J Appl Physiol 95: 931-937, 2003;
doi:10.1152/japplphysiol.01087.2002
8750-7587/03 $5.00
TRANSLATIONAL PHYSIOLOGY
Noninvasive measurement of the tension-time index in children with neuromuscular disease
Laura T. Mulreany,
Daniel J. Weiner,
Joseph M. McDonough,
Howard B. Panitch, and
Julian L. Allen
Division of Pulmonary Medicine, Children's Hospital of Philadelphia, and
University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
19104
Submitted 27 November 2002
; accepted in final form 2 May 2003
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ABSTRACT
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Respiratory muscle weakness is common in children with neuromuscular
disease (NMD). We hypothesized that weakness puts them at risk for respiratory
muscle fatigue, a harbinger of chronic respiratory failure. We therefore
measured a noninvasive index of respiratory muscle fatigue, the tension-time
index of the respiratory muscles (TTmus), in 11 children with NMD
and 13 control subjects. Spirometric flow rates and maximal inspiratory
pressure were significantly lower in the NMD group than in controls (43
± 23 vs. 99 ± 21 cmH2O, P < 0.001). The
mean TTmus was significantly higher in the NMD group than in
controls (0.205 ± 0.117 vs. 0.054 ± 0.021, P <
0.001). The increase in TTmus was primarily due to an increase in
the ratio of average mean inspiratory pressure to maximal inspiratory
pressure, indicating decreased respiratory muscle strength reserve. We found a
significant correlation between TTmus and the residual
volume-to-total lung capacity ratio (r = 0.504, P = 0.03)
and a negative correlation between TTmus and forced expiratory
volume in 1 s (r = -0.704, P < 0.001). In conclusion,
children with NMD are prone to respiratory muscle fatigue. TTmus
may be useful in assessing tolerance during weaning from mechanical
ventilation, identifying impending respiratory failure, and aiding in the
decision to institute therapies.
respiratory muscles; muscular dystrophy
CHRONIC RESPIRATORY FAILURE may be due to lung (parenchymal)
failure or failure of the respiratory pump. The respiratory pump includes the
centers for control of breathing as well as the chest wall and the muscles of
respiration. Lung failure typical of pneumonia or the adult respiratory
distress syndrome usually results in mixed gas-exchange abnormalities, whereas
pump failure, depending on severity, is predominantly characterized by
hypoventilation and hypercarbia
(13). Pump failure may be
caused by central (respiratory drive) depression, muscle fatigue, or an
imbalance between the respiratory pump and the load placed on it. Patients
with neuromuscular disease (NMD) are at increased risk for pump failure and
premature death due to decreased respiratory muscle strength
(20); it is not clear whether
they may also be at increased risk for respiratory muscle fatigue. Determining
when a patient is imminently at risk for respiratory failure may aid in the
decision to institute therapy for patients with NMD.
The tension-time index (TTI), a dimensionless index relating the force
developed by the respiratory muscles to the time that they are being used, has
been proposed as a measure of respiratory muscle fatigue
(2). TTI is calculated as the
product of two ratios: 1) the ratio of mean inspiratory
transdiaphragmatic pressure (Pdi) to maximal transdiaphragmatic pressure
(Pdimax) and 2) the ratio of inspiratory time
(TI) to respiratory cycle time (TT). Thus TTI =
(Pdi/Pdimax) x (TI/TT). This can be
thought of as a fraction of maximal effort that the diaphragm performs during
its contraction time.
A noninvasive analog of the TTI, termed the tension-time index of the
respiratory muscles (TTmus), has been described. The
TTmus is based on pressure measurements at the mouth and, in
adults, correlates well with the traditional TTI
(18). It is defined by the
following equation: TTmus = (PI/MIP) x
(TI/TT), where PI is mean inspiratory
pressure and MIP is maximal inspiratory pressure measured from functional
residual capacity (FRC). Higher values of TTmus can result from
increased respiratory load, decreased strength in the respiratory pump, or an
imbalance between the two. Increased TTmus is indicative of
respiratory muscle fatigue and, in turn, decreased endurance
(2). Inspiratory resistive
loading increases TTmus as a result of increased PI
(16). Expiratory resistive
loading decreases TTmus because of prolongation of expiratory time
and decreased TI/TT
(21). Patients with increased
intrinsic resistive loads [chronic obstructive pulmonary disease or cystic
fibrosis (CF)] have increased TTmus
(6,
9), presumably because of an
increased numerator in the PI/MIP term. Measurement of
TTmus would be useful in a variety of settings, including guiding
decisions to institute ventilatory support (i.e., predicting respiratory
failure) and assessing a child's tolerance of liberation
("weaning") from mechanical ventilation during recovery.
Several different mechanical defects contribute to impaired pulmonary
function and respiratory failure in patients with NMD. Decreased flow rates
[e.g., forced expiratory volume in 1 s (FEV1)] and lung volumes
[e.g., vital capacity and total lung capacity (TLC)] are due to respiratory
muscle weakness and/or decreased respiratory system compliance. Expiratory
muscle weakness inhibits chest wall distortion to residual volume (RV),
increasing RV as a fraction of TLC (RV/TLC). Patients with NMD would be
expected to be at increased risk for respiratory muscle fatigue due to the
combination of mechanical abnormalities and pump weakness, decreasing the
denominator of the PI/MIP term of the TTmus. We
therefore hypothesized that children with NMD would be predisposed to
development of respiratory muscle fatigue, as assessed by
TTmus.
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MATERIALS AND METHODS
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Subjects. Eleven patients with NMD (8-25 yr of age) were recruited
from the Division of Pulmonary Medicine at The Children's Hospital of
Philadelphia. Representative diseases included Duchenne muscular dystrophy
(DMD), prune belly syndrome, spinal muscular atrophy type II, and nonspecific
muscular dystrophy. These patients were studied while undergoing routine
pulmonary function testing and were clinically stable at the time of
evaluation. They were compared with 13 healthy controls (8-26 yr of age)
recruited from siblings of patients or children of faculty. Subjects were
eligible if they were able to perform spirometric and plethysmographic or
helium-dilution measurements. Informed consent was obtained from parents, and
assent was obtained from children before the study. The protocol was approved
by the Institutional Review Board of The Children's Hospital of
Philadelphia.
Measurements. Spirometry [forced vital capacity (FVC),
FEV1, and midmaximal expiratory flow (FEF25-75%)] and
lung volume measurements (TLC and RV) were performed according to standard
techniques and procedures (1)
(2130 Spirometer, Vmax Series Software, Sensormedics, Yorba Linda, CA). Lung
volumes were measured by plethysmography (V6200 Autobox, Sensormedics) or
helium-dilution techniques (Vmax22 series, Sensormedics)
(1). Maximal respiratory
pressures were measured using the Portaresp (model MRPB028, S & M
Instrument, Doylestown, PA; operating range ±350 cmH2O). MIP
was measured at functional residual capacity (FRC) using the technique of
Black and Hyatt (3). Subjects
generated maximal respiratory efforts while breathing through the mouthpiece
while the nose was occluded. At the distal end of the tube, a small leak
(0.5-1 mm) prevented buccal pressure buildup and glottic closure during
measurements. The occlusion was maintained for 2-3 s. At least five maneuvers
were performed at each starting lung volume until three reproducible values
were obtained, and the highest value was reported. Inadequate maneuvers due to
mouth leak, assessed by observation, were excluded. Pulmonary function testing
results were normalized to height and age using standard reference values
(11,
12).
TTmus. TTmus was derived from
measurements of the occlusion pressure measured at the mouth 100 ms after the
onset of inspiration (P100), MIP measured from FRC, TI,
and TT. Mouth occlusion pressure was measured with a pressure
transducer (model MP-45, Validyne, Northridge, CA; operating range
±22.5 cmH2O). Pressure, flow, and volume signals were
collected using a computerized system developed by the investigators and a
digital signal-processing program (TestPoint, Capital Equipment, Billerica,
MA), which samples mouth pressure and flow at 200 Hz from an analog-to-digital
converter (model KPCMCIA-12AIAO, Keithley, Cleveland, OH). Volume was
calculated by integrating the flow signal from the pneumotachometer (model PNT
3700A, Hans Rudolph, Kansas City, MO), and all three signals were displayed
graphically.
The subjects were asked to breathe quietly, with the nose occluded, through
a mouthpiece connected to the pneumotach with a two-way valve (Hans Rudolph).
During the exhalation phase of breathing, a balloon (model 9300 occlusion
valve, Hans Rudolph) was rapidly inflated in the inspiratory limb of the
breathing circuit to occlude the subsequent inspiratory flow. It was released
150-250 ms after the onset of the subsequent inspiration. The balloon was
inflated with helium from a small gas cylinder, and the valve was controlled
manually with a small switch. The subject was asked to continue to breathe
normally despite the occlusions. After this maneuver was repeated 10-15
times over a period of 3 min, testing was completed. The subject wore
headphones and listened to music to dampen any noise from the switching device
controlling the balloon, lest the subject anticipate the occlusions and change
his or her respiratory pattern. The analysis portion of our computer program
displayed flow, volume, and pressure waveforms and values. A cursor on the
screen was used to identify the onset of inspiration (where pressure crossed 0
cmH2O), and P100 (20 samples) was determined (Figs.
1 and
2). TI and
TT were measured for the breath immediately preceding the occlusion
maneuver.
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Fig. 2. Pressure traces from multiple (n = 12) inspiratory maneuvers in 1
control subject. Initial phase of inspiration after occlusion has a linear
decrease in pressure.
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Calculation of TTmus. PI was
estimated as 5 x P100 x TI
(6) (see APPENDIX).
TTmus was calculated as PI/MIP x
TI/TT. Calculations used the mean values for
P100 and respiratory timing variables. The highest and lowest
values for TTmus (in a given testing session) were excluded from
analysis in calculating mean TTmus.
Anthropometry. Height (measured with a stadiometer, in cm) and
weight (digital standing scale, in kg) were recorded. Arm span was used as a
surrogate for height in wheelchair-dependent subjects. Body mass index (BMI)
was calculated as 10,000 x (wt/ht2). Ideal BMI (for age) was
derived from Center for Disease Control growth charts.
Statistics. Statistical comparisons were performed using SigmaStat
2.03 (SPSS Software). Comparison of continuous variables for NMD patients and
controls was performed using Student's t-test or Mann-Whitney's rank
sum test, where appropriate. Differences were considered significant for
P < 0.05. Relations between variables were quantified using
Spearman's correlation coefficient.
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RESULTS
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Mean anthropometric and pulmonary function data of the NMD and control
groups are presented in Table
1. The clinical characteristics of the NMD patients are described
in Table 2. Scoliosis curvature
(Cobb angle) was measured from an anterior-posterior chest radio-graph within
1 yr of study. There were no significant differences between the groups in
age, weight, height, or percent ideal BMI, although the NMD patients tended to
be lighter and have a lower BMI. The NMD group had significantly lower values
for FVC, FEV1 (% predicted), and FEF25-75% and
significantly higher FEV1/FVC and RV/TLC than controls. The NMD
group tended to have lower TLC, although this difference did not reach
statistical significance.
Mean values for breathing pattern, inspiratory muscle function, and
respiratory mechanics are reported in Table
3. Duty cycle (TI/TT) and calculated
PI were not statistically different between the NMD and control
groups. P100 was significantly higher in the NMD group than in
controls (P = 0.01). The NMD group had significantly lower MIP than
controls (P < 0.001). The calculated values for PI/MIP
and mean TTmus were significantly higher in the NMD group than in
controls (P < 0.001 for both comparisons).
Figure 3 shows the relation
between TI/TT and PI/MIP for the study
subjects. Each isopleth represents a single value of TTmus, with
higher isopleths representing increased likelihood of fatigue or fatigue
potential. In our population, we found a significant correlation between
TTmus and RV/TLC (r = 0.504, P = 0.03) and a
negative correlation between TTmus and FEV1 (r
= -0.704, P < 0.001; Fig.
4). However, when only subjects with NMD were analyzed, these
correlations no longer were statistically significant (P = 0.360 and
0.08, respectively). TTmus was not significantly correlated with
percent ideal BMI (r = 0.347, P = 0.09) or age (r =
0.02, P = 0.908).
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DISCUSSION
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The principal finding of our study is that the noninvasive TTI of the
respiratory muscles is increased in children with NMD compared with healthy
controls. A noninvasive test that is easy to perform clinically, this measure
may be helpful in predicting worsening respiratory muscle fatigue and
impending respiratory failure in patients with NMD. For a patient population
at risk for respiratory failure, the ability to predict such deterioration may
lead to earlier introduction of therapies to prevent or slow the progression
to respiratory failure.
TTI of the diaphragm is a measure of impending respiratory muscle fatigue
that negatively correlates with the time required to develop respiratory
muscle fatigue (Tlim)
(2). In the previously
published values of control subjects, TTI >0.2 was predictive of the
development of respiratory muscle fatigue. Although Tlim is a
measure of respiratory muscle endurance and TTI is a measure of muscle
fatigue, they are complementary values in patients with respiratory muscle
abnormalities. TTI has been studied in adults with chronic obstructive
pulmonary disease, as well as in patients with quadriplegia and chronic
congestive heart failure (14,
17). There have been no
studies assessing TTI in children with NMD.
Methodological considerations. TTI is not ideally suited for use
in children because of the invasive nature of the test, which involves
placement of esophageal and gastric pressure transducers. Gaultier et al.
(6) described the use of
P100 to estimate PI in the context of estimating
inspiratory force reserve in children with obstructive lung disease. Ramonatxo
et al. (18) utilized this
technique to develop the noninvasive TTmus
(18), which was strongly
correlated with TTI (TTmus = 2.0 TTI + 0.024, r = 0.97,
P < 0.001). This technique utilizes the MIP measured at the mouth,
and a PI extrapolated from P100, also measured at the
mouth (6). It has subsequently
been applied to the study of tension-time characteristics of the respiratory
muscles in adults (4,
10,
21,
22) and children
(9). On the basis of the TTI
studies (2), it would be
expected that patients with TTmus >0.4 would develop respiratory
muscle fatigue.
Although MIP is highest when the maneuver is performed from RV
(5,
8), the PI values
are measured during tidal breathing, near FRC, and it is therefore at this
lung volume that the maximal pressures are measured for TTmus
calculation.
It is traditionally assumed that P100 reflects respiratory
drive. In patients with NMD, use of P100 has been preferred over
other measures of drive such as ventilatory response to carbon dioxide,
because it is less dependent on respiratory system mechanics. This preference
arises from the fact that the pressures generated during the P100
maneuver are usually far lower than the maximal pressures that can be produced
by a patient with even severe NMD. For this reason, extrapolation of the
P100 to estimate PI is likely valid in patients with
NMD, inasmuch as the extrapolated pressure (PI) was still well
below the MIP of our patients (Table
3). The higher P100 values in the NMD patients than in
the controls likely reflect increased drive in response to altered respiratory
system mechanics.
Our review of prior studies using TTmus measurements revealed
that the measurement of P100 is not straightforward, inasmuch as
the start of inspiration and pressure 100 ms later may not always be easily
determined from chart recordings of pressure traces. Using a digitally sampled
signal (Fig. 1), we developed a
precise method for measurement of P100, and we defined the start of
inspiration as the initial negative pressure deflection, which may be visually
determined by the pressure wave trace and numerically determined when the
recorded pressure equals zero. By providing a more exact measurement of
P100, this method may be more helpful in comparing small changes in
P100 that can occur with worsening disease or changes in therapy.
Our signal-analysis program also allowed us to confirm that the pressure
decrease during the first 100 ms of inspiration is linear, consistent with the
assumptions underlying the extrapolation of the P100 according to
Ramonatxo et al. (18)
(Fig. 2).
TTmus in disease states. Other
investigators have shown that children with CF
(9) and other obstructive lung
diseases (7) have elevated
TTmus relative to normal controls. This is due primarily to an
increase in the PI/MIP term and, more specifically, to the increase
in PI imposed by the added resistive load of obstructive lung
disease. In these studies, an association between increased TTmus
and decreased lung function (e.g., FEV1) has been shown. Children
with mild CF lung disease had elevated TTmus (0.087 ± 0.030)
compared with healthy controls (0.056 ± 0.014, P < 0.01)
(9). In the control subjects,
values of TTmus were similar to those in our control population.
Children with NMD, in whom respiratory muscle function plays an important role
in sequelae and survival, have not been evaluated using TTmus. Our
findings demonstrated elevated TTmus in children with NMD, a class
of diseases characterized by respiratory muscle weakness and restrictive lung
disease. As in children with CF, this was due nearly entirely to an increase
in the PI/MIP term. However, in contrast to children with CF, the
increase resulted from a decrease in MIP
(Table 3), rather than an
increase in PI. We did not find a correlation between BMI and
TTmus, which had previously been demonstrated for children with CF
(9). This was not surprising,
because the population studied here is affected by disorders influencing
intrinsic muscle strength in ways that may be dissociated from body mass
(e.g., in patients with muscular dystrophy). In addition, when analyzing only
patients with NMD, we did not find a significant correlation between
TTmus and RV/TLC or FEV1. This lack of correlation is
not particularly surprising, because measurement of TTmus
specifically addresses the ability of the respiratory pump to overcome the
imposed load. Standard measures of pulmonary function, such as spirometric
flow rates or lung volumes, may not be sensitive to this balance.
The use of TTmus in evaluating patients with NMD may be
especially informative for several reasons. Most patients with NMD have
weakness that is not limited to the diaphragm. Because TTmus
reflects the contributions of all the inspiratory muscles, measurement of
TTmus may be preferable to measurement of TTI. Although respiratory
muscle strength (MIP) is the most commonly used method to assess NMD patients,
a more integrated analysis that includes breathing pattern, strength, and
mechanical load provides a more thorough assessment of the respiratory
pump.
Our results are consistent with those of Matecki et al.
(15). In their study of 10 DMD
patients (mean age 11.5 ± 1.5 yr) and 10 healthy children (mean age 12
± 1 yr), they measured the maximal time (Tlim) that a fixed
threshold load (35% of the individual's MIP) could be tolerated until
exhaustion. Tlim was significantly shorter in the DMD children
(4.45 ± 1.45 min) than in the controls (>30 min) and seemed to be
reproducible. Such measures of endurance time require adherence to a
challenging protocol, and it remains unclear whether termination of the test
is truly due to muscle fatigue or other reasons. The use of TTmus
integrates assessments of TI/TT, MIP, and
P100 during tidal breathing. Therefore, compared with
Tlim and TTI, TTmus is a simple test for patients to
perform that may be easily incorporated into the clinical setting.
Patients with NMD often adopt a breathing strategy to avoid respiratory
muscle fatigue, such as decreasing TI/TT, to balance the
increased PI/MIP
(2). Although we did not
observe this strategy in our subjects, we have observed tidal breathing below
FRC to allow chest wall recoil to aid in inspiration
(19).
TTmus provides an objective parameter that may predict worsening
respiratory muscle function and impending respiratory failure independently
from routine clinical assessment or traditional pulmonary function
measurements. Earlier recognition of impending respiratory failure would allow
for more timely institution of therapies such as noninvasive ventilation.
Additionally, assessment of other therapies (pharmacological and gene
transfer) for neuromuscular diseases (e.g., spinal muscular atrophy and DMD)
and their effects on respiratory muscle fatigue might be evaluated using
TTmus. Although TTmus was <0.1 in all our control
subjects and >0.1 in nearly all NMD patients, it is unclear at which value
of TTmus respiratory muscle fatigue occurs. Three of our subjects
with TTmus 0.2 were receiving assisted ventilation. Because
they were not studied before they received assisted ventilation, it is unknown
whether their TTmus values were affected by this therapy. Two
subjects with very high TTmus (0.342 and 0.437) were not receiving
assisted ventilation at the time of study but are under consideration for
respiratory muscle support.
In conclusion, we have shown that TTmus is elevated in children
with NMD. Such a measure would be useful for monitoring the progression of
respiratory muscle dysfunction in patients with NMD. Therapeutically,
TTmus may help identify worsening respiratory muscle fatigue and
impending respiratory failure, thereby aiding in the decision to institute
therapies such as mechanical ventilation or respiratory muscle training.
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APPENDIX
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Calculation of PI from P100.
PI was calculated from P100 as follows
(Fig. 5)
If it is assumed that pressure increases linearly from point a
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ACKNOWLEDGMENTS
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The authors gratefully acknowledge the participation of the patients and
control subjects and the assistance of the Pulmonary Function Laboratory of
the Children's Hospital of Philadelphia. We appreciate the efforts of Dr.
Nadav Traeger, Laurie Miske, Eileen Hickey, and Susan Kolb for assistance in
subject recruitment.
L. T. Mulreany is affiliated with the Dept. of Pediatrics, Tripler Army
Medical Center, 1 Jarrett White Rd., Honolulu, HI 96859-5000.
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FOOTNOTES
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Address for reprint requests and other correspondence: J. L. Allen, Div. of
Pulmonary Medicine, Children's Hospital of Philadelphia, 34th St. & Civic
Center Blvd., Philadelphia, PA 19104 (E-mail:
allenj{at}email.chop.edu).
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
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Copyright © 2003 by the American Physiological Society.
TOP
ABSTRACT
MATERIALS AND METHODS
on pressure waveform). 
, Timing measurements, i.e., onset of
inspiration, end of inspiration, and end of exhalation, respectively.
) and neuromuscular disease (NMD) patients
(
). Each isopleth represents an identical product of the ratio of mean
inspiratory pressure to maximal inspiratory pressure (PI/MIP) and
duty cycle (TI/TT, where TI is inspiratory
time and TT is respiratory cycle time). Higher values of
TTmus are associated with increasing likelihood of fatigue.
). For the
entire group, FEV1 was negatively correlated with TTmus
(r = -0.704, P < 0.001), whereas RV/TLC was positively
correlated (r = 0.504, P = 0.03). Lung volume measurements
could not be obtained from all NMD patients.