department of Functional Restoration (Drs. Lin,
Perkash), and Department of Medicine (Dr. Chitkara), Stanford University School of
Medicine, Stanford, CA.
Submitted for publication May 27, 1997. Accepted in revised form September 2,
1997.
Supported by the Paralyzed Veterans of America Spinal Cord Injury Research
Foundation and the VA Rehabilitation Research and Development Service.
No commercial party having a direct or indirect interest in the subject matter of this
article has conferred or will confer a benefit upon the authors or upon any organization
with which the authors are associated.
Reprint request to Vernon W.H. Lin, MD, PhD, Spinal Cord Injury Service, VAPalo
Alto Health Care System, 3801 Miranda Avenue, Palo Alto, CA94304.
0 1998 by the American Congress of Rehabilitation Medicine and the American
Academy of Physical Medicine and Rehabilitation
0003~9993/98/7905-4520$3.00/O
517
for Restoring Cough
partly because of the loss of supraspinal control on the
expiratory muscles and because of difficulties in clearing
airway secretions effectively.
Current management of expiratory dysfunction in patients
with SC1 includes passive postural drainage, suction, and
assisted or “quad” cough.4 Each method has a varying degree
of effectiveness and all require active assistance. In addition,
functional electrical stimulation (FES) of the abdominal muscles
has been demonstrated to produce effective expiratory function
in tetraplegic patients. 5,6This method requires electrode place-
ment and can be painful to patients with preserved sensation
below the level of injury. FES of the lower thoracic nerves has
also resulted in significant expired pressure and flow rate in
dogs.7 Recently, functional magnetic stimulation (FMS) has
been developed into a noninvasive technique for stimulating the
spinal nerves.8 FMS has been applied to stimulate phrenic
nerves,9,i0 thoracic spinal nerves,” and cerebral cortex to
evaluate the respiratory system.*2%‘3
In a preliminary study using normal and able-bodied sub-
jects, FMS of the expiratory muscles resulted in substantial
improvement in expired pressure, volume, and flow rate to a
level comparable with that of voluntary maximal effort.14 In
most subjects with SCI, the spinal motor neurons below the
level of injury are spared. Therefore, it is conceivable that the
expiratory muscles innervated by these spinal nerves can be
activated by applying FMS along the dorsal spine.
The goals of this study were (1) to assessthe usefulness of
FMS for restoring cough in subjects with SCI; (2) to determine
the optimal stimulation intensity and magnetic coil (MC)
placement for maximal expiratory function, and (3) to compare
the effect of FMS with other methods used for restoring cough
in patients with SCI.
METHODS
Thirteen male patients with chronic SC1 were recruited for
this study. Table 1 describes the characteristics of this study
population. Patients with cardiac pacemakers, other metallic
devices, or active pulmonary conditions were excluded from
the study. An informed consent was processed in accordance to
the Stanford University Human Subjects Administrative Panel.
Each patient underwent a thorough history and physical exami-
nation to determine eligibility for the study.
A commercially available magnetic stimulator (Dantec Mag
Proa) with a round coil (13.7cm in outer diameter) was used in
this study. This stimulator was capable of generating biphasic
pulses (280 microseconds pulse width) with magnetic gradient
up to SOkTesla/sec.The time-varying magnetic field produced
an induced electric current that facilitated the activation of the
nervous tissue.i5
Baseline Evaluation
The baseline pulmonary function tests (PFTs) were per-
formed using a Medical Graphics PFT system.b The measure-
ments included maximum expired pressure (MEP), maximum
inspired pressure (MIP), slow vital capacity (SVC), expiratory
reserve volume (ERV), forced vital capacity (FVC), forced
expiratory flow (FEF) rate from total lung capacity (FEF-TLC),
Arch Phys Med Rehabil Vol 79, May 1998
518 MAGNETIC STIMULATION FOR COUGH, Lin

Table 1: Injury Profile of Study Participants expressed in mean + SEM, and compared with MEP, ERV, and
Level of ASIA Duration of Cause of FEF-FRC. Statistical analyses were performed using a one-way
Patient Injury Classification Age (yrs) Injury (yrs) Injury analysis of variance and Student’s t test; p < .05 was considered
significant.
1 C5 8 56 33 MVA
2 c5 A 47 26 MVA RESULTS
3 c7 A 36 6 DA
Thirteen patients with chronic SC1with injury levels ranging
4 c5 B 48 10 MVA
from C4 to C7 were recruited for this study. The mean values
5 c5 A 42 19 MVA
for the baseline PFTs were MEP = 56.2 + 7.95cmHz0, MIP =
6 C6 A 52 19 MVA
72.6 _t 6.91cmHz0, SVC = 2.10 +- .25L, ERV = .46 + .06L,
7 c4 8 70 1 Fall
FVC = 2.19 ? .17L/sec, and FEF-FRC = 4.73 + .37Wsec.
8 c5 A 43 14 GSW
Two patients (no. 2 and no. 11) were excluded from the regular
9 c5 A 47 15 MVA
protocol because no observable CMAP was observed in re-
IO C6 A 36 13 DA
sponse to magnetic stimulation during the screening nerve
11 c5 A 41 21 MVA
conduction study and their PFT values were also not included in
12 c4 D 45 6 Fall
the baseline PFT mean. The nerve conduction study showed
13 c5 A 47 8 MCA
simultaneous multiple thoracic nerve activation by magnetic
Abbreviations: ASIA, American Spinal Injury Association; MVA, stimulation. The T7 intercostal muscle was maximally activated
motor vehicle accident; DA, diving accident; GSW, gunshot wound; when the MC was placed near the T7 spinous process. When the
MCA, motorcycle accident.
MC was placed at TlO, the rectus abdominis and external
oblique muscles were maximally activated while the T7 inter-
and FEF rate at functional residual capacity (FEF-FRC). A costal muscle was only partially activated (20% of maximal
Medical Graphics respiratory pressure module was used to amplitude). No T7 intercostal muscle CMAP was observed
determine pressure, and a heated pneumotach was used for when the coil was moved above T2 or below T12 levels.
volume and flow measurements. The pressure transducers and In this study group, the highest mean MEP obtained by FMS
pneumotachs were calibrated daily to maintain accuratemeasure- was observed when the MC was placed at the TlO to Tll
ments. spinous processes (fig 2). Magnetic stimulation at these spinal
The study was performed while the subjects were sitting in a
wheelchair. Spinous processes between T2 and L2 were pal-
pated and marked. For screening purposes, a preliminary nerve
conduction study of the lower intercostal nerves was also
performed using a standard electromyography (EMG) machine
(Nicolet Vikingc). Active electrodes were placed in the 7th
intercostal muscle, rectus abdominis, and external oblique
muscles. While using single-pulse magnetic stimulation, the
MC placement profile was generated by moving the center of
the MC along the spinous processesfrom T2 to L2.“,14 Patients
who did not respond to magnetic stimulation or did not exhibit
appropriate compound muscle action potential (CMAP) were
excluded from the FMS protocol, and only selected measure-
ments were made for comparison purposes.
FMS Protocol
Subjects were instructed to breathe normally through a
respiratory pressure module. Once they established three tidal
breaths, FMS was applied at the end of a normal inspiration and
the expired pressure was measured. Stimulation parameters
were 70% intensity, 20Hz frequency, and 2-second burst length.
While performing FMS, the center of the MC was moved along
the spinous processes between T6 and T12 (fig 1). The
corresponding changes in airway pressure (AP) were deter-
mined. The MC placement that produced maximal AP was used
for the rest of the FMS protocol.
After the optimal MC placement was established, an inten-
sity profile was generated using varying intensities (50%, 60%,
70%, SO%, and 90%) while keeping the frequency and burst
length at 20Hz and 2sec, respectively. The MEP obtained by
FMS was compared with voluntary MEP. Similarly, measure-
ments of ERV and FEF obtained by FMS were performed at
70% intensity, 20Hz frequency, and 2-set burst length. In
addition, a similar intensity profile (50%, 60%, 70%, 80%, and
90%) was also performed for FEF by FMS.
Statistical Methods
Fig 1. Schematic drawing of the placement of the MC along the
Data obtained from the PFTs were expressed in mean t spine for most effective expiratory function. In this figure, the center
SEM. MEP, ERV, and FEF obtained by FMS were also of the MC is located at the T9 spinous process.

Arch Phys Med Rehabil Vol 79, May 1998

 MAGNETIC STIMULATION FOR COUGH, Lin 519

levels produced a significant contraction of abdominal muscles 150

without an observable contraction of upper chest or upper
extremity muscles. This effect of varying MC placements on
expired pressure is demonstrated in figure 3.
This study also found that the expired pressure increased 100
progressively as the stimulation intensity increased to SO%. 6
Subsequent stimulation at a higher intensity did not result in a s
further increase in pressure. Figures 4 and 5 show the effect of E
varying stimulation intensity on AP. Similar results were also
found in the nerve conduction study, which showed that the g 50
CMAP amplitude increased progressively with the increase in
stimulation intensity up to 80%. I4 Figure 6 shows the increase
in expiratory flow with respect to varying stimulation intensi-
ties. Maximal FEF by FMS was observed at 80% intensity.
The mean MEP, ERV, and FEF obtained by FMS were 0
66.40 t 6.69cmHz0, .77 -t .14L, and 5.28 ? .42L/sec,
T6 T7 T8 T9 TlO Tll T12
respectively. These values corresponded to 118%, 169%, and
110% of the subjects’ voluntary maximum. Of the three values Coil Placement
compared above, only ERV showed a statistically significant
improvement with FMS (p < .OS). With FMS, 8 of the 11 Fig 3. An example of changes in airway pressure (AP) generated by
subjects generated MEP and ERV greater than voluntary different MC placements along the spinous processes of T6 to T12,
maximum values; 6 of these 8 subjects produced more than The stimulation parameters were fixed at 70% intensity, 20Hz
frequency, and 2-set burst length. The maximum expired pressure
150% of their voluntary maximum. Figures 7 and 8 illustrate was observed between TIO and Tll.
the significant increase in ERV and FEF obtained by FMS in
one subject.
When comparing these results with our previous normal comparable results. When compared with able-bodied, normal
subject study on FMS of the expiratory muscles, MEP, ERV, controls, FMS produced comparable tlow rates but lower MEP
and FEF generated by FMS in patients with SC1 were 61%, and ERV. These values also were consistent with other existing
49%, and 110% of the normal subjects’ values, respectively.14 methods, assisted cough (quad cough) and FES of abdominal
The two subjects that were excluded from the FMS protocol muscles, for facilitating cough in SCI.5,6 Using the assisted
responded poorly to FMS; using similar stimulation parameters, cough method, Braun et alI9 demonstrated a mean increase of
the MEPs obtained by FMS in these two subjects were 24 and 11.8% of flow over nonassisted cough (3.73 t lSL/sec). Using
29cmHz0, 73% and 45%, respectively, of their voluntary MEP. FES of the abdominal muscles, Linder5 demonstrated a signifi-
cant increase in mean MEP from 27.3 t 6.4 to 60 i
DISCUSSION 22.8cmH20.
Patients with SC1 often have impaired cough and difficulty in This study found that the best MC placement was at TlO to
clearing airway secretions. This is attributed to the loss of Tll, which was one to two levels below the optimal placement
expiratory and inspiratory muscle functions, thus predisposing in normal subjects.‘” This may be caused by changes in truncal
them to frequent respiratory tract complications.r6J7 When and abdominal muscle anatomy as the result of chronic SCI. In
comparing the mean PFT data obtained in this study with a nerve conduction study using normal subjects, we found that
normal, able-bodied subjects,l5 the mean MEP, ERV, and FEF FMS of the spinal nerves may activate nerves three levels away
in the SC1 patients were 50%, 70%, and 25%, respectively, of from the center of the MCI4 Thus, by placing the MC at TlO,
those in the normal controls. This degree of expiratory dysfunc- the spinal nerves between T7 and Ll may all be activated.
tion is consistent with earlier PFT findings in chronic SCI.ls These spinal nerves serve to innervate most of the major
The major finding in this study was that FMS of the expiratory muscles, which include the abdominal, lower inter-
expiratory muscles resulted in substantial increases in expired costal, and serratus posterior inferior muscles. Increasing
pressure, volume, and flow rate. When compared with their stimulation intensity up to 80% of maximum resulted in
voluntary maximum efforts, FMS produced either better or increasing expiratory function. However, a further increase in

70

60-

50- I
AP I
cm H,O 40-
!
30-

01
OL T6 50%
,
60%
I
70%
I
80%
I
90%
T7 TX T9 TlO Tll T12 Intensity
Coil Placements
Fig 4. Intensity profile: changes in airway pressure (AP) by FMS at
Fig 2. Changes in airway pressure (AP) generated by different MC various stimulation intensities, while the stimulation frequency and
placements. The center of the MC varied from T6 to Tll. burst length remained at 20H2 and 2 seconds, respectively.

Arch Phys Med Rehabil Vol 79, May 1996

520 MAGNETIC STIMULATION FOR COUGH, Lin

150 6

100
8

I
2 I
E
I
3 50
% *

30 B Time (Set)
30
Time (Set)
0
50% 60% 70% 80% 90% Fig 7. An example of improvement in ERV by FMS: (A) an ERV of
.5OL with maximum voluntary effort; (B) an ERV of 2.13L generated
by FMS, which is 326% more than voluntary maximum. The stimula-
Stimulation Intensity tion parameters were 70% intensity, 20Hz frequency, and 2-second
burst length.
Fig 5. An example of changes in airway pressure (AP) generated by
FMS of varying stimulation intensities (from 50% to 90%). The
maximum expired pressure was observed at 80% of stimulation and antispasticity medications that may have also contributed to
intensity. the reduced/absent expiratory muscle response to FMS.
The mechanism of expiratory muscle activation by FMS is
more similar to lower thoracic ventral root stimulation7 than
intensity to 90% resulted in a decrease in expiratory function. FES of the abdominal muscles. FES of the abdominal muscles
This decrease in expiratory function may be from suboptimal stimulates these muscles transabdominally from placement of
activation of the thoracic nerves, as previously demonstrated by several electrodes on the abdomen.5Jj Ventral root stimulation,
the decrease in CMAP amplitude in our earlier normal subject on the other hand, requires laminectomy initially to expose the
study.14This decrease in expiratory function may also be caused spinal canal and then the placement of electrodes along the
by the recruitment of inspiratory agonists, such as the upper ventral aspect of the spinal cord.7 Lower thoracic ventral root
intercostal muscles (parasternal and external intercostals) and stimulation has been shown to produce significant expiratory
the accessory muscles. It is unlikely that diaphragm activation function in dogs,7 but there have been no human study data to
would be a contributing factor to this expiratory function date, possibly because of the invasive nature of ventral root
decrement because our previous animal study using thoracic
FMS did not show significant diaphragmatic activation.20
This study also illustrates that patients with preserved lower
motor neuron function of the spinal nerves respond well to
FMS. The two patients who were excluded from the FMS
protocol had no observable CMAP response to intercostal nerve
stimulation and responded poorly to FMS of the expiratory
muscles. We speculate that these patients had lower motor
neuron injury to the lower thoracic spinal nerves related either
to the original SCI, subsequent trauma, or neuropathy from
other causes. One subject was taking multiple anticholinergic

I I

A
St. Volume (L) 8
BL Volume (L)

50% 60% 70% 80% 90% Fig 8. An example of flow volume loop with and without FMS: (A)
maximum voluntary expiratory flow at the end of a normal inspira-
tion was 5.56Lkec; (B) the FEF generated by FMS was 7.65L/sec, a
Fig 6. Intensity profile: FEF obtained by FMS at various stimulation 38% improvement when compared with (A). The stimulation param-
intensities while the stimulation frequency and burst length re- eters were 70% intensity, 20Hz frequency, and 2-second burst
mained at ZOHz and 2 seconds, respectively. length.

Arch Phys Med Rehabil Vol 79, May 1998

 MAGNETIC STIMULATION
stimulation. Regarding the stimulation focus of magnetic
stimulation, recent reports have suggested that the point of
activation by magnetic stimulation is at the neuroforamen.11,21
We have confirmed this by our independent investigation using
nerve conduction techniques in comparing FMS with FES
(unpublished observation). This is in contrast to the point of
activation by ventral root stimulation which is at the level of the
proximal root near the cord. Both FMS and ventral root
stimulation can activate multiple roots/nerves simultaneously,
thus producing similar clinical responses. The number of roots
stimulated depends on the size of the electrode and the intensity
of stimulation that results in current spread or volume conduc-
tion. Similarly, the number of spinal nerves that can be activated
by FMS depends on the MC design and the intensity of the
stimuli. When compared with our earlier animal study, in this
study we used a bigger coil that has a superior design, thus
resulting in a much improved clinical response.
FMS of the cervical spinal nerves has been demonstrated to
produce significant inspiratory function.g In a separate animal
investigation, we were able to isolate the contribution of the
diaphragm versus the upper intercostal and accessory muscles
by performing phrenectomized dog studies (unpublished obser-
vation). By moving the MC along the spine caudally, we found
a gradual decrease in inspiratory function. By the time the MC
reached the midthoracic region, expiratory function began to
emerge and reached a maximum when the MC was placed
along the T9 spinous process. This illustrates that FMS can be
easily applied to condition both the inspiratory as well as the
expiratory muscles. Patients with tetraplegia often have both
expiratory and inspiratory dysfunction. In particular, patients
with partial phrenic function, without inspiratory assistance
from the intercostal or accessory muscles, are often ventilator-
dependent. By conditioning the accessory and intercostal
muscles, the inspiratory capacity necessary for the patient to be
ventilator-independent may be produced. In recent years, our
laboratory has also had good successwith FMS of the bladder
and bowel for facilitating bladder and bowel emptying in
patients with SCIz2 Besides being used as a therapeutic tool,
FMS can also be used as a diagnostic tool to determine the
end-organ response to spinal nerve stimulation.
There are several distinct advantages for FMS of the
expiratory muscles. FMS is not painful and is well tolerated by
normal, able-bodied subjects or those with SC1 and intact,
partial, or no sensation. This is in contrast to an earlier FES
study that reported that 5 of 24 subjects could not tolerate FES
because of painful sensation.6 In addition, FMS is easy to use;
there is no need to place electrodes or apply electrode gels, and
the MC can be placed outside of regular clothing. FMS is also a
safe technology; we have not observed any adverse effect from
FMS of the spinal nerves over the last 5 years.
Of course, patients with pacemakers or other metallic
implants will not be eligible for FMS. In addition, patients with
a history of spinal nerve/root irritation or radiculopathy may
experience worsening of the symptoms, and patients with
urinary incontinence may have worse incontinence because of
either direct abdominal muscle contraction or bladder stimula-
tion. There are also a few technical drawbacks to FMS. FMS is
inefficient and requires a bulky power supply and consumes up
to 250 Joules per pulse. Thus, a portable FMS system will not
be available in the near future. In addition, long stimulation
bursts will frequently result in overheating of the MC. Thus,
improvement in MC design for cooling and for more effective
expiratory muscle activation will be necessary.
Magnetic stimulation of the spinal nerves is clearly an
emerging technology with many important clinical applica-
FOR COUGH, Lin 521
tions. Diagnostically, magnetic stimulation can be used in
various cervical, thoracic, lumbar, or sacral motor nerve
conduction studies. Using repetitive stimulation, FMS can
produce tetanic muscle contraction and result in useful physi-
ologic function. The present study particularly addresses the
usefulness of stimulating the expiratory agonists to generate
expired pressure or flow in patients with SCI. This technology
is not limited only to patients with respiratory muscle dysfunc-
tion, such as those with SCI, multiple sclerosis, or other upper
motor neuron lesion. FMS for cough can also be applied to
patients in the critical care or perioperative settings. FMS of the
expiratory muscles produces physiologic expiratory function
and should prove to be more effective than the passive postural
drainage or chest percussion techniques. It is conceivable that
FMS may prove to be a very useful therapeutic modality for
mobilizing bronchial secretions, thus preventing respiratory
tract infections, atelectasis, or bronchiectasis. Furthermore, this
study introduces a new tool to stimulate the spinal nerves and
the respiratory muscles that will facilitate greater understanding
of the respiratory system in future investigations.
In summary, FMS of the expiratory muscles produced
significant expired pressure, volume, and flow either compa-
rable to or better than other existing modalities. FMS is a
noninvasive and easy-to-use method of restoring cough in
patients with SCI. FMS may prove to be an important therapeu-
tic tool to restore cough in patients with SCI, with other upper
motor neuron pathologies, and in critical care/perioperative
settings.
Acknowledgments: The authors thank Tamara Bushnik, PhD,
JamesCanfield, BS, Ian Hsiao, PhD, and Roy Sasaki,MD, for their
assistanceat various stagesof this project. The authors also thank
Dantec Medical, Inc. for providing the magnetic stimulator and the
magneticcoil. This work includesportions of the graduate dissertation
of VernonLin, MD.
References
1. Bellamy R, Pim FW, Stauffer ES. Respiratory complications in
traumatic quadriplegia: analysis of 20 years’ experience. J Neuro-
surg 1973;39:596-600.
2. Fishbum MJ, Marino RJ, Ditunno JF. Atelectasis and pneumonia
in acute spinal cord injury. Arch Phys Med Rehabil 1990;71:197-
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3. McMichan JC, Michel L, Westbrook PR. Pulmonary dysfunction
following traumatic quadriplegia. JAMA 1980;243:528-3 1,
4. Kirby N, Bamerias MJ, Siebens AA. An evaluation of assisted
cough in quadriplegic patients. Arch Phys Med Rehabil 1966;47:
705-10.
5. Linder SH. Functional electrical stimulation to enhance cough in
quadriplegia. Chest 1993;103:166-9.
6. Jaeger RJ, Turba RM, Yarkony GM, Roth EJ. Cough in spinal cord
injured patients: comparison of three methods to produce cough.
Arch Phys Med Rehabil 1993;74:1358-61.
7. DiMarco AF, Romaniuk JR, Supinski GS. Electrical activation of
the expiratory muscles to restore cough. Am J Respir Crit Care
Med 1995;151:1466-71.
8. Cadwell J. Principles of magnetoelectric stimulation. In: Chokro-
verty S, editor. Magnetic stimulation in clinical neurophysiology.
Boston IMA): Butterworths: 1989. u. 16-32.
9. Similowski T, Fleury B, Launois S, ‘Cathala HP, Bouche P, Derenne
JP. Cervical magnetic stimulation: a new painless method for
bilateral phrenic nerve stimulation in conscious humans. J Appl
Physiol 1989;67:1311-8.
10. Wragg S, Aquiline R, Moran J, Ridding M, Hamnegard C, Feam T,
et al. Comparison of cervical magnetic stimulation and bilateral
percutaneous electrical stimulation of the phrenic nerves in normal
subjects. Eur Respir 1994;7:1778-92.
11. Chokroverty S, Deutsch A, Guha C, Gonzalez A, Kwan P, Burger
R, et al. Thoracic spinal nerve and root conduction: a magnetic
stimulation study. Muscle Nerve 1995;18:987-91.
Arch Phys Med Rehabil Vol 79, May 1998
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12. L&ens MA. Motor evoked potentials of the human diaphragm
elicited through magnetic transcranial brain stimulation. J Neurol
Sci 1994;124?204-7:
13. Zifko U. Remtulla H. Power K. Harker L. Bolton CF. Transcortical
and cervical mag&ic stimulation with recording of the dia-
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stimulation for cough [abstract]. Am Resp Crit Care Med 1997;155:
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15. Barker A, Jalinous R, Freeston I, Jaratt J. Magnetic stimulation of
the human nervous system: an introduction and the results of an
initial clinical evaluation. Neurosurgery 1987;20: 100-9.
16. Stone DJ, Keltz H. The effect of respiratory muscle dysfunction on
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AmRev Resp Dis 1963;88:621-9.
17. Fugl-Meyer AR. Effects of respiratory muscle paralysis in tetraple-
gic and aaraoleeic natients. Stand J Rehab Med 1971:3:141-50.
18. Ledsomk Ji, Iitiniola P, Alba AS. Pulmonary fun&on in acute
cervical cord injuries. Am Rev Respir Dis 1981;124:41-4.
19. Braun SR, Giovannoni R, O’Connor M. Improving the cough in
patients with spinal cord injury. Am J Phys Med 1984;63:1-10.
20. Lin VWH, Romaniuk JR, DiMarco AF. Magnetic stimulation of
the intercostal muscles [abstract]. Arch Phys Med Rehabil1993;74:
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21. Macabee PJ, Amassian VE, Eberle LP, Rude11AP, Cracco RQ, Lai
KS, et al. Measurement of the electric field induced into inhomoge-
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Suppliers
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b. Medical Graphics Corporation, 350 Oak Grove Parkway, St. Paul,
MN 55127.
c. Nicolet Biomedical, Inc., 5525-2 Verona Road, Madison, WI
53711-4495.

Arch Phys Med Rehabil Vol 79, May 1998

162
Functional Magnetic Stimulation for Conditioning of
Expiratory Muscles in Patients With Spinal Cord Injury
Vernon W. Lin, MD, PhD, Ian N. Hsiao, PhD, Ercheng Zhu, MD, PhD, Inder Perkash, MD
ABSTRACT. Lin VW, Hsiao IN, Zhu E, Perkash I. Func-
tional magnetic stimulation for conditioning of expiratory mus-
cles in patients with spinal cord injury. Arch Phys Med Rehabil
2001;82:162-6.
Objective: To evaluate the effectiveness of functional mag-
netic stimulation (FMS) in conditioning expiratory muscles
patients with spinal cord injury (SCI).
Design: A prospective before-after trial.
Setting: The Functional Magnetic Stimulation Laboratory of
the SCI Health Care Group, VA Long Beach Health Care
System, and the Spinal Cord Injury Services, Department of
Veterans Affairs, Palo Alto Health Care System.
Participants: Eight men with tetraplegia.
Intervention: Expiratory muscle training was achieved by
placing a magnetic stimulator with a round magnetic coil along
subjects’ lower thoracic spine.
Main Outcome Measures: Measures taken were the max-
imal expired pressure at total lung capacity (MEP-TLC) and at
functional residual capacity (MEP-FRC), expiratory reserve
volume (ERV), and the forced expiratory flow rate at TLC
(FEF-TLC) and at FRC (FEF-FRC) by subjects’ voluntary
maximal efforts.
Results: After 4 weeks of conditioning, the mean ⫾ stan-
dard error of the mean values were: MEP-TLC, 55.3 ⫾
8.6cmH2O; MEP-FRC, 29.6 ⫾ 5.6cmH2O; ERV, .57 ⫾ .08L;
FEF-TLC, 4.3 ⫾ 0.5L/s; and FEF-FRC, 1.9 ⫾ 0.2L/s. These
values correspond to, respectively, 129%, 137%, 162%, 109%,
and 127% of pre-FMS conditioning values. When FMS was
discontinued for 2 weeks, the MEP-TLC returned to its pre-
FMS training value.
Conclusion: A 4-week protocol of FMS of the expiratory
muscles improves voluntary expiratory muscle strength signif-
icantly, indicating that FMS can be a noninvasive therapeutic
technology in respiratory muscle training for persons with
tetraplegia.
Key Words: Magnetic stimulation; Muscles; Rehabilitation;
Spinal cord injuries.
© 2001 by the American Congress of Rehabilitation Medi-
cine and the American Academy of Physical Medicine and
Rehabilitation
From the Functional Magnetic Stimulation Laboratory, Spinal Cord Injury/Disor-
der, Health Care Group, VA Long Beach Health Care System, Long Beach, CA (Lin,
Hsaio, Zhu); Department of Physical Medicine and Rehabilitation, University of
California, Irvine, CA (Lin, Zhu); Spinal Cord Injury Services, Department of
Veterans Affairs, Palo Alto Health Care System, Palo Alto, CA (Perkash); and
Department of Urology and Functional Restoration, Stanford University, School of
Medicine, Stanford CA (Perkash).
Accepted in revised form May 17, 2000.
Supported by the VA Rehabilitation Research and Development and the Paralyzed
Veterans of America Spinal Cord Injury Research Foundation (grant no. 1692-20).
No commercial party having a direct financial interest in the results of the research
supporting this article has or will confer a benefit upon the authors or upon any
organization with which the author(s) is/are associated.
Reprint request to Vernon W. Lin, MD, PhD, Spinal Cord Injury/Disorder Health
Care Group (07/128), 5901 E Seventh St, Long Beach, CA 90822.
0003-9993/01/8202-6087$35.00/0
doi:10.1053/apmr.2001.18230
Arch Phys Med Rehabil Vol 82, February 2001
MPAIRED COUGH in patients with spinal cord injury
Iratory
(SCI) is among the most important causes of frequent respi-
complications such as mucus plugging, atelectasis, and
pneumonia. Respiratory management of patients with chronic
SCI includes frequent suctioning, chest percussion and postural
drainage, quad-cough, and respiratory muscle–training exer-
cises. Functional electric stimulation (FES) of the abdominal
muscles and ventral thoracic spinal nerves is also effective in
producing expiratory flow and pressure.1,2 Despite the success
of these techniques, there remains a need for a noninvasive and
effective procedure that is suitable for long-term respiratory
muscle conditioning.
Functional magnetic stimulation (FMS) is effective in stim-
ulating the expiratory muscles in both humans and animals.3-6
In patients with chronic SCI, FMS has resulted in expiratory
function that was substantially above their maximal voluntary
efforts.6 FMS of the expiratory muscles is easy to use, is
noninvasive, and does not require extensive preparation. Un-
like FES, FMS is well tolerated by subjects with intact or
partial sensation.
This study evaluated the effect of expiratory muscle condi-
tioning with FMS on pulmonary function in patients with SCI.
Expiratory functions of these patients were measured at several
stages: baseline, 2-week conditioning, 4-week conditioning,
and 2-week postconditioning.
METHODS
Eight men with chronic SCI were recruited for the study.
Patients with cardiac pacemakers, other metallic devices, high
blood pressure, or with active pulmonary conditions were ex-
cluded. Informed consent was processed in accordance with the
Human Subjects Committee at the Department of Veterans
Affairs, Palo Alto Health Care System, and at the Department
of Veterans Affairs, Long Beach Health Care System. Each
patient underwent a history and physical examination to estab-
lish eligibility for the study.
A commercially available magnetic stimulatora with a round
magnetic coil (20cm in outer diameter) was used. A cooling
unit that circulated oil in and out of the coil was designed to
allow continuous stimulation for 30 or more minutes. The
stimulator could generate biphasic pulses (280-␮s pulse width)
with magnetic gradients up to 50kTesla/s. This time-varying
magnetic field produced an induced electric current that facil-
itated activation of the nervous tissue.7
Baseline Pulmonary Function Tests Evaluation
Baseline pulmonary function tests (PFTs) were performed
with a Vmax 229 Sensormedics System.b Subjects were tested
between 1 and 3 PM. A 15-minute rest period was required to
avoid the influences of daily activities on the PFT results. In
this system, we used a respiratory pressure module to deter-
mine pressure and a heated pneumotach to measure volume and
flow. The pressure transducers and pneumotachs were cali-
brated daily to ensure accurate measurements. The maximum
expiratory pressure at total lung capacity (MEP-TLC), the
expiratory reserve volume (ERV), and the forced expiratory
flow rate at TLC (FEF-TLC) were measured as indicators of
 MAGNETIC CONDITIONING OF EXPIRATORY MUSCLES, Lin
the expiratory muscle strength. For comparison, MEP and FEF
at functional residual capacity (MEP-FRC, FEF-FRC) were
also measured. Other PFT parameters, such as forced vital
capacity (FVC) and forced expiratory volume (FEV1), were
recorded.
To detect patients’ responses to magnetic stimulation, MEP,
ERV, and FEF at FRC generated by FMS (MEP-FMS, ERV-
FMS, FEF-FMS) was conducted on each patient. The stimula-
tion parameters were 70% of maximum intensity, 20Hz fre-
quency, 2-second burst length, and a T10 magnetic coil
placement.6 The stimulation was performed while the subjects
were sitting in their wheelchairs.
FMS Conditioning Protocol
The experimental protocol continued for 6 weeks. In the first
week, subjects underwent screening histories and physical ex-
aminations. Thereafter, a baseline PFT was evaluated and
recorded with subjects in a sitting position. Physical examina-
tions and PFTs were repeated in the final week. Before the
conditioning protocol, subjects were instructed to maintain
regular diets and their routine activities of daily living. At the
beginning of the second week, each subject received a 4-week
FMS conditioning program (20min twice a day, 5d/wk) in the
SCI center. During this conditioning program, a PFT was
repeated at 2-week intervals, ending with a 2-week postcondi-
tioning PFT. The subjects were asked to note any changes in
their physical condition during the 4 weeks. Before each con-
ditioning session, subjects were asked if they had any discom-
fort and/or abnormalities. After each session, subjects’ skin
was checked for possible thermal injury. Blood pressure was
monitored before and every 5 minutes during the conditioning
period to ensure patient safety. Magnetic stimulation parame-
ters were initially set at 50% intensity, 20Hz frequency, and
2-second burst length. Intensity was gradually increased from
50% to 70%, depending on subject’s comfort zone. The center
of the magnetic coil was placed at T10 to T11.4 FMS of the
expiratory muscles was performed 5 days a week. In week 2
and at the completion of the training session (week 4), the
expiratory muscle strength was evaluated by measuring the
MEP, ERV, and FEF.
Statistical Methods
Data from the PFTs were expressed in mean ⫾ standard
error of the mean (SEM). Statistical analyses were performed
by using a 2-way analysis of variance and Student’s t test; p ⬍
.05 was considered significant.
RESULTS
Demographics
The mean age and time since injury of the 8 subjects were
51 ⫾ 8 years and 18 ⫾ 9 years, respectively. Seven subjects
had a SCI level between C5 and C7, and one had a SCI level
at T5 (table 1). All subjects completed the conditioning proto-
col.
Baseline PFT Results
Baseline PFT results are summarized in figures 1 through 3
and table 2. The mean baseline PFT results were: MEP-TLC ⫽
48 ⫾ 9.7cmH2O, MEP-FRC ⫽ 24.3 ⫾ 6.1cmH2O, ERV ⫽
0.4 ⫾ 0.1L, FEF-TLC ⫽ 4.0 ⫾ 0.5L/s, FEF-FRC ⫽ 1.6 ⫾
0.2L/s, FVC ⫽ 2.4 ⫾ 0.1L, and FEV1 ⫽ 1.9 ⫾ 0.1L. Two
parameters of interest were the percentage of the predicted
normal value of the mean FVC ⫽ 50.7% ⫾ 5.2% and the mean
FEV1% (FEV1/FVC) ⫽ 82.8% ⫾ 1.7%. The means of MEP-
163
Table 1: SCI Profile of Study Participants
Level of ASIA Age Duration of Cause of
Patient Injury Classification (yr) Injury (yr) Injury
1 C5–C6 A 57 18 MVA
2 C4–C5 A 47 23 Fall
3 C5–C7 A 49 26 MVA
4 C5 B 43 20 MVA
5 C4 B 40 6 MVA
6 C5–C7 A 66 27 DA
7 T5 A 53 20 MVA
8 C4–C5 A 55 2 MVA
Abbreviations: ASIA, American Spinal Injury Association; MVA, mo-
tor vehicle accident; DA, diving accident.
FMS, ERV-FMS, and FEF-FMS were 42 ⫾ 4.9cmH2O, 0.6 ⫾
0.10L, and 2.9 ⫾ 0.42L/s, respectively.
PFT Results After 2 Weeks
All subjects completed the first 2 weeks of training. Condi-
tioning sessions were at approximately the same time each day.
No unusual alterations in daily activities or diets, including
medications, were reported. No medical complications or side-
effects were noted. A routine skin check after stimulation
showed no inauspicious conditions. Blood pressure remained
within subjects’ normal values during FMS conditioning. The
2-week conditioning PFT results showed that the mean MEP-
TLC, MEP-FRC, ERV, FEF-TLC, FEF-FRC, FVC, and FEV1
were 56 ⫾ 10.1cmH2O, 28 ⫾ 5.9cmH2O, 0.51 ⫾ 0.1L, 4.1 ⫾
0.4L/s, 1.9 ⫾ 0.3L/s, 2.5 ⫾ 0.1L, and 2.0 ⫾ 0.1L, respectively.
These values showed a 22%, 24%, 40%, 4%, 20%, 10%, and
9% increase from subjects’ respective mean baseline PFT
results, respectively. Significant improvements ( p ⬍ .05)
were seen in MEP-TLC and MEP-FRC (fig 1). FEF-TLC and
FEF-FRC showed moderate increases (fig 2). The results were
not statistically significant. FVC and FEV1 had negligible
changes. Among all the parameters, ERV showed the most
improvement after the first 2 weeks of conditioning (fig 3).
When asked for their reaction to FMS conditioning, 6 subjects
said that they experienced “tightening” or “strengthening” of
their abdominal muscles, and an improved ability to cough up
secretions. These changes occurred within the first week of
conditioning. Two subjects reported no changes. None of the
subjects had any negative responses or complaints about FMS.
PFT Results After 4 Weeks
All subjects continued the second half of the conditioning
protocol. No medical complications or adverse effects were
reported in the final 2 weeks. The consensus of the participants
was that FMS training of expiratory muscle was not painful,
was well tolerated, and was helpful. The 4-week conditioning
PFT results showed that the mean (n ⫽ 8) MEP-TLC, MEP-
FRC, ERV, FEF-TLC, FEF-FRC, FVC, and FEV1 were 55.3 ⫾
8.6cmH2O, 29.0 ⫾ 5.6cmH2O, 0.6 ⫾ 0.1L, 4.3 ⫾ 0.5L/s, 1.9 ⫾
0.2L/s, 2.5 ⫾ 0.1L, and 2.0 ⫾ 0.1L, respectively. These values
showed increases of 29%, 37%, 62%, 9%, 27%, 7%, and 10%
of subjects’ respective mean baseline PFT results, respectively.
The improvements were significant ( p ⬍ .05) for MEP-TLC,
MEP-FRC, and ERV. FVC and FEV1 increased by ⱕ10% of
their normal values after 4 weeks of training and were not
significant ( p ⬎ .05). Final physical examinations showed no
new abnormalities. The increases of MEP-TLC, MEP-FRC,
ERV, FEF-TLC, FEF-FRC, FVC, and FEV1 from the second
week to the fourth week of FMS conditioning were 6%, 12%,
Arch Phys Med Rehabil Vol 82, February 2001
164 MAGNETIC CONDITIONING OF EXPIRATORY MUSCLES, Lin

Fig 1. MEP improvements at TLC and FRC. Changes in airway pres- Fig 3. ERV improvement. Changes in lung volume (L) throughout
sure (cmH2O) throughout the conditioning protocol. (䊐), MEP-TLC; the conditioning protocol. *Versus baseline, p < .05.
(■), MEP-FRC. *Versus baseline, p < .05.

19%, 4%, 6%, 0%, and 2%, respectively. However, no statis-
tical significance was observed for any of the parameters in the
last 2 weeks of conditioning ( p ⬎ .05).
PFT Results at 2 Weeks Postconditioning
Six subjects returned 2 weeks after completing the condi-
tioning protocol. The mean values of MEP-TLC, ERV, FEF-
TLC obtained during this postconditioning protocol showed
decreases of 13%, 16%, and 5%, respectively, from their values
at the end of the 4-week conditioning protocol. The poststimu-
lation data, when compared with the baseline data, showed no
statistically significant differences.
DISCUSSION
Persons with chronic cervical SCI typically show a restric-
tive respiratory pattern with both inspiratory and expiratory
dysfunction.8 Their PFT results showed low mean TLC, vital
capacity, and inspiratory capacity as well as a high FEV1: FVC
ratio, in addition to low expiratory pressure, flow, and ERV,
indicating a decrease or absence of expiratory muscle func-
tion.6,8,9 Patients with thoracic spinal lesions may have only
expiratory dysfunction with preserved inspiratory capacities.8
In this study, we applied FMS to restore the impaired expi-
ratory function in SCI patients by using a 4-week FMS expi-
ratory muscle-training program. This is a continuation of our
previous efforts, which showed efficacy in magnetically stim-
ulating the expiratory muscles by placing a magnetic coil in the
lower thoracic region.3-6 By conditioning the expiratory mus-
cles for only 2 weeks, we observed significant improvement in
voluntary MEP (22%), FEF (20%), and ERV (40%). We also
observed continued improvement after 2 additional weeks of
conditioning. According to the present protocol, expiratory
muscles were stimulated for 20 minutes twice a day. The
stimulation intensity was set with a minimum intensity of 50%,
and a burst length of 2 seconds, which produced a substantial
contraction of the expiratory muscles.3
Recent respiratory training protocols have focused on in-
spiratory and expiratory efforts against a closed airway or
airway resistance loading for respiratory muscle training.10 In
patients with SCI, reports have shown improvement in inspira-
tory muscle strength and endurance after inspiratory resistance
training.10,11 Biering-Sorensen et al12 showed that the peak
expiratory flow of 10 cervical injured patients improved by
11% (from 371 to 412L/min) by using a 6-week inspiratory
resistance training protocol. Suzuki et al13 reported a 25%

Table 2: PFT Profile of Study Participants

Patient FVC (L) FEV1 (L) IC (L) ERV (L)

1 3.09 2.34 2.56 0.53

2 2.87 2.47 2.19 0.68
3 2.67 2.02 2.35 0.32
4 2.17 1.52 1.84 0.33
5 2.24 1.29 2.04 0.20
6 2.75 2.36 2.32 0.43
7 0.56 0.56 0.56 0.00
8 3.13 2.52 2.71 0.42
Mean 2.44 1.89 2.07 0.36
Fig 2. FEF improvements at TLC and FRC. Changes in airway flow SEM 0.11 0.10 0.10 0.07
(L/s) throughout the conditioning protocol. (䊐), FEF-TLC; (■), FEF-
FRC. Abbreviation: IC, inspiratory capacity.

Arch Phys Med Rehabil Vol 82, February 2001

 MAGNETIC CONDITIONING OF EXPIRATORY MUSCLES, Lin
increase in MEP after 4 weeks of threshold pressure training (at
30% of MEP) by using healthy subjects. Their subjects were
trained for 15 minutes twice daily for 4 weeks at their own
breathing frequency and tidal volume. The length of training
and stimulation duration were comparable with our protocol.
Smeltzer14 reported a similar finding in patients with multiple
sclerosis. They observed an increase in MEP of 19.4 ⫹
9.9cmH2O from a baseline value of 53.6 ⫹ 14.9cmH2O after 3
months of expiratory muscle training by using a threshold
training device.
The goals of FMS expiratory muscle conditioning in patients
with SCI are to restore strength and endurance of the disused
expiratory muscles. Muscle disuse usually leads to a decrease
in muscle mass, in the proportion of type I (fatigue resistant)
fibers, and in oxidative enzymes, and results in reduced
strength and endurance. There are 3 major principles of muscle
training: overload, training specificity, and reversibility.15 The
muscle must be overloaded above a threshold to a point at
which the muscle will be activated more than usual. The
stimulation protocol given to the muscles has to be specific to
the desired effect. The training effect is reversible once training
is stopped. This study has shown significant contraction of the
expiratory muscles with stimulation and functional improve-
ment of the expiratory muscles, as well as the reduction of
expiratory function after the conditioning protocol. The clinical
significance of our results is that FMS restored partial strength
of the disused expiratory muscles and potentially improved
coughing capacity in patients with tetraplegia. The limitation of
this study is that we have not provided results on respiratory
muscle fatigue or muscle biopsies. Nevertheless, this is the first
report on the effects of FMS in the conditioning of the expi-
ratory muscles.
Two weeks after the conditioning protocol ended, the vol-
untary expiratory function decreased sharply to a level compa-
rable with the baseline. This functional decrease is comparable
to that seen by Gurney et al,16 which showed decreased skeletal
muscle performance after cessation of training in SCI. This
also suggests that for FMS to be beneficial to subjects with
SCI, persistent training is required.
FES of the respiratory muscles has been an active area of
research in recent decades. Devices have been designed to
stimulate the phrenic nerves,17 ventral roots,18 intercostal
nerves,19 diaphragm, and abdominal muscles.1,2 By placing
surface electrodes on the abdomen, significant expiratory func-
tion was observed.1,2 DiMarco et al20 showed impressive ex-
piratory function in dogs by using plate electrodes implanted in
the ventral aspect of the spinal cord near T9. Electric stimula-
tion conditioning of denervated skeletal muscles at 20Hz,
5-second bursts, 15 minutes to 8 hours a day for 24 weeks
increases the proportion of type I fibers, and enhances endur-
ance properties of the paralyzed muscles.21 FES techniques
require placing electrodes on the muscles or on the nerve
tissues, which requires skin preparation or surgical procedures.
These procedures may be inconvenient, painful to patients with
preserved sensation, or they may result in medical complica-
tions.2
In contrast to FES, FMS is relatively easy to use, is nonin-
vasive, and is not painful. As shown in an earlier study,3,6 the
optimal placement of the magnetic coil in patients centers near
T10 –T11 spinous process. This placement stimulates spinal
nerves between T7 and L2, which activate most of the expira-
tory agonists such as the internal intercostal muscles, internal
and external oblique, transversus abdominis, and rectus ab-
dominis. This placement was further supported by another
study in which we sequentially placed the magnetic coil be-
tween T1 through L5.5 The size of the coil and its configuration
165
are important factors for stimulation effects.22 With magnetic
coil placement near the spinous process, the loci of spinal nerve
activation is at the neuroforamen.23 Activation of the spinal
nerves at the foramina leads to simultaneous contraction of the
major expiratory muscles. Depending on the appropriate design
and placement of the coil, significant inspiratory or expiratory
function can be produced.6 In unimpaired subjects, FMS pro-
duced expiratory function similar to the subjects’ voluntary
maximum. In tetraplegic patients, FMS reached a mean expired
pressure, volume, and flow rate of 121%, 167%, and 110%,
respectively, of their voluntary maximum.6
The mechanism underlying the effect of long-term FMS
conditioning is likely the myosin isoform shifts induced by
near maximal muscle contraction.24 The intensity of FMS that
is applied to reload the disused muscles in patients with SCI
may also induce transient muscle fiber injuries.25 It is proposed
that exercise-induced injury initiates muscle fiber proliferation
and phenotype remodeling.26,27 Whether FMS conditioning
applied in the present study induces changes in muscle mass
and other metabolic or morphologic properties attracts great
attention.
The benefits of FMS of the expiratory muscles were not
limited to improvement of voluntary cough function, thus,
reducing the risk of life-threatening respiratory complications.
We also observed improvement of inspiratory function after the
4-week conditioning protocol. The inspiratory capacity in-
creased approximately 5% after 4 weeks of training and was
associated with a 6% increase of the FEF-TLC (fig 2). Similar
improvements occurred in FVC and FEV1. We propose that to
achieve the optimal respiratory muscle conditioning results,
both expiratory and inspiratory muscles should be trained. In
addition to patients with SCI or with other neurologic pathol-
ogies, patients with respiratory dysfunction, or who are under
sedation, or are in intensive care settings, may benefit from
such a controlled expiratory muscle stimulation technology. In
addition to the respiratory muscles, FMS has been used to
stimulate the bladder and gastrointestinal tract successfully.28,29
Placing the magnetic coil near the lumbosacral region activates
pelvic nerves that facilitate micturition and colonic transit in
patients with SCI.30,31 In unimpaired subjects, FMS of the calf
muscles has also proven useful in improving fibrinolysis.32 In
the sedentary population, FMS may be an attractive option for
abdominal muscle strengthening.
CONCLUSION
Expiratory muscle conditioning was achieved by placing a
magnetic coil along the subject’s lower thoracic spine. A
4-week conditioning protocol resulted in significant improve-
ment in voluntary expiratory pressure, volume, and flow when
compared with baseline. Two weeks after the conclusion of the
FMS conditioning, the voluntary expiratory function decreased
sharply to baseline. For patients with SCI to benefit from the
FMS technology, persistent stimulation is required. FMS of the
expiratory muscles is noninvasive and easy to use. FMS may
be an attractive therapeutic tool for patients with SCI or other
neurologic disorders.
Acknowledgments: The authors thank David Liu, BS, Ellenore
Palmer, MS, PT, Kathie Kim, MPH, RD, and Marilyn Yu, MD, for
their assistance in various stages of this project.
References
1. Linder SH. Functional electrical stimulation to enhance cough in
quadriplegia. Chest 1993;103:166-9.
2. Jaeger RJ, Turba RM, Yarkony GM, Roth EJ. Cough in spinal
cord injured patients: comparison of three methods to produce
cough. Arch Phys Med Rehabil 1993;74:1358-61.
Arch Phys Med Rehabil Vol 82, February 2001
166 MAGNETIC CONDITIONING OF EXPIRATORY MUSCLES, Lin
3. Lin VW, Hsieh C, Hsiao IN, Canfield J. Functional magnetic
stimulation of expiratory muscles: a noninvasive and new method
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Suppliers
a. Dantec MagPro; Dantec Medical Inc, 3 Pearl Ct, Allendale, NJ
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b. SensorMedics Corp, 22705 Savi Ranch Pkwy, Yorba Linda, CA
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