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Effects of The Aging Process On Respiratory Function

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Clinical Section

Gerontology 2009;55:505510
DOI: 10.1159/000235853

Received: September 20, 2007


Accepted: July 1, 2008
Published online: August 27, 2009

Effects of the Aging Process on


Respiratory Function
Raquel Rodrigues Britto Camila Camargos Zampa Tatiana Antunes de Oliveira
Lvia Fontes Prado Vernica Franco Parreira
Department of Physical Therapy, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil

Key Words
Plethysmography Respiratory function Aging

Abstract
Background: The identification of breathing patterns in
healthy elderly individuals and changes in the respiratory
system related to the normal aging process is important to
detect and prevent respiratory dysfunction. Objectives: To
assess and compare respiratory function between adults
and elderly individuals according to baseline conditions.
Methods: Nineteen adults aged 2059 years (group 1), 12
elderly aged 6069 years (group 2) and 12 elderly above 69
years of age (group 3) who were all nonsmokers, untrained
and with normal pulmonary function tests were studied using calibrated respiratory inductive plethysmography to assess tidal volume (Vt), respiratory frequency (f ), minute ventilation, mean inspiratory flow [Vt/inspiratory time (Ti)],
inspiratory duty cycle (Ti/total cycle time), labored breathing
index (an asynchrony index measurement), percentage of
rib cage motion and abdominal motion. Measurements of
the maximal inspiratory pressure (MIP), maximal expiratory
pressure and transcutaneous oxygen saturation were also
obtained. Results: The MIP was statistically significantly lower in group 2 (54.58 8 32.37 cm H2O) and group 3 (54.58 8
33.61 cm H2O) compared to group 1 (92.11 8 43.22 cm H2O;
p = 0.037). There were no significant differences between
the groups regarding breathing patterns, respiratory variables and thoracoabdominal motion. No statistically signifi-

2009 S. Karger AG, Basel


0304324X/09/05550505$26.00/0
Fax +41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com

Accessible online at:


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cant differences between groups 2 and 3 were found for any


of the investigated variables. Conclusion: These findings
suggest that the aging process of the respiratory system reduces the inspiratory muscle strength but does not have a
significant impact on breathing pattern variables.
Copyright 2009 S. Karger AG, Basel

Introduction

The aging process is characterized by physiological


changes which compromise several organs and systems,
leading to impairment of their functions. The respiratory
system can undergo anatomical and functional modifications that are inherent to the normal aging process, although they might vary in amplitude [13]. Knowledge
regarding these changes and identification of the breathing patterns of healthy elderly individuals are important
to detect and prevent respiratory dysfunction and to contribute to the elaboration of intervention protocols.
The physiological changes in pulmonary function in
the elderly include changes in the lungs, rib cage, respiratory muscles and respiratory drive, characterized by decreases in elastic recoil of the lung, chest wall compliance,
respiratory muscle strength and response to hypoxemia
and hypercapnia [1, 2, 47]. In healthy individuals, these
changes are more evident when they are about 80 years
old, in spite of being present since the age of 50 years [3].

Raquel Rodrigues Britto, PT, PhD


Departamento de Fisioterapia, Universidade Federal de Minas Gerais
Av. Antnio Carlos, 6627, Pampulha
Belo Horizonte, Minas Gerais 31 270 901 (Brazil)
Tel./Fax +55 31 3499 4783, E-Mail rbrito@ufmg.br

In senile lungs, there are decreases in the number of


elastic fibers [1, 2, 6, 7], in the elastic recoil of the lungs as
well as an increase in the air flow resistance, which lead
to progressive air trapping and cause increases in the lung
parenchyma compliance [13, 68].
The main physiological changes of the aging process
related to the thoracic cage consist of a decrease in dynamic compliance [13, 6, 7], which is related to costal
cartilage calcification, the costovertebral joints and decreases in the intervertebral spaces [13, 6]. The structural changes that occur in the thoracic wall promote alterations in the posture and respiratory efforts of elderly
people [2].
In addition to the changes in the lung parenchyma and
thoracic cage, the respiratory muscles also undergo modifications with aging [13]. These modifications include
decreases in the size and number of muscle fibers and in
the capacity of the neuromuscular junctions to transmit
nervous impulses, loss of peripheral motor neurons and
reduction of the muscular work capacity, which together
can reduce muscular strength [1, 2, 6, 7, 9, 10]. Tolep et al.
[11] and Polkey et al. [12] showed decreases of 1325% in
the strength of the diaphragm in elderly subjects [2]. Respiratory muscular strength can be assessed using static
measures which correspond to the maximal respiratory
pressures [9, 10, 13].
The aging process is also characterized by changes in
the respiratory drive [1, 2, 5, 6]. With increases in age,
there is a reduction of the central nervous activity and of
the neuronal impulses to the respiratory muscles which
decrease the response to hypoxemia and hypercapnia [1,
2, 57].
Although a range of aspects of the aging of the respiratory system have been well defined in the literature, there
are parameters provided by respiratory inductive plethysmography that have not been thoroughly investigated.
Studies that have evaluated pulmonary function in elderly
subjects have commonly employed static spirometry [14].
Meta-analysis has shown that few studies approached
the dynamics of breathing through the assessment of the
thoracoabdominal configuration [2, 6, 7]. Amongst them,
Tobin et al. [15] and Verschakelen and Demedts [16] used
plethysmography during baseline breathing and demonstrated that the effects of age were not significant. Britto
et al. [17] did not find statistically significant differences
with regard to respiratory variables when elderly subjects
(66 8 5 years) were compared to adults. The evaluation
of breathing patterns and thoracoabdominal configuration of the older elderly is important to distinguish the
patterns related to the physiological aging process from
506

Gerontology 2009;55:505510

those related to diseases that could compromise respiratory function.


Therefore, the aims of this study were to assess and
compare the respiratory function of adults (2059 years),
elderly aged 6069 years and elderly aged more than 69
years in baseline conditions through analyses of thoracoabdominal motion and respiratory muscle strength.

Materials and Methods


Subjects
The elderly were recruited from the outpatient clinic of the
Geriatric Department of the Universidade Federal de Minas
Gerais, Brazil, and the adults from among staff and students at
the same university. The following inclusion criteria were adopted: age between 20 and 59 years (group 1), between 60 and 69 years
(group 2) or above 69 years (group 3); nonsmokers [15, 18]; untrained [2, 19]; body mass index lower than 35 [20]; normal pulmonary function tests (Vitalograph 2120, Vitalograph Ltd., Buckingham, UK) according to the Global Initiative for Chronic Obstructive Lung Disease (update 2005) [9, 13, 18, 19, 21, 22]; no
treatment with medications that could interfere with evaluations,
such as beta-blockers, muscular relaxants, steroids and tranquilizers [21], and clinical stability (no hospitalization, no active infectious diseases and no flu or cough exacerbation) 3 weeks before
the tests [21]. The exclusion criteria were: cognitive deficits (MiniMental State Examination score below 18 for illiterate elderly and
24 for literate subjects) [23]; unstable arterial pressure (systolic
pressure above 130 mm Hg and diastolic pressure above 85 mm
Hg with or without medication) [21, 24]; unstable angina pectoris
[21]; history of stroke; recent myocardial infarction, neuromuscular disease, cutaneous indication of edema or dehydration [21], or
difficulties in understanding and executing the study tests.
The institutional ethics committee approved the study protocol, and all participants provided informed consent.
Instruments and Recorded Signs
Measurements of maximal inspiratory pressure (MIP) and
maximal expiratory pressure (MEP) were obtained using a manovacuometer with an operational interval of +300 to 300 cm H2O
(Gerar, Brazil).
Calibrated respiratory inductive plethysmography (Respitrace, NIMS, Miami, Fla., USA) was used to assess pulmonary
ventilation through the changes in the transverse sectional area
of the thorax and abdomen. The changes in the cross-sectional
area of the rib cage and abdominal compartments were assessed
using 2 coils of Teflon-insulated wire covered with an elastic
band. One coil was positioned on the rib cage, in the axial line,
and the other encircled the abdomen in the umbilical line. For
data acquisition, the coils were connected to the Respitrace equipment by 2 cables, which showed 3 curves, 2 corresponding to the
movement of each compartment (rib cage and abdomen) and the
other corresponding to the total signs [15, 25].
The calibration of the tidal volume was performed during
5 min of quiet breathing, using software (RespiPanel 4.0, NIMS)
and a specific procedure, qualitative diagnostic calibration, to
equilibrate the electric gains of the channels related to the rib cage

Britto/Zampa/de Oliveira/Prado/Parreira

and abdomen. Then, the participant breathed through a mouthpiece into a previously calibrated spirometer (Vitatrace VT 130,
Pro Mdico, Rio de Janeiro, Brazil) with the nose occluded by a
nasal clip during a period of 3060 s. Electric signals sent from
the spirometer to the computer were used to calibrate the total
signal (tidal volume) of the respiratory inductive plethysmography to the absolute volume in milliliters [26].
Procedures
Initially, all participants were interviewed to investigate their
histories of respiratory disease, followed by a clinical assessment
including the measurement of blood pressure using a sphygmomanometer (BD), heart rate (HR) and transcutaneous oxygen
saturation (SpO2) using pulse oximetry (Datex-Ohmeda, Louisville, Colo., USA), and weight and height using a calibrated balance (Filizola Ind. Ltda, Brazil). Then, the pulmonary function
tests were carried out (Vitalograph 2120, Vitalograph). For the
elderly subjects, the Mini-Mental State Examination was applied
to investigate their cognitive condition [23].
In a second session, measurements of MIP and MEP were obtained. First of all, 2 learning maneuvers were performed [21], and
after that, a minimum of 3 measurements was collected. The assessment was considered complete when the subject performed 3
acceptable measurements and at least 2 of them were reproducible. The last measurement could not be higher than the others
[10]. Maneuvers without air leak that could be maintained for at
least 1 s and measurements with variation equal to or lower than
10% of the higher value were considerate acceptable and reproducible [10]. There was an interval of about 1 min between the
maneuvers, and the higher value was selected for analysis [10].
The participants expired in the mouthpiece into residual volume
and, after that, performed a maximal inspiratory effort against an
occluded airway to provide the MIP measurements [10]. To evaluate the MEP, the participants inspired in the mouthpiece up to
their total pulmonary capacity and, after that, a maximal expiratory effort was performed against an occluded airway [10]. During this last maneuver, the participants held their cheeks with
their hands to prevent the occurrence of oral leaks [10]. The same
researcher always performed the procedures.
Finally, to allow pulmonary ventilation assessment by respiratory inductive plethysmography, the participants were placed
comfortably in the supine position on a clinical exam table, with
0 trunk inclination. The subjects were instructed to breathe
calmly, not to move any body segment, not to talk and not to sleep
until the end of the recordings. After the calibration procedure,
data were recorded for about 10 min for each individual with quiet breathing. The variables were obtained with a digital acquisition system (RespiEvents 5.2, NIMS). An interval of 1 min of a
stable respiratory pattern was selected for analysis after the initial
5 min of recording, considered the time necessary for stabilization of the breathing pattern.

(Ti)], inspiratory duty cycle [Ti/total cycle time (Ttot)], labored


breathing index (LBI; an asynchrony index measurement), percentage of rib cage motion (RC%) and abdominal motion (AB%).
The sum of RC% and AB% was considered to be 100%.
SpO2 and HR were measured after 5 min of recording using
pulse oximetry (Datex-Ohmeda).
Statistical Analysis
Descriptive statistics and tests for normality were calculated
for all outcome variables, using the software SPSS 10.1 for Windows (SPSS Inc., Chicago, Ill., USA). Depending on the data distribution, one-way ANOVA followed by Scheffe post hoc or Kruskal-Wallis tests were employed to investigate differences between
the groups, with a significance level of ! 0.05. Based on the results of previous studies [10, 17] considering the power of 80% and
an of 0.05, a sample size of 12 individuals for each group was
estimated to be necessary to detect differences of 35 mm Hg in
MIP and MEP and 16 individuals for each group to detect differences of 100 ml in Vt.

Results

Variables Measured
For pulmonary function tests, the following variables were
measured: forced vital capacity (FVC), forced expiratory volume
in 1 s (FEV1) and FEV1/FVC. For each respiratory cycle, the following breathing pattern and thoracoabdominal motion variables were assessed using calibrated respiratory inductive plethysmography: tidal volume (Vt), respiratory frequency ( f ), minute
ventilation (VE), mean inspiratory flow [Vt/inspiratory time

Out of the 49 subjects evaluated (group 1: 20 adults;


group 2: 13 elderly; group 3: 16 older elderly), 6 were excluded (1 from group 1, 1 from group 2 and 4 from group
3) because of their inability to perform the pulmonary
function tests or evidence of obstructive or restrictive
pulmonary diseases. Therefore, the study was completed
by 43 subjects: 19 in group 1 (8 men and 11 women), 12
in group 2 (6 men and 6 women) and 12 in group 3 (5 men
and 7 women). The subjects in group 1 did not report any
medical problems; in group 2, there were 2 subjects with
controlled hypertension, 2 with knee osteoarthritis and 3
with labyrinthitis, and in group 3, there were 2 individuals with diabetes, 6 with controlled hypertension, 1 with
Chagas disease and a pacemaker, 2 with rheumatoid arthritis and 4 with knee osteoarthritis. Table 1 gives the
demographic and anthropometric data of the 3 groups.
Based on the plethysmography, a total of 737 respiratory cycles were evaluated: 328 cycles in group 1, with an
average of 17.26 8 4.98 cycles per subject; 208 cycles in
group 2, with an average of 17.33 8 2.31 cycles per subject, and 201 cycles in group 3, with an average of 17.00
8 3.25 cycles per subject.
Table 2 shows the means and standard deviations of
the plethysmography and spirometry results. The variables VE, Vt, f, Ti/Ttot, Vt/Ti, AB%, RC%, FVC, FEV1 and
FEV1/FVC were similar between the groups. The asynchrony (LBI) was higher in group 2 than in group 1 (p =
0.01).
As illustrated in figure 1, the mean MEP value of
group 1 (107.37 8 39.59 cm H2O) was not significantly

Respiratory Function and Aging Process

Gerontology 2009;55:505510

507

Table 1. Subject characteristics

160

Men
Women
Age, years
Women (range)
Men (range)
Age, mean 8 SD
BMI

Group 2
(n = 12)

8
11

Group 3
(n = 12)

6
6

2255
2455
35.89811.28
23.7883.66

5
7

6366
6068
64.5082.71
27.1282.97

140
120
MEP (cm H2O)

Group 1
(n = 19)

80
60
40

7587
7388
77.6785.00
27.7383.94

Group 1: 2059 years old; group 2: 6069 years old; group 3:


above 69 years old. BMI = Body mass index.

100

20
0
Group
1

Group
2

Group
3

Fig. 1. Means and standard deviations of MEP values. Group 1:


2059 years old; group 2: 6069 years old; group 3: above 69 years
old. No significant differences between groups were found.

Table 2. Variables evaluated by plethysmography and spirome-

try

160
140

Group 2
(n = 12)

Group 3
(n = 12)

VE, liters/min
4.9281.57
4.4981.37
4.9981.61
Vt, ml
353.838209.91 282.40889.06 332.658128.61
f, bpm
15.7384.79
16.0782.36
15.5983.43
Ti/Ttot
0.3980.01
0.3680.001
0.3880.001
Vt/Ti, ml/s
208.03863.61 205.72860.23 214.98865.82
AB%
64.91813.70
66.60818.18 65.37816.21
RC%
35.08813.70
33.39818.18 34.62816.21
LBI
1.0980.01
1.1480.01
1.1980.01*
FVC, % pred
3.8180.84
3.0781.04
2.5680.68
FEV1, % pred
3.2280.77
2.3480.76
1.9880.62
FEV1/FVC
% pred
84.3285.71
76.5083.04
77.2587.97
Group 1: 2059 years old; group 2: 6069 years old; group 3:
above 69 years old. pred = Predicted.
* p < 0.05 compared to group 1.

different from that of group 2 (102.08 8 47.89 cm H2O)


and group 3 (87.92 8 59.71 cm H2O). However, as shown
in figure 2, the MIP values were lower in group 2 (54.58
8 32.37 cm H2O; p = 0.037) and group 3 (54.58 8 33.61
cm H2O; p = 0.037) compared to group 1 (92.11 8 43.22
cm H2O).
The SpO2 values were lower in the elderly groups 2
(95.25 8 2.22%; p = 0.040) and 3 (94.90 8 1.52%; p =
0.040) compared to the adults (group 1: 96.95 8 0.84%).
No statistically significant differences were found between the groups with regard to the resting HR (fig. 3).
508

Gerontology 2009;55:505510

120
MIP (cm H2O)

Group 1
(n = 19)

100
80

Group
2

Group
3

60
40
20
0
Group
1

Fig. 2. Means and standard deviations of MIP values. Group 1:

2059 years old; group 2: 6069 years old; group 3: above 69 years
old. * p ! 0.05 compared to group 1.

Discussion

This study assessed the respiratory function of healthy


adults, elderly people aged between 60 and 69 years and
elderly people more than 69 years old through respiratory inductive plethysmography, pulse oximetry and
measurements of maximal respiratory pressures. The results showed that there were no statistically significant
differences between the groups in relation to the breathing pattern and the thoracoabdominal motion variables
and that the MIP was lower in the elderly groups.
Regarding the plethysmography variables VE, Vt, f, Ti/
Ttot and Vt/Ti, the results of this study were similar to
those of Tobin et al. [15] and Britto et al. [17], who also
used respiratory inductive plethysmography to evaluate
Britto/Zampa/de Oliveira/Prado/Parreira

healthy individuals in baseline conditions. Tobin et al.


[15] studied the breathing patterns of 47 adults (22.6 8
5.3 years) and 18 elderly subjects (68.9 8 6.5 years) in the
supine position. Britto et al. [17] assessed the respiratory
variables of 19 adults (24 8 3 years) and 18 elderly subjects
(66 8 5 years) with a 30 recumbency angle. They did not
observe statistically significant differences between adults
and elderly subjects. However, in these previous 2 studies,
the age of the elderly subjects was less than 75 years. Other previous studies found more evident changes in respiratory function in elderly subjects of about 80 years, but
not using the plethysmography system [3]. In the present
study, the mean age of the subjects in group 3 was about
78 years, and the number of subjects was less than the estimated necessary sample size for this variable. Therefore,
future studies with older subjects and a larger sample size
are required to confirm this evidence.
AB% was predominant over RC% in all groups, without differences between them. Tobin et al. [15] and Verschakelen and Demedts [16], using plethysmography, also
observed predominance of the abdominal compartment
in adults and elderly subjects assessed in baseline conditions in the supine position. Likewise, Britto et al. [17]
also found more movement of the abdominal compartment than of the rib cage in adults and elderly individuals
at a 30 recumbency angle. These observations help to
confirm the physiological action of the diaphragm and
the abdominal muscles as major inspiratory and expiratory muscles, respectively.
The higher LBI values found in group 2 indicated more
asynchronism in this group, although without clinical implications. The LBI is an index of the work performed dur-

ing 1 respiratory cycle that takes into consideration the


phase and amplitude of RC% and AB%. Perfect thoracoabdominal coordination produces an LBI of 1.0, and values
below 1.2 are considered normal [27]. Higher LBI values
indicate asynchrony, and in patients with chronic obstructive pulmonary disease, they are associated with the severity of the disease and lower prognosis [28, 29]. We found no
studies that investigated this variable in healthy subjects.
The reduction of MIP observed in both elderly groups
has also been reported previously [10]. Neder et al. [10]
evaluated the maximal respiratory pressures and maximal voluntary ventilation in 100 individuals of 2080
years and found negative correlations between age and
these variables. Enright et al. [18], in an observational
study involving 4,443 elderly of 65 years or more, also
observed negative correlations between age and maximal
respiratory pressures. They also reported that the average
was lower in the elderly over 80 years when compared to
the elderly of 6579 years. However, in the present study,
no statistically significant differences were observed between the 2 elderly groups, probably because the mean
age of the oldest group was 78 years. The decreases in
MIP and MEP values could be related to the gradual reduction in mass and muscle strength due to sarcopenia
in the aging process [30]. The absence of a significant difference for MEP could be related to the higher standard
deviation found in the present study, in comparison with
those of Neder et al. [10], who used to calculate the sample
size which resulted in a power of 40%. Poor respiratory
muscle strength may lead to reduced exercise tolerance
[2], contribute to physiological decline and accelerate the
reduction in respiratory function in the presence of common illnesses such as pneumonia, chronic obstructive respiratory disease and neuromuscular diseases.
Regular exercise may attenuate the age-related decline
in respiratory muscle strength, since greater diaphragm
thickness was found in the active elderly [31]. A pilot study
indicated that 8 weeks of specific inspiratory muscle training improved the time to exhaustion during a fixed workload endurance test [32]. However, whether such exercise
improves the functional capacity is still controversial.
SpO2, measured by pulse oximetry, reflects arterial
hemoglobin oxygen saturation [33], and an acceptable
value for this parameter is above 94% [34]. Despite the
statistically significant differences found in the present
study, these data may not have clinical significance, since
the elderly demonstrated SpO2 values within normal limits. The average HR values for all groups were also within
the limits of normality (6080 bpm) proposed for individuals during quiet breathing [35].

Respiratory Function and Aging Process

Gerontology 2009;55:505510

120

HR (bpm)

100
80
60
40
20
0
Group
1

Group
2

Group
3

Fig. 3. Means and standard deviations of HR values. Group 1:

2059 years old; group 2: 6069 years old; group 3: above 69 years
old. No statistically significant differences between groups were
found.

509

Despite the limitation related to the small sample size,


the findings from the present pilot and explorative study
may contribute to enhancing knowledge about breathing
patterns of adults and elderly assessed in normal conditions. The present values could be used as a reference for
future studies, thus contributing to a better characterization of the respiratory function of elderly people.
In conclusion, discreet differences in respiratory patterns and thoracoabdominal motion were found between
healthy adults and elderly subjects, suggesting that the
aging process on the respiratory system did not cause a
significant impact on the breathing patterns of the inves-

tigated sample. On the other hand, the present results did


show that the aging process produces significant reduction of the strength of the inspiratory muscles. Studies
with a larger number of subjects are necessary to confirm
the effects of the aging process on respiratory function.

Acknowledgements
This study was supported by the National Council of Scientific and Technologic Development (CNPq) and the Coordination
for the Improvement of Higher Education Personnel of Brazil
(CAPES).

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