Introduction

As part of the normative aging process, there is an overall decline in skeletal muscle mass and strength. This decline has also been documented for the muscles of respiration. Prior studies have described a negative association between age and measurements of respiratory muscle strength in older adults [1–8]. These investigations have been largely in the form of cohort studies. Discrepancies among them include differences in the age of onset of decline as well as the degree to which the respiratory muscles weaken. These discrepancies may in part be attributable to methodologic differences in assessing respiratory muscle strength or to uncontrolled variables such as physical activity. As training with nonrespiratory maneuvers has been shown to have a positive effect on the strength of the muscles of respiration [9, 10], we hypothesized that elderly individuals with a greater level of daily physical activity would concomitantly possess greater respiratory muscle strength.

The most commonly used noninvasive means to assess respiratory muscle strength include measurements of maximal static inspiratory pressure (PImax) and maximal static expiratory pressure (PEmax). These maneuvers require significant subject learning and cooperation. Recently, a high degree of correlation has been noted between the maximal transdiaphragmatic pressure (Pdimax) and diaphragm thickness (tdi) in the zone of apposition of the diaphragm to the rib cage as measured via two-dimensional (2-D) ultrasound [11]. Because measurement of tdi via ultrasound is noninvasive and does not require the active cooperation of the subject, it may help to overcome some of the technical barriers to measurement of diaphragmatic strength. We therefore included this measurement as part of our testing.

Methods

Twenty-five volunteers older than age 65 years were enrolled in the study (14 women and 11 men) (Table 1). Because anthropometric data were not available for one subject, only 13 women were included in the final analysis. Subjects were recruited from among 1300 community-dwelling older adults participating in the Study of Exercise and Nutrition in Older Rhode Islanders (SENIOR) physical activity and nutrition investigation. Inclusion criteria for the SENIOR study included age greater than 65 years and residence in one selected community and its immediate environs within the state of Rhode Island. The SENIOR study population was representative of the demographics of the elderly population within this community as a whole [12]. The subjects in the present investigation formed a subset of the larger study. Volunteers were excluded only in the presence of known pulmonary or cardiac disease. The Institutional Review Board at the study site approved the study and informed consent was obtained from all subjects.

Table 1 Anthropomorphic and spirometric data
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Physical Activity Score

Subjects were asked to complete a general health questionnaire and a detailed physical activity questionnaire, the Yale Physical Activity Survey (YPAS) [13]. The YPAS is an interviewer-administered physical activity survey validated for use in older adults. Based on their participation in regular vigorous cardiovascular endurance (aerobic) activity, subjects were assigned to either an active (group 1) or an inactive (group 2) category. Subjects who reported 30 min or more of vigorous physical activity three or more days per week, consistent with the recommendations of the American College of Sports Medicine [14, 15], were classified as active. Those not meeting this criterion were considered inactive.

Lung Volumes, Spirometry, and Pressure Measurements

Forced vital capacity (FVC) and forced expiratory volume in one second (FEV1) were measured using the Collins Medical CPLPF spirometer (Ferraris; Louisville, CO, USA). At least three acceptable maneuvers were performed by each subject until the difference between the largest and the second largest values was less than or equal to 0.150 L [16]. The maximal effort was then recorded. Lung volumes were measured by body plethysmography (Collins Medical BPd; Ferraris). At least three values within a 5% level of agreement were obtained and the mean value recorded [17]. PImax was measured by instructing subjects to forcefully inhale against an occluded mouthpiece for 3 s or more (maximal Mueller maneuver). Inspiratory efforts were initiated from residual volume (RV) [3, 18]. Artifactual measurements of airway opening pressure (Pao) due to buccal muscle use were prevented by a small leak at one end of the mouthpiece [3]. PEmax was measured at total lung capacity (TLC). The subjects were instructed to forcefully exhale against an occluded mouthpiece for 3 s or more (maximal expulsive maneuver). Effort was maximized by providing visual feedback of Pao on an oscilloscope during the Mueller and expulsive maneuvers. The maximal value of PImax and of PEmax following a minimum of six attempts that varied by less than 10% was then recorded [18]. Pressure transducers were calibrated with a water manometer before studying each subject.

Measurements of Diaphragm Thickness

Diaphragm thickness was measured via 2-D B-mode ultrasound at the zone of apposition between the diaphragm and the rib cage. A 7.5-10.0-MHz transducer was applied over the eighth to ninth intercostal space in the right midaxillary line. The diaphragm was visualized as a relatively nonechogenic central muscular layer sandwiched between the peritoneum and the diaphragmatic visceral pleura. The diaphragm was identified immediately superficial to the liver. Images obtained at end-expiration were selected for clarity and parallelism of the three layers. Diaphragm thickness was measured at FRC as the perpendicular distance (to the nearest 0.1 mm) between the superficial edge of the diaphragmatic pleura and the deep edge of the peritoneum. Reproducibility of measurements was approximately 10% [19].

Statistical Analysis

SPSS version 11.0 (SPSS Inc., Chicago, IL, USA) was used for the statistical analyses. Descriptive statistics were derived using the descriptives subroutine. Comparisons of demographic and anthropomorphic data were made using an independent-samples t test. Levine’s test of equal variance was calculated to determine the need for correction of the t test for unequal variances between the groups. Cross tabulations were used to compare gender between groups, and the likelihood ratio and Fisher’s exact test were calculated. Univariate analyses of covariance (ANCOVA) using general linear models were performed to determine whether tdi, PImax, PImax expressed as % predicted, PEmax, and PEmax expressed as % predicted differed between groups. Post-hoc power analyses for the ANCOVA analyses on the primary variable of interest, tdi, was 79%. Power for the secondary variables, PEmax and PImax, were 91% and 62%, respectively.

Results

Thirteen women and 11 men aged 66–84 years were included in the final analysis. Twelve subjects (8 men and 4 women) were classified as active and 12 subjects (3 men and 9 women) were inactive. There were more women than men in the inactive group. However, as depicted in Table 1, there were no significant differences between the active and inactive groups with respect to age (75 ± 5 vs. 73 ± 4 years), height (165.5 ± 9.7 vs. 162.4 ± 12.1 cm), weight (69.1 ± 11.2 vs. 69.9 ± 9.5 kg), BMI (25.1 ± 2.9 vs. 26.6 ± 3.3 kg/m2), FEV1 (91 ± 13 vs. 97 ± 9% predicted), or FVC (91 ± 15 vs. 96 ± 10% predicted).

Measures of respiratory muscle strength were significantly greater in the active group. As shown in Figure 1, expiratory muscle strength in the active group was nearly double that in the inactive group (PEmax [mean ± SD] = 130 ± 44 cmH2O compared to 80 ± 24 cmH2O, p = 0.002). Inspiratory muscle strength was also greater in the active group (PImax = 99 ± 32 cmH2O vs. 75 ± 14 cmH2O, p = 0.03) (Fig. 2). The greater inspiratory muscle strength found in the active group may be related to increased tdi (0.31 ± 0.06 cm vs. 0.25 ± 0.04 cm, p= 0.01), as shown in Figure 3. This assertion is supported by the significant positive association between tdi and PImax (r = 0.43; p = 0.035).

Fig. 1
figure 1

Mean maximal expiratory pressure (PEmax) is indicated by the bars. The standard deviation is shown as the line above the bar

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Fig. 2
figure 2

Mean maximal inspiratory pressure (PImax) is indicated by the bars. The standard deviation is shown as the line above the bar

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Fig. 3
figure 3

Mean diaphragm muscle thickness (tdi) is indicated by the bars. The standard deviation (SD) is shown as the line above the bar

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Because there was a gender difference between the active and inactive groups, we evaluated differences in inspiratory and expiratory muscle strength as % predicted PImax and % predicted PEmax. When performing this gender-corrected analysis, respiratory muscle strength remained significantly greater in the active group for % predicted PImax (p = 0.036) and % predicted PEmax (p = 0.005). To further evaluate the potential effect of gender on strength, ANCOVA was performed, adjusting for gender in each group. This analysis also demonstrated that respiratory muscle strength remained significantly greater in the active group (p = 0.031 for PImax and p= 0.047 for PEmax).

Discussion

With normative aging comes an overall decline in skeletal muscle mass and strength, although this decline is attenuated by regular physical exertion [14]. The underlying etiology of aging-related sarcopenia is unknown but may be related to alterations in one or more of the following: muscle protein metabolism, endocrine system and hormonal milieu, neural control, gene expression, and apoptosis [21]. The majority of evidence to date indicates that this decline does not spare the muscles of respiration [1–8, 22]. Interventions that minimize the loss of respiratory muscle strength in the elderly may be important in reducing morbidity from common respiratory illnesses such as pneumonia and COPD.

In this small cohort of older healthy adults ranging in age from 66 to 84 years, regular exercise was associated with stronger inspiratory and expiratory muscles as well as significantly greater diaphragm muscle thickness. These findings are consistent with the notion that routine engagement in physical activity can increase respiratory muscle mass and strength in the elderly. These adaptations by the respiratory muscles are similar to the increases in quadriceps strength and mass noted in elderly individuals following resistive strength training [23, 24] and suggest that the age-related decline in muscle strength may be attenuated by routine vigorous physical activity.

We postulate that recruitment of the abdominal muscles during nonrespiratory activities may have been the source of the strength training stimulus on the diaphragm and expiratory muscles. When performing maneuvers that raise intra-abdominal pressure, the diaphragm is activated to minimize the transmission of high intra-abominal pressures into the thorax. By minimizing the rise in intrathoracic pressure, adverse hemodynamic consequences of high intrathoracic pressure are averted. Diaphragm recruitment can be seen during nonrespiratory maneuvers involving the upper extremities and trunk, such as lifting or performing situps. The magnitude of Pdi attained during these nonrespiratory maneuvers is dependent on the type of maneuver performed, its intensity, and abdominal compliance. The degree to which Pdi increases during these maneuvers can be great enough to provide a strength training stimulus to the diaphragm. Similarly, the level of intra-abdominal pressures attained during these activities can be high enough to provide a strength-training stimulus to the expiratory abdominal muscles in healthy volunteers [9, 10].

In general, measurements of PEmax assess the strength of the abdominal and expiratory intercostal muscles, and PImax reflects the strength of the diaphragm and inspiratory muscles of the rib cage. If our active elderly subjects routinely engaged in activities that raised intra-abdominal pressure, they would strengthen both the diaphragm and the expiratory abdominal muscles. Our finding of an increase in tdi, PImax, and PEmax in the active elderly group is similar to the finding of increased diaphragm muscle mass in more muscular younger individuals [20, 25] and to the observation that inspiratory and expiratory muscle strength increase in younger healthy individuals following training with biceps curls and situps [10]. Further study with invasive determinations of gastric pressure (Pga), esophageal pressure (Pes), and Pdimax might be helpful in further clarifying the strength-training stimulus in the elderly.

The results of two previous investigations in older adults support our findings. The largest study to date that examined respiratory muscle strength in the elderly was the Cardiovascular Health Study. In that study PImax was measured in 4443 and PEmax in 790 ambulatory adults aged 65 and older. Measurements of PImax correlated not only with age and gender, but with handgrip strength, a measure that correlates well with overall muscle strength [5]. Similarly, the Baltimore Longitudinal Study of Aging investigators found a high degree of correlation between forearm circumference, a surrogate measure of muscle mass, and PImax [8].

The results of our study need to be confirmed by studying a much larger cohort of elderly individuals. Because there were more men in the active group, it might be postulated that some of our results might be related to this gender difference between the subjects of the two groups. However, given that PImax and PEmax remained significantly greater in the active group when the analyses were adjusted for gender as well as when expressed as % predicted, it is unlikely that gender could explain the differences between the two groups.

We conclude that general exercise in the elderly is associated with an increase in diaphragm thickness. It has been shown that cardiovascular and resistance exercise as well as specific respiratory muscle training is beneficial in patients with respiratory disease [26, 27]. The results of the present study support the postulate that an overall greater level of activity and generalized exercise may be beneficial in maintaining muscle mass and perhaps diaphragm strength in the elderly.