Archives of Gerontology and Geriatrics 89 (2020) 104082

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Archives of Gerontology and Geriatrics

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Respiratory muscle strength for discriminating frailty in community- T

dwelling elderly: a cross-sectional study
Marcela B. Vidal, Maycon S. Pegorari*, Elinaldo C. Santos, Areolino P. Matos,
Ana Carolina P.N. Pinto, Daniela G. Ohara
Department of Biological and Health Sciences, Federal University of Amapá, Macapá, Amapá, Brazil

ARTICLE INFO ABSTRACT

Keywords: Objectives: To compare obtained and predicted inspiratory and expiratory muscle strength between frail, pre-
Frailty frail, and non-frail older people; to examine the association between inspiratory and expiratory muscle strength
Respiratory muscles and frailty in older people; and to determine cut-off points for inspiratory and expiratory muscle strength for
Muscle strength discriminating frailty in older people.
Aged
Methods: A cross-sectional study was conducted with 379 community-dwelling older adults. Frailty was assessed
Maximal respiratory pressures
using Fried’s phenotype, while inspiratory and expiratory muscle strength were measured with maximum in-
spiratory and maximum expiratory pressures. Inferential analyses were performed using paired Student t-tests,
one-way analysis of variance (ANOVA) tests, and a multinomial logistic regression model. ROC curves were
constructed to establish cut-off points of maximum inspiratory and expiratory pressures for discriminating frailty
and pre-frailty.
Results: Frail and pre-frail participants presented significantly lower mean inspiratory and expiratory pressures
compared to non-frail participants; values were significantly lower than predicted. Inspiratory and expiratory
muscle strength were inversely associated with frailty and pre-frailty. Cut-off points ≥-50cmH2O and
≤60cmH2O for maximum inspiratory and expiratory pressures, respectively, were established as optimal dis-
criminators of frailty. The cut-off point ≤65cmH2O for maximum expiratory pressure was established as a
discriminant for the presence of pre-frailty.
Conclusions: Inspiratory and expiratory muscle strength were lower in frail than in pre-frail older adults, and
lower in pre-frail than in non-frail peers. Frailty and pre-frailty were inversely associated with inspiratory and
expiratory muscle strength. Cut-off points for inspiratory and expiratory muscle strength may be useful in
clinical practice for discriminating frailty and pre-frailty in older adults.

1. Introduction
Frailty is defined by the World Health Organization as, “a clinically
recognizable state in which the ability of older people to cope with
every day or acute stressors is compromised by an increased vulner-
ability brought by age-associated declines in physiological reserve and
function across multiple organ systems” (World Health Organization,
2017). Frail older adults are more susceptible to falls, fractures, phy-
sical disability, dependency, hospitalizations, and death (Vermeiren
et al., 2016).
The prevalence of frailty is high in older adults and increases with
age. Approximately 10.7% of community-dwelling adults older than 65
years and 26.1% of those older than 85 years are frail (Collard, Boter,
Schoevers, & Oude Voshaar, 2012). Given the rapid increase in life
expectancy worldwide, frailty is, without question, one of the most
serious public health challenges to be faced in the upcoming years
(Dent et al., 2019). Accurate and early identification of frail individuals
can inform clinical decision-making and help formulate treatment goals
and recovery expectations (Rajabali, Rolfson, & Bagshaw, 2016).
Several methods of measuring frailty are currently in use, but a
consensus surrounding the most appropriate clinical measurement has
not yet been reached (Dent, Kowal, & Hoogendijk, 2016). Fried’s phe-
notype method (Fried et al., 2001) and Rockwood and Mitnitski frailty
index (Mitnitski, Mogilner, & Rockwood, 2001) are currently the most-
used frailty assessment tools (Dent et al., 2016).
Although these two measures (Fried et al., 2001; Mitnitski et al.,

⁎
Corresponding author at: Federal University of Amapá, Department of Biological and Health Sciences, Physical Therapy Course, Road Juscelino Kubitschek, Km –
02, Jardim Marco Zero, Macapá, AP, CEP 68903-419, Brazil.
E-mail address: mayconpegorari@yahoo.com.br (M.S. Pegorari).

https://doi.org/10.1016/j.archger.2020.104082
Received 23 January 2020; Received in revised form 24 March 2020; Accepted 14 April 2020
Available online 20 April 2020
0167-4943/ © 2020 Elsevier B.V. All rights reserved.
M.B. Vidal, et al.
2001) are relatively well recognized, recent studies have suggested that
parameters not covered by current indices may also be associated with
frailty, such as those related to respiratory system function. In 2012,
Vaz Fragoso et al. identified that frailty and pre-frailty were associated
with airflow limitation and a restrictive breathing pattern (Vaz Fragoso,
Enright, McAvay, Van Ness, & Gill, 2012). In the following year, Pe-
gorari, Ruas, and Patrizzi (Pegorari, Ruas, & Patrizzi, 2013) and later,
Parentoni et al. (Parentoni et al., 2013) found that frail community-
dwelling older people had significantly lower inspiratory and ex-
piratory muscle strength than their non-frail peers. Pegorari, Ruas, and
Patrizzi add that inspiratory and expiratory muscle strength were lower
in frail older adults than in their pre-frail and non-frail peers, suggesting
that respiratory muscle strength decreases as the severity of frailty in-
creases (Pegorari et al., 2013). Nevertheless, these previous studies
(Parentoni et al., 2013; Pegorari et al., 2013) used small sample sizes
and did not specifically clarify whether respiratory muscle strength
assessments could discriminate frailty in older adults. Thus, this current
study aimed to compare obtained and predicted inspiratory and ex-
piratory muscle strength between frail, pre-frail, and non-frail com-
munity-dwelling older adults; verify the association of inspiratory and
expiratory muscle strength with frailty; and determine cut-off points for
inspiratory and expiratory muscle strength for discriminating frailty in
this same population.
2. Methods
2.1. Study design and sample
Community-dwelling older adults were recruited in 2017 in
Macapá, Brazil, to participate in this cross-sectional study. Individuals
aged 60 years or older who were ambulatory (with or without walking
assistance devices) were included. Individuals were excluded if they
had any medical conditions contraindicated for assessing respiratory
muscle strength, specifically: neurological sequelae, acute myocardial
infarction, recent unstable angina, aortic aneurysm, abdominal hernias,
middle ear disorders, glaucoma or retinal detachment, facial paralysis,
or uncontrolled hypertension. Individuals were also excluded if they
refused to participate in any of the stages of the study, moved out of
town, were hospitalized, were not located after three attempts, were
unable to answer interview questions, unable to perform the tests, or
presented cognitive decline. A Mini-Mental State Examination was used
to screen all possible participants for cognitive decline. The translated
version of the Mini-Mental Examination validated for use in Brazil was
used (Bertolucci, Brucki, Campacci, & Juliano, 1994), which adjusts the
cut-off point for the patient’s level of schooling. The MMSE has a total
score ranging from 0 to 30 points, and the cutoff points for cognitive
decline in the elderly are adjusted for level of education. Cognitive
decline is defined as below 13 points for illiterate, 18 points for in-
dividuals with 1 to 11 years of education, and 26 points for individuals
with more than 11 years of education (Bertolucci et al., 1994).
In 2010, 5.21% of the population living in the urban area of Macapá
were aged 60 years or older (Instituto Brasileiro de Geografia e
Estatística, 2010). For the sample size calculation, an assumption of a
prevalence of 50% of health problems among the urban elderly popu-
lation, and an accuracy of 5% and a confidence interval of 95% were
set. A minimum sample of 377 individuals was found to be necessary to
be representative of the study population. The research team carried
out a two-stage cluster sampling process by first sampling government-
defined pre-established census tracts and then subsequently identifying
residences with older adults.
This study was approved by the Ethics Committee of the Federal
University of Amapá. All individuals signed informed consent before
commencing their participation. Select data from this study has been
previously analyzed and published (Ohara et al., 2018, 2019).
2
Archives of Gerontology and Geriatrics 89 (2020) 104082
2.2. Data collection instruments and measures
2.2.1. Respiratory muscle strength (independent variable)
The maximum inspiratory and expiratory pressures were obtained
using a Wika (WIKA, Ind, Ipero, SP, Brazil) manovacuometer to esti-
mate the inspiratory and expiratory muscle strength. Maximum in-
spiratory pressure was obtained from residual volume and maximum
expiratory pressure from total lung capacity (Neder, Andreoni, Lerario,
& Nery, 1999). The tests were performed with the participant in a se-
ated position (American Thoracic Society/European Respiratory, S.,
2002) while wearing nasal clips and a rigid, plastic mouthpiece (Neder
et al., 1999). The maneuvers were executed between three and five
times, with the highest value being used for analysis (Neder et al.,
1999). The assessment was considered valid if three acceptable and two
reproducible measures were obtained (Neder et al., 1999). A measure
was considered acceptable if the pressure was sustained for at least one
second and reproducible if the variation of the values was below 10%
(Neder et al., 1999).
2.2.2. Frailty phenotype (dependent variable)
The presence of frailty was assessed with the following five com-
ponents, as proposed by Fried et al. (Fried et al., 2001).
1 Unintentional weight loss: Assessed with the following question: “In
the last year, have you lost more than 4.5 kg unintentionally (i.e.,
not due to dieting or exercise)?” The weight loss criterion was ful-
filled if the answer was affirmative.
2 Self-reported fatigue: Operationalized as the two items of the
Brazilian version of the Center for Epidemiological Studies (CES-D)
Scale: (Batistoni, Neri, & Cupertino, 2007) First item: “I felt that
everything I did was an effort.” Second item: “I could not get going.”
The answers were obtained using a Likert scale, with 0 = rarely or
never, 1 = sometimes, 2 = frequently, or 3 = all of the time.
Participants who answered “2” or “3” to either of these items ful-
filled the self-reported fatigue criterion.
3 Decreased handgrip strength: Measured with an SH5001 – 973
(SAEHAN, Yangdeck – Dong, Korea) manual hydraulic dynam-
ometer. The test procedure followed the recommendations of the
American Society of Hand Therapists (ASHT) (MacDermid,
Solomon, Fedorczyk, & Valdes, 2015) and the cut-off values, ad-
justed for gender and body mass index, proposed by Fried et al.
(Fried et al., 2001).
4 Low level of physical activity: Assessed with the elderly-adapted long
version of the International Physical Activity Questionnaire (IPAQ)
(Benedetti, Mazo, & de Barros, 2004). The recommendations used
were those of the American College of Sports Medicine and Amer-
ican Heart Association (Pate et al., 1995) to classify levels of phy-
sical activity.
5 Slowed walking speed: Operationalized as the time spent to walk 4.6
meters at a usual pace. The cut-off points proposed by Fried et al.
(Fried et al., 2001), adjusted for gender and height, were adopted.
Participants that fulfilled three or more among the five components
were considered frail. Those who filled one or two components were
classified as pre-frail, and those who had none of these components
were considered not frail.
2.3. Data Analysis
Descriptive analysis was performed with means, standard devia-
tions, percentages, and frequencies. One-way analysis of variance
(ANOVA) with Dunnet T3 post hoc—for continuous variables—or chi-
square tests—for categorical variables—were used to compare the ob-
tained values between frail, pre-frail, and not frail participants. Paired
Student t-tests were used to compare obtained and predicted values.
The association between the maximum inspiratory and expiratory
M.B. Vidal, et al. Archives of Gerontology and Geriatrics 89 (2020) 104082

11.4.4 program. For all measurements, 95% confidence intervals and

5% significance level were used.

3. Results

Three hundred seventy-nine older adults made up the final sample.

Fig. 1. Flow diagram of the recruitment and data collection process.
pressures (continuous variables) and frailty was verified with crude and
adjusted analyzes using a multinomial logistic regression model. Odds-
ratios, with 95% confidence interval, were estimated (p < 0.05). All
data were analyzed using the version 21.0 of the Statistical Package for
Social Sciences (SPSS) program. The models were adjusted for age,
gender, number of diseases (Tavares, Pelizaro, Pegorari, Paiva, &
Marchiori, 2019), chronic conditions (asthma, chronic obstructive
pulmonary disease [COPD], diabetes, systemic arterial hypertension
[SAH], stroke e heart diseases), number of medications, and smoking
status.
To determine the cut-off points of the maximum inspiratory and
maximum expiratory pressures, Receiver Operating Characteristic
(ROC) curves, their associated areas under the curve (AUC), and sen-
sitivity and specificity parameters were calculated in the MedCalc
The number of recruited, assessed, included, and excluded participants
are detailed in Fig. 1. In the 379 individuals included in the study, the
prevalence of frailty and pre-frailty was 12.4% and 58%, respectively.
Participant characteristics, organized by frailty, are detailed in Table 1.
Maximum inspiratory and expiratory pressures in frail participants
were significantly lower compared to pre-frail participants, and sig-
nificantly lower in pre-frail compared to non-frail participants.
Significant differences were also found between obtained and predicted
values of maximum inspiratory and expiratory pressures (Table 2).
Table 3 displays how adjusted maximum respiratory obtained
pressures are inversely associated with frailty and pre-frailty. Specifi-
cally, a 1cmH2O increase in maximum inspiratory pressure and max-
imum expiratory pressure reduces the probability of frailty in older
adults by 3%. Similarly, a 1cmH2O increase in both maximum in-
spiratory pressure and maximum expiratory pressure reduces the
probability of pre-frailty in older adults by 2%.
Fig. 2 presents the cut-off points of maximum inspiratory and ex-
piratory pressures for discriminating frailty and pre-frailty. Values
≥-50cmH2O for maximum inspiratory pressure and ≤60cmH2O for
maximum expiratory pressure constituted a discriminant criterion for
the presence of frailty. Values ≤65cmH2O for maximum expiratory
pressure discriminated pre-frailty.
4. Discussion
This study showed that community-dwelling frail older adults pre-
sent lower maximum inspiratory and expiratory pressures than their
pre-frail peers, and pre-frail older adults present lower values than their
non-frail peers. Frail and pre-frail older adults obtained values lower
than predicted for age (Neder et al., 1999). This study is the first to
identify an inverse relationship between respiratory muscle strength

Table 1
Characteristics of older adults by level of frailty. Macapá, AP, Brazil, 2017 (n = 379)
Variables Frail Pre-frail Non-frail Total
(n = 47) (n = 220) (n = 112) (n = 379)

Age (years)† 73.68 ± 8.66 70.46 ± 7.36 67.50 ± 5.40€ 69.99 ± 7.26

Gender*
Male 10(21.3) 75(34.1) 47(42)** 132(34.8)
Female 37(78.7) 145(65.9) 65(58) 247(65.2)
Height (m)† 1.51 ± 0.07 1.53 ± 0.08 1.56 ± 0.09€ 1.54 ± 0.08
Weight (Kg)† 68.98 ± 14.59 66.89 ± 13.35 65.38 ± 12.72 66.70 ± 13.33
BMI (kg/m2)† 30.06 ± 5.73 28.34 ± 4.86 26.64 ± 4.33€ 28.05 ± 4.93
Number of diseases† 7.12 ± 3.17 5.51 ± 2.75 4.29 ± 2.49†† 5.35 ± 2.86

Chronic conditions (yes/n (%)*

Asthma 3(6.5) 21(9.5) 9(8.0) 33(8.7)
COPD 1(2.1) 4(1.8) 1(0.9) 6(1.6)
Diabetes 19(40.4) 54(24.5) 18(16.1)** 91(24.0)
SAH 38(80.9) 136(61.8) 56(50.0)** 230(60.7)
Heart diseases 13(27.7) 25(11.4) 9(8.0)** 47(12.4)
Stroke 14(29.8) 20(9.1) 6(5.4)** 40(10.6)
Number of medications† 2.14 ± 1.74 1.70 ± 1.81 1.28 ± 1.61# 1.63 ± 1.76

Smoking*
Yes 2(4.3) 22(10) 9(8) 33(8.7)
No 45(95.7) 198(90) 103(92) 346(91.3)

Data are expressed as n: number of subjects; mean+standard deviation; m: meters; Kg: kilogram; BMI: body mass index; COPD: chronic ob-
structive pulmonary disease; SAH: Systemic Arterial Hypertension; *chi-square test; **(p<0.05); †One-way ANOVA test. ††Multiple comparisons
between groups: significant differences (p < 0.05) were observed between the three groups. #Non-frail ≠ frail; €Non-frail ≠ pre-frail and frail.

3
M.B. Vidal, et al. Archives of Gerontology and Geriatrics 89 (2020) 104082

Table 2
Comparison between obtained and predicted respiratory pressures in frail, pre-frail, and non-frail participants. Macapá, AP, Brazil, 2017 (n = 379)
Maximum respiratory pressures Frail Pre-frail Non-frail Total
(n = 47) (n = 220) (n = 112) (n = 379)

Obtained MIP (cmH2O) £ −46.17 ± 19.73 −57.07 ± 24.26 −67.23 ± 27.76 −58.72 ± 25.64
Predicted MIP (cmH2O) −78.98 ± 10.09 −83.68 ± 11.69 −87.51 ± 12.91 −84.23 ± 12.14
Obtained x predicted p < 0.001† p < 0.001† p < 0.001† p < 0.001†
% of predicted MIP (cmH2O) −58.45 −68.20 −78.82 −69.71

Obtained MEP (cmH2O) £ 57.65 ± 24.82 68.59 ± 27.36 81.56 ± 29.54 71.07 ± 28.69
Predicted MEP (cmH2O) 78.08 ± 15.38 84.72 ± 17.44 89.69 ± 18.95 85.37 ± 17.97
Obtained x predicted p < 0.001† p < 0.001† p = 0.001† p < 0.001†
% of predicted MEP (cmH2O) 73.83 80.96 90.93 83.24

Data are expressed as n: number of subjects; mean+standard deviation; MIP: Maximum inspiratory pressure; MEP Maximum expiratory pressure; p < 0.05. † Paired
Student t-test; £ Multiple comparisons between groups: significant differences (p < 0.05) were found between all groups.

Table 3 confirm the importance of considering respiratory muscle strength in

Association between maximum respiratory pressures and frailty in community- assessing frailty in older adult populations. Our results also show that,
dwelling older adults. Macapá, AP, Brazil, 2017 (n = 379) even after adjustment, frailty is associated with reduced respiratory
Maximum Frailty muscle strength in older adults. A 1cmH2O increase in maximum in-
Respiratory spiratory pressure reduces the probability of frailty and pre-frailty in
Pressures Pre-frail Frail the elderly by 3%. Furthermore, a 1cmH2O increase in maximum ex-
piratory pressure reduces the probability of frailty and pre-frailty in 2%.
OR 95% CI p* OR 95% CI p*
These data suggest that interventions to promote respiratory muscle
MIP (cmH2O) strengthening in older adults may be useful for preventing or stopping
Unadjusted 0.98 0.97-0.99 0.001 0.96 0.95-0.98 <0.001 frailty from progressing. However, randomized clinical trials are
Adjusted 0.98 0.97-0.99 0.034 0.97 0.95-0.99 0.004 needed to confirm the utility of respiratory muscle strengthening pro-
MEP (cmH2O)
grams in frail older adults, as well as the effects that these programs
Unadjusted 0.98 0.97-0.99 <0.001 0.96 0.95-0.98 <0.001
Adjusted 0.98 0.97-0.99 0.010 0.97 0.96-0.99 0.021 could have on frailty-related morbidity and mortality in older adults.
In our study, we determined the cut-off values of respiratory muscle
CI: Confidence Interval; OR: Odds Ratio; MIP: Maximum inspiratory pressure; strength for discriminating frailty in older adults. Respiratory muscle
MEP: Maximum expiratory pressure; *p < 0.05; Adjusted for age, gender, strength may be an additional measure to be used to screen the elderly
number of diseases, chronic conditions (asthma, chronic obstructive pulmonary for frailty. Values ≥-50 cmH2O for maximum inspiratory pressure and
disease, diabetes, systemic arterial hypertension, stroke, and heart diseases) ≤60 cmH2O for maximum expiratory pressure constituted a dis-
number of medications and smoking.
criminant criterion for the presence of frailty. Values ≤65 cmH2O for
maximum expiratory pressure discriminated pre-frailty. A previous study
and frailty and pre-frailty and to demonstrate that cut-off points for (Ohara et al., 2018) posited that cut-off values of respiratory muscle
respiratory muscle pressures may be useful for discriminating frailty strength could be useful as a discriminator of sarcopenia and that they
and pre-frailty in older adults. are associated with handgrip strength and gait speed in older people. The
The aging process leads to a reduction in respiratory muscle association between respiratory muscle strength and these variables is
strength (Lalley, 2013). As calcium deposition increases in the synovial especially relevant and ratifies the importance of considering respiratory
joints between the sternum and costal cartilages in older adults, their muscle strength in evaluating frailty, as sarcopenia, handgrip strength,
chest walls become more rigid and less compliant (Janssens, 2005). and gait speed are common indicators of frailty (Fried et al., 2001).
Additionally, aging is associated with a loss of the intrinsic elastic recoil This study is not without limitations. Most of the participants in-
of the pulmonary parenchyma, which leads to an increase in residual cluded in this study were female, which may be reflected in lower values
volume and results in pulmonary hyperinflation (Lalley, 2013). The of respiratory muscle strength. To minimize this limitation, all analyses
reduction in chest wall compliance and the pulmonary hyperinflation were adjusted for gender. Another limit is that our study did not limit our
promote diaphragm horizontalization, which reduces diaphragm con- sample to non-smokers, former smokers, or individuals without re-
tractile efficiency and may explain the reduction of inspiratory muscle spiratory diseases. Hence, the analyses were also adjusted for smoking
strength (Vaz Fragoso & Gill, 2012). Expiratory muscle strength, in its status and the number of diseases. Finally, as this study has a cross-
turn, seems to reduce with aging as a result of the decrease in type I and sectional design, causal relationships between respiratory muscle
type II fibers, but more predominantly in type II of the internal inter- strength and frailty cannot be inferred. Prospective studies may clarify
costal muscles (Mizuno, 1991). the relationship between these variables. Despite these limitations, this
The decrease in inspiratory muscle strength as people age can not only study was made up of a representative sample of community-dwelling
promote reductions in tidal volume, increase in respiratory rate, re- older adults and showed that respiratory muscle strength is an important
spiratory effort (Janssens, 2005), and exercise intolerance (Giua et al., component to be considered in the evaluation of older adults. This study
2014; Watsford, Murphy, & Pine, 2007), but is also considered an in- additionally established cut-off points for maximum respiratory muscle
dependent risk factor for cardiovascular death (van der Palen et al., 2004). pressures for discriminating frailty and pre-frailty in older adults, which
The reduction in expiratory muscle strength can lead to airflow limitation can facilitate assessing frailty when other resources are not available.
and impairment of the cough mechanism, which predispose the accumu-
lation of secretions and pulmonary infections (Kim & Sapienza, 2005). 5. Conclusion
Our study identified that the reduction in respiratory muscle
strength is greater in frail and pre-frail older people than in pre-frail Frail older adult participants presented maximum inspiratory and
older people, indicating that respiratory muscle strength decreases as expiratory pressures lower than pre-frail participants, and pre-frail
the severity of frailty increases. Our findings are in line with previous participants presented lower values than non-frail participants. Frail
studies (Parentoni et al., 2013; Pegorari et al., 2013), and together, and pre-frail participants obtained values lower than predicted for age.

4
M.B. Vidal, et al.
Fig. 2. Areas under the ROC curve for maximum respiratory pressures as discriminators for the presence of frailty (A) and pre-frailty (B) in older adults. Macapá, AP,
Brazil, 2017 (n = 379).
AUC: Area under the curve; CI: Confidence Interval; MIP: Maximum inspiratory pressure; MEP: Maximum expiratory pressure.
Frailty and pre-frailty were inversely associated with inspiratory and
expiratory muscle strength. Finally, cut-off points for maximum in-
spiratory (≥-50 cmH2O) and maximum expiratory pressures (≤60
cmH2O) could discriminate frailty. The values of maximum expiratory
pressure (≤65 cmH2O) could discriminate pre-frailty in older adults.
Contributors
DGO, MBV and MSP contributed to the conception and design of the
study, its critical review and approval of the version to be published;
ACPNP, ECS, APM contributed to the conception and design and the
writing of the article; MSP performed data analysis and contributed to
the writing of the article.
Funding
This research was financed by the Foundation for Research Support
of the State of Amapá (FAPEAP, Concession nº 250.203.029/2016).
5
Archives of Gerontology and Geriatrics 89 (2020) 104082
Ethical declaration
This study received approval from the Research Ethics Committee of
the Federal University of Amapá, number 1.738.671.
Declaration of Competing Interest
There were no conflicts of interest.
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