Skip to main content

Influence of an inspiratory muscle fatigue protocol on older adults on respiratory muscle strength, muscle oxygen saturation, and functional capacity: a randomized controlled trial

Abstract

Background

The fatigue of the inspiratory musculature, particularly the diaphragm, has been demonstrated to exert systemic effects on the body, impacting cardiovascular and performance outcomes. This study aimed to evaluate the influence of an inspiratory muscle fatigue protocol on respiratory muscle strength, functionality, and muscle oxygen saturation in older adults.

Methods

A single-blinded randomized controlled clinical trial was conducted on twenty-four older adults aged over 60 years, who met inclusion criteria were physically independent in terms of gait and functionality. Participants were randomly assigned to one of three groups: control group, inspiratory muscle fatigue group, or activation group. Diaphragmatic ultrasonography (diaphragmatic thickness, thickening fraction, diaphragm movement curve), maximal inspiratory mouth pressure, muscle oxygen saturation, and functionality (timed up and go test, for five times sit to stand test) were used to measure the study variables at two time points: pre-intervention (T1) and post-intervention (T2).

Results

In the maximum inspiratory pressure variable in the activation group an increase was found between baseline and post-treatment of 3.00 ± 0.93 cmH2O (P < 0.01), while in the inspiratory muscle fatigue a decrease of -6.75 ± 2.66 cmH2O (P < 0.01) was found. In addition, the inspiratory muscle fatigue group showed lower scores for respiratory and functional variables after performing the diaphragmatic fatigue intervention than the activation and control group (P < 0.05), on the other hand, the activation group showed more positive values for functional and respiratory capacity variables after performing the inspiratory muscle activation training (P < 0.05).

Conclusions

Fatigue of the inspiratory musculature appears to negatively impact inspiratory muscle strength, peripheral muscle strength, muscular oxygenation, and functionality in older adults. Activation of the inspiratory musculature could contribute to improved respiratory muscle strength and function in these individuals.

Trial registration

ClinicalTrials.gov ID: NCT06266013.

Peer Review reports

Background

As of today, population aging is an increasingly visible reality. For instance, the number of individuals over 65 years old in the European Union is higher in comparative terms than in other regions [1]. This aging, combined with various physiological changes, often leads to the onset of sarcopenia, characterized by muscle mass loss, muscle coordination alterations, decreased strength and contraction speed, and increased muscle fatigue [2]. This process also occurs at the level of respiratory muscles, resulting in a decrease in the strength of the respiratory muscles, which in turn will have a negative impact on pulmonary function, physical fitness, and quality of life [3].

The inspiratory muscles play a vital role in human life, facilitating gas exchange with the external environment and sustaining essential bodily functions. Among the main inspiratory muscles, the diaphragm stands out, which is capable of producing between 60–80% of the alveolar ventilation through its activation. Secondly, we have the external intercostals. Additionally, there are a series of accessory inspiratory muscles such as the scalenes or the sternocleidomastoid, which allow for the maintenance of this respiratory function in situations that increase the demand for gas exchange and cannot be met solely with the main inspiratory musculature [4]. Contraction of these muscles overcomes pleural pressure, facilitating gas exchange between atmospheric air and the alveolar space, taking in oxygen and releasing carbon dioxide. Furthermore, this process also regulates the acid–base balance, maintaining pH within normal values [5]. In addition to their respiratory function, inspiratory muscles serve other roles. For instance, the diaphragm, through the production and control of intra-abdominal pressure, as well as its attachment to the lumbar vertebrae, plays a pivotal role in lumbar stabilization and trunk motor control. On the other hand, its relationship with the vagus nerve via its connection to the esophagus allows this muscle to act on the parasympathetic nervous system through breathing, modulating various cardiovascular variables such as heart rate, blood pressure, or heart rate variability. Lastly, concerning its relationship with the lymphatic system, diaphragmatic contraction enables drainage of lymph nodes and vessels, especially those related to the lower limbs, due to the vacuum and suction effect produced during such contraction [6].

However, excessive stimulation of these muscles can lead to adverse consequences. Inspiratory muscle fatigue resulting from excessive stimulation triggers a competition for blood flow between respiratory and peripheral muscles, known as the metaboreflex. This can lead to reduced blood flow in peripheral muscles in favor of respiratory muscles, resulting in diminished blood perfusion and performance decline in affected musculature [7, 8]. Numerous studies conducted on healthy individuals and within the realm of sports have highlighted the influence of the metaboreflex on athletic performance, resulting, for example, in greater quadriceps fatigue during cycling tests, as well as an increased perception of effort [9], or leading to shorter apneas and turns in swimmers [10]. Furthermore, previous studies conducted on older adults have demonstrated the negative effects of the metaboreflex increasing blood pressure and reducing blood flow and perceived effort in the lower limbs, with a greater negative impact than that observed in younger subjects [11, 12]. Despite the available evidence on the negative effects of inspiratory muscle fatigue on variables such as blood flow, dyspnea, muscle fatigue, and perceived effort in peripheral muscles, no studies have evaluated the effects of fatigue on functionality, inspiratory muscle strength or muscle oxygen saturation in older adults. This could provide very useful information on the importance of the respiratory system and respiratory muscles in the physical condition and activities of daily living for this population, allowing for the incorporation of assessment and treatment/training of respiratory muscles to optimize or improve treatments or training programs for this population group. Therefore, the aim of this study was to objectively evaluate the acute effects of inspiratory muscle fatigue on functional capacity, inspiratory muscle strength, and muscular oxygen saturation in older adults. The hypothesis of this study is that inspiratory muscle fatigue may have a negative effect on inspiratory muscle strength, muscle oxygen saturation and functionality in older adults.

Methods

Study design

This study utilized a parallel randomized clinical trial design, conducted at the Physiotherapy Department of Residencial Montes de Toledo (Manzaneque, Spain), following the Consolidated Standards of Reporting Trials (CONSORT) guidelines [13]. Informed consent was obtained for all participants. The participants attended the laboratory on two occasions. The first visit was used to inform the participants about the study, collect informed consent and demographic data, as well as select participants based on inclusion and exclusion criteria. During the second visit, the interventions were carried out, along with the pre- and post-intervention assessments. The Research Ethics Committee of the Complejo Hospitalario Universitario de Toledo approved this study (approval number: 1070), and it was registered at ClinicalTrials.gov (NCT06266013, date of first registration: 14/02/2024).

Participants

Twenty-four older adults participated in the study and were randomized with a randomization process was performed using the randomization.com program. The participants were divided into 3 groups: inspiratory muscle fatigue group (IMFG), control group (CG) and activation group (AG). This process was performed by a third party who was not involved in the study. Both the evaluator and the data analyst were unaware of each participant's group assignment. Inclusion criteria for participants in this study were: being over 60 years of age and physical independence in terms of walking and functionality. The assessment of the exclusion criteria was conducted through interviews with the subjects. These criteria included subjects with impaired cognitive abilities, tympanic perforation or middle-internal ear pathology, pulmonary hypertension, decompensated cardiac or respiratory failure, undergoing lower extremity surgery within the last 12 months.

The sample size was determined using G*Power Software (3.1.9.2), based on maximal inspiratory mouth pressure (MIP) values data obtained on other previous study [14] with an alpha error of 0.05, a beta error of 0.2, and a medium effect size (f = 0.25 or Eta partial squared = 0.06). 30% estimated dropout rate was considered due to the study design. Therefore, a total sample size of 24 participants, divided into three groups (n = 8), was determined.

Intervention

IMFG performed the inspiratory muscle fatigue protocol using a threshold valve device (Big Breathe®; GH Innotek Co., Ltd., Busan, Republic of Korea). They breathed against submaximal inspiratory loads set at 60% of their MIP until they were unable to establish flow in at least three inspiratory efforts [15]. The AG followed a protocol of two sets of 30 repetitions at 40% of their MIP using the same threshold device as the IMFG, based on other study [16]. Finally, CG did not receive any intervention. Participants simply sat and waited for the same duration as the intervention and activation groups required to complete their protocol approximately 10 min.

Outcomes

Two measurements were taken at different times: pre-intervention (T1) and immediately post-intervention (T2). The evaluator responsible for conducting the measurements was blinded to each participant's group assignment. Firstly, the primary variables were analyzed to objectively confirm that the condition of inspiratory muscle fatigue had been achieved. Subsequently, the secondary variables were measured to assess the impact of this fatigue on functionality and muscle oxygen saturation.

Primary outcomes

MIP was measured using the Respiratory Pressure Measurement Device MicroRPM® (MicroMedical, Kent, UK) with subjects in a seated position, from residual volume to total lung capacity. To allow airflow through the mouth, the nose was plugged. Participants rested for 1 min between maneuvers and performed up to 6 maneuvers. The highest value obtained from three efforts that varied less than 5% was recorded [17].

Diaphragmatic thickness and thickening fraction

Diaphragmatic thickness was evaluated using a linear probe (L13-3 s) and a high-resolution device (GE Healthcare, Chicago, United States) with a frequency of 3.2–12.3 MHz placed perpendicular to the chest wall, with subjects in a supine position, in the anterior and mid-axillary lines, between the 8th and 9th intercostal spaces. B-mode ultrasound was utilized to visualize the structure in the juxtaposition region. Diaphragm thickness was measured three times at the end of expiration (Thickesp) and peak inspiration (Thickinsp), with the mean values recorded. The thickness observed at the end of expiration was designated as diaphragmatic thickness. The thickening fraction (TF%) was calculated using the formula: TF = [(Thickness at end of maximum inspiration—Thickness at end of expiration) / Thickness at end of expiration] × 100% [18].

Diaphragm movement curve

Evaluation of the diaphragmatic movement curve employed a convex probe (C5-1 s) with a frequency of 1.2–6 MHz placed on the mid-clavicular line of the right costal margin longitudinally, using the liver as an acoustic window and orienting the probe cephalically, with subjects in a supine position. M-mode was used to record the diaphragmatic movement curve during maximal deep breathing and sniff breathing. Diaphragmatic excursion (Mobinsp and Mobsniff), inspiratory time (Timeinsp and Timesniff), and maximum contraction velocity (Velinsp and Velsniff) were analyzed in both types of breathing. Three successive respiratory cycles were measured, and the average value of each parameter was recorded [18].

Secondary outcomes

For Timed Up and Go test (TUG), patients sat on a chair with armrests and were instructed to stand up (start of trial and timing), walk 3 m, and then sit back down in the initial chair (end of timing) [19].

For Five Times Sit to Stand test (FTSST), patients sat on an armless chair with a height of 43-45 cm, with their arms crossed over their chest, and were asked to stand up and sit down 5 times in place as quickly as possible [20].

Muscle oxygen saturation levels (SmO2) were assessed using the Moxy Monitor device (Fortiori Design LLC, Hutchinson, MN, USA). This wireless and portable device utilizes infrared spectroscopy to evaluate SmO2. Data analysis was conducted using computer software (Moxy Software v1.5.5; Idiag, Fehraltorf, Switzerland). The measurement protocol., consists of a 180-s measurement at rest, followed by continuous measurement during all three protocols. Measurements were taken on the medial gastrocnemius of the dominant leg with the patient in a standing position. The selected values corresponded to the mean recorded during the last 30 s of each phase [21].

Statistical analysis

Statistical analysis was performed using IBM SPSS Statistics v.22.0. The significance level was set at P < 0.05. The normality of each variable was assessed using the Shapiro-Wilks test test, indicating a normal distribution for all variables. Descriptive statistics were applied to examine demographic with measurements presented as mean ± SD. A 2-way repeated measures ANOVA was used for outcome variables, investigating the interaction between the IMFG, AG and CG) and the time of assessment (Baseline, Posttreatment). Post hoc Bonferroni multiple-comparisons test were applied when differences were identified. The effect size (ES) was interpreted using Cohen’s scale [22]: low (< 0.20), medium (0.50) and high (> 0.80).

Results

Demographic data

Twenty-four older adults were recruited for the study on February 2024 and participate on March 2024. They were distributed among IMFG (5-men, 3-women), AG (4-men, 4-women) and CG (6-men, 2-women). There were no dropouts due to complications, adverse effects or during follow up. The CONSORT flow chart was included (Fig. 1). No significant differences were found between IMFG, AG and CG in demographic characteristics (Table 1).

Fig. 1
figure 1

CONSORT Flow diagram of the study

Table 1 Demographic and clinical characteristics of patients

Changes in respiratory variables after fatigue and activation

Results for primary outcomes are presented in Table 2.

Table 2 Primary outcomes measurements (respiratory variables)

In the analysis of the MIP variable, the IMFG had lower values than the AG after performing the treatment (P < 0.05). Within the IMFG analysis, there was a decreased between baseline and post-treatment of -6.75 ± 2.66 cmH2O (P < 0.01; ES = 0.72; 95% CI of the difference = -8.06 to -5.44). In contrast, the AG showed an increased between baseline and post-treatment of 3.00 ± 0.93 cmH2O (P < 0.01; ES = 0.45; 95% CI of the difference = 1.69 to 4.31).

In the analysis of the TF%, the IMFG had lower values than the AG and the CG after performing the treatment (P < 0.01). Within the IMFG analysis there was a decreased between baseline and posttreatment of -22.13 ± 10.49% (P < 0.01; ES = 1.21; 95% CI of the difference = -27.29 to -16.96). Conversely, the AG showed an increased between baseline and post-treatment of 9.72 ± 5.78% (P < 0.01; ES = 0.61; 95% CI of the difference = 4.55 to 14.89).

In the analysis of Mobinsp, the IMFG had lower values than the AG and the CG after performing the treatment (P < 0.01). Within the IMFG analysis, there was a decreased between baseline and post-treatment of -0.79 ± 0.24 cm (P < 0.01; ES = 3.02; 95% CI of the difference = -0.96 to -0.61). Conversely, the AG showed an increased between baseline and post-treatment of 0.28 ± 0.18 cm (P < 0.01; ES = 0.96; 95% CI of the difference = 0.10 to 0.46).

Changes in functional and muscle oxygen saturation variables after fatigue and activation

Results for secondary outcomes are presented in Table 3.

Table 3 Secondary outcome measurements (functional and muscle oxygen saturation variables)

In the analysis of TUG, the inspiratory muscle fatigue group had higher values than the activation group after performing the treatment (P < 0.05). Within the inspiratory muscle fatigue group analysis, there was an increased between baseline and post-treatment of 3.42 ± 1.11 s (P < 0.01; ES = 0.82; 95% CI of the difference = 2.85 to 3.99), on the other hand, the activation group showed a decreased between baseline and posttreatment of -1.95 ± 0.63 s (P < 0.01; ES = 0.59; 95% CI of the difference = -2.52 to -1.38).

In the analysis of FTSST, the inspiratory muscle fatigue group had higher values than the activation group after performing the treatment (P < 0.01). Within the inspiratory muscle fatigue group analysis, there was an increased between baseline and post-treatment of 3.23 ± 1.25 s (P < 0.01; ES = 1.44; 95% CI of the difference = 2.40 to 4.07). Conversely, the activation group showed a decreased between baseline and post-treatment of -1.73 ± 1.12 s (P < 0.01; ES = 0.51; 95% CI of the difference = -2.57 to -0.90).

In the analysis of the SmO2, the inspiratory muscle fatigue group had lower values than the activation group and the control group after performing the treatment (P < 0.01). Within the inspiratory muscle fatigue group analysis, there was a decrease between baseline and post-treatment of -8.55 ± 1.50% (P < 0.01; ES = 7.99; 95% CI of the difference = -9.21 to -7.89). Conversely, the activation group showed an increased between baseline and post-treatment of 0.55 ± 0.32% (P < 0.01; ES = 0.21; 95% CI of the difference = 0.11 to 1.21).

Discussion

The results of our study suggest a decrease in inspiratory muscle strength, as well as a decline in functional capacity and muscle oxygen saturation when isolated inspiratory muscle fatigue occurs in older subjects. Furthermore, both inspiratory strength and functionality appear to improve with inspiratory muscle activation.

The aging process has negative effects on respiratory musculature, especially concerning the inspiratory musculature, particularly the diaphragm. Factors such as hyperinflation due to increased residual volume, increased dorsal kyphosis, or the greater rigidity of the thoracic cage induce a loss of strength in the diaphragm of around 30% in older subjects compared to younger individuals, also becoming a marker of sarcopenia [23]. Additionally, greater diaphragmatic thickening has been demonstrated in older adults, likely due to the increased need for lumbar stabilization in this population, as well as greater flattening and decreased muscle contraction velocity [3].

The results obtained in this study demonstrated reduced MIP values in the IMFG, consistent with previous studies conducted with similar protocols [24]. Inspiratory muscle fatigue involves the inability of the inspiratory muscles to overcome a given pleural pressure and is considered a limiting factor in both sports performance and exercise tolerance. Such respiratory muscle fatigue induces the appearance of the so-called respiratory metaboreflex or metaboreflex, whereby, through an afferent stimulus from type III and IV fibers, it reaches the supraspinal level, producing reflex vasoconstriction of active peripheral musculature, increasing perceived effort and decreasing performance [7] which is further intensified, with a significant increase in the vasopressor response as subject age increases [12]. Various studies throughout current scientific literature have examined the effects of inducing fatigue on respiratory musculature. For example, in another study, it was demonstrated that inducing diaphragmatic fatigue in healthy subjects resulted in decreased exercise tolerance, as well as increased sensation of dyspnea and leg discomfort [25].

Regarding the ultrasound measurements obtained, they appear to be reduced in the IMFG, yielding results similar to those found in previous studies [26]. Ultrasound constitutes a non-invasive imaging technique that allows for objective evaluation of muscle structure and function, in our case, of respiratory musculature, specifically the diaphragm, and is also a reliable and reproducible assessment method [18]. There is evidence regarding the different correlations between diaphragmatic thickness measurements made with the B-mode and diaphragmatic mobility measurements made using the M-mode. Regarding diaphragmatic thickness measurement, its correlation with inspiratory muscle strength and pulmonary function has been demonstrated, while diaphragmatic mobility correlates equally with inspiratory muscle strength, transdiaphragmatic pressure, and esophageal pressure, specifically through deep breathing and sniff maneuvers [27, 28]. On the other hand, another determinant of diaphragmatic functionality, in addition to the force it can develop, is diaphragmatic contraction velocity, which is also not influenced by other variables such as thoracic stiffness or pulmonary distensibility, allowing for an accurate reflection of diaphragmatic contraction efficiency [29]. Previous studies analyzing diaphragmatic dysfunction using ultrasound demonstrated a decrease in respiratory time, thickening fraction, strength, and diaphragmatic contraction velocity in subjects with sepsis-induced diaphragmatic dysfunction [30]. Among the potential effects that may explain these negative outcomes, we find that fatigue can affect the ability of the muscles to generate pressure and force, resulting in a decrease in diaphragm thickness and mobility during contraction [31, 32]. On the other hand, the improvements observed in the AG could be explained by the neuromuscular and biochemical enhancements resulting from the activation of the inspiratory muscles [33].

Muscle oxygen saturation measurements using infrared spectroscopy devices have proven to be an effective measurement method both during activity and at rest, whether for research or training purposes [34]. The lower values of muscle oxygen saturation found in the fatigue group may be due to peripheral vasoconstriction and blood flow redistribution resulting from excessive inspiratory muscle work and the appearance of the metaboreflex, leading to reduced blood supply to the area and thus reduced oxygen delivery [35, 36], also occurring in the lower limbs at rest [37]. It should be noted that in older adults, there is already dysfunction of the cardiovascular system, leading to reduced vasodilatory capacity during exercise, as well as slower oxygen uptake at the onset of exercise [38, 39]. Our results align with another previous study, where subjects subjected to increased respiratory work showed increased blood flow in accessory respiratory musculature, as well as a decrease in locomotor musculature [40].

TUG is a commonly used test in clinical practice to assess functionality and fall risk in older adults [41]. Additionally, it is widely validated and integrated into the management of respiratory pathology due to its ease of use and its ability to stratify frailty in COPD patients [42]. On the other hand, FTSST is a widely validated test in older adults aimed at assessing lower limb strength, as well as postural control and balance [43]. Currently, there are no studies investigating the relationship between inspiratory muscle fatigue and functionality, balance, and strength in older adults. Although these tests may initially seem too short in duration, it is important to consider that the negative effects of the metaboreflex can be triggered by short-duration stimuli that involve significant effort for the patient [44], such as performing five squats or walking three meters as quickly as possible for an older adult. Our results demonstrate a significant increase in the execution time of TUG and FTSST in the IMFG. We can hypothesize that, as a decrease in blood flow and oxygen supply to peripheral musculature induced by the metaboreflex occurs [35, 36], ischemia may lead to a loss of muscle contractile capacity and strength [38]. This ischemia may present the same issue in respiratory musculature, considering that the diaphragm plays a fundamental role in lumbar stability through control and generation of intra-abdominal pressure [45].

Regarding the improvements obtained by the AG, several studies available in the current scientific literature evidence the various effects produced by activation of respiratory musculature. On one hand, improvements in MIP and various ultrasound variables may be due to improved neuromuscular function of the diaphragm and accessory inspiratory musculature [46]. Additionally, moderate loads like those used in our study also allowed for a decrease in dyspnea sensation and increased oxygen supply to active muscles [47] thus improving exercise tolerance [48] with improvements also found in lung function [16].

Although the results of this study should be interpreted with caution, they seem to have a number of interesting clinical implications. Firstly, there appear to be a series of negative functional implications resulting from respiratory muscle fatigue. Secondly, it seems that the activation of the inspiratory muscles may have beneficial effects on functionality in older adults. Therefore, these results suggest that inspiratory muscle training should be considered in clinical contexts, both rehabilitative and preventive, as part of treatment and training programs for older adults. Among the possible limitations of this study, we found that only pre and post measurements of the different variables were performed, not allowing for the objective assessment of how long the effects of the interventions may last. For its part, neither respiratory rate or tidal volume were standardized; the breathing pattern was free as long as the ratio of two seconds of expiration for every second of inspiration was maintained. On the other hand, although other correlated measurements were employed, the application of specific measurements such as phrenic stimulation at the cervical level or transdiaphragmatic pressure could have provided greater objectivity to inspiratory muscle fatigue. Future lines of research may focus on evaluating the long-term effects of inspiratory muscle fatigue on functionality, as well as examining its effects on other variables or parameters such as time to task failure, muscle strength, or aerobic capacity.

Conclusions

Fatigue of the inspiratory musculature seems to have a detrimental effect on inspiratory muscle strength, peripheral muscle strength, muscular oxygenation and functionality in older adults. On the other hand, activation of the inspiratory musculature appears to contribute to improvements in respiratory muscle strength and functionality in these individuals.

Data availability

We have the availability of the data, and the materials are available at the request of the publisher.

Abbreviations

IMFG:

Inspiratory muscle fatigue group

AG:

Activation group

CG:

Control group

MIP:

Maximal inspiratory pressure

Thickinsp :

Diaphragmatic thickness in inspiration

Thickesp :

Expiratory diaphragmatic thickness

TF:

Thickness ratio inspiration/expiration

Mobinsp :

Maximal inspiration diaphragmatic mobility

Timeinsp :

Maximum inspiratory contraction time

Velinsp :

Maximum inspiration contraction velocity

Mobsniff :

Diaphragmatic mobility sniff

Timesniff :

Sniff contraction time

Velsniff :

Sniff contraction velocity

TUG:

Timed up and go test

FTSST:

Five times sit to stand test

SmO2 :

Muscle oxygen saturation

References

  1. Franse CB, Zhang X, van Grieken A, Rietjens J, Alhambra-Borras T, Dura E, Garces-Ferrer J, van Staveren R, Rentoumis T, Markaki A, et al. A coordinated preventive care approach for healthy ageing in five European cities: A mixed methods study of process evaluation components. J Adv Nurs. 2019;75(12):3689–701.

    Article  PubMed  Google Scholar 

  2. Kalyani RR, Corriere M, Ferrucci L. Age-related and disease-related muscle loss: the effect of diabetes, obesity, and other diseases. Lancet Diabetes Endocrinol. 2014;2(10):819–29.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Bordoni B, Morabito B, Simonelli M. Ageing of the Diaphragm Muscle. Cureus. 2020;12(1):e6645.

    PubMed  PubMed Central  Google Scholar 

  4. Dominelli PB, Sheel AW. The pulmonary physiology of exercise. Adv Physiol Educ. 2024;48(2):238–51.

    Article  PubMed  Google Scholar 

  5. De Troyer A, Boriek AM. Mechanics of the respiratory muscles. Compr Physiol. 2011;1(3):1273–300.

    Article  PubMed  Google Scholar 

  6. Kocjan J, Adamek M, Gzik-Zroska B, Czyzewski D, Rydel M. Network of breathing. Multifunctional role of the diaphragm: a review. Adv Respir Med. 2017;85(4):224–32.

    Article  PubMed  Google Scholar 

  7. Romer LM, Polkey MI. Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol (1985). 2008;104(3):879–88.

    Article  PubMed  Google Scholar 

  8. Romer LM, Lovering AT, Haverkamp HC, Pegelow DF, Dempsey JA. Effect of inspiratory muscle work on peripheral fatigue of locomotor muscles in healthy humans. J Physiol. 2006;571(Pt 2):425–39.

    Article  CAS  PubMed  Google Scholar 

  9. Wuthrich TU, Notter DA, Spengler CM. Effect of inspiratory muscle fatigue on exercise performance taking into account the fatigue-induced excess respiratory drive. Exp Physiol. 2013;98(12):1705–17.

    Article  PubMed  Google Scholar 

  10. Moravec T, Lomax M, Usaj A, Kapus J. Inspiratory muscle fatigue at the swimming tumble turns: its occurrence and effects on kinematic parameters of the turns. Front Physiol. 2023;14:1219520.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Smith JR, Alexander AM, Hammer SM, Didier KD, Kurti SP, Broxterman RM, Barstow TJ, Harms CA. Cardiovascular consequences of the inspiratory muscle metaboreflex: effects of age and sex. Am J Physiol Heart Circ Physiol. 2017;312(5):H1013–20.

    Article  PubMed  Google Scholar 

  12. Leahy MG, Kipp S, Benbaruj JM, Charkoudian N, Foster GE, Koehle MS, Sheel AW. Effects of sex and ageing on the human respiratory muscle metaboreflex. J Physiol. 2023;601(3):689–702.

    Article  CAS  PubMed  Google Scholar 

  13. Cuschieri S. The CONSORT statement. Saudi J Anaesth. 2019;13(Suppl 1):S27–30.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Holtzhausen S, Unger M, Lupton-Smith A, Hanekom S. An investigation into the use of ultrasound as a surrogate measure of diaphragm function. Heart Lung. 2018;47(4):418–24.

    Article  PubMed  Google Scholar 

  15. Welch JF, Archiza B, Guenette JA, West CR, Sheel AW. Sex differences in diaphragmatic fatigue: the cardiovascular response to inspiratory resistance. J Physiol. 2018;596(17):4017–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ozdal M. Acute effects of inspiratory muscle warm-up on pulmonary function in healthy subjects. Respir Physiol Neurobiol. 2016;227:23–6.

    Article  PubMed  Google Scholar 

  17. American Thoracic Society/European Respiratory S: ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med 2002, 166(4):518–624.

  18. Santana PV, Cardenas LZ, Albuquerque ALP, Carvalho CRR, Caruso P. Diaphragmatic ultrasound: a review of its methodological aspects and clinical uses. J Bras Pneumol. 2020;46(6): e20200064.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Hendriks S, Huisman MG, Ghignone F, Vigano A, de Liguori CN, Farinella E, Girocchi R, Audisio RA, van Munster B, de Bock GH, et al. Timed up and go test and long-term survival in older adults after oncologic surgery. BMC Geriatr. 2022;22(1):934.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Schaubert KL, Bohannon RW. Reliability and validity of three strength measures obtained from community-dwelling elderly persons. J Strength Cond Res. 2005;19(3):717–20.

    PubMed  Google Scholar 

  21. Contreras-Briceno F, Espinosa-Ramirez M, Moya-Gallardo E, Fuentes-Kloss R, Gabrielli L, Araneda OF, Viscor G: Intercostal Muscles Oxygenation and Breathing Pattern during Exercise in Competitive Marathon Runners. Int J Environ Res Public Health 2021;18(16).

  22. Cohen J: Statistical power analysis for the behavioral sciences, 2nd edn. Hillsdale, N.J.: L. Erlbaum Associates; 1988.

  23. Ohara DG, Pegorari MS. Oliveira Dos Santos NL, de Fatima Ribeiro Silva C, Monteiro RL, Matos AP, Jamami M: Respiratory Muscle Strength as a Discriminator of Sarcopenia in Community-Dwelling Elderly: A Cross-Sectional Study. J Nutr Health Aging. 2018;22(8):952–8.

    Article  CAS  PubMed  Google Scholar 

  24. Ladrinan-Maestro A, Sanchez-Infante J, Martin-Vera D, Sanchez-Sierra A. Influence of an inspiratory muscle fatigue protocol on healthy youths on respiratory muscle strength, vertical jump performance and muscle oxygen saturation: a randomized controlled trial. J Transl Med. 2024;22(1):732.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Welch JF, Archiza B, Guenette JA, West CR, Sheel AW. Effect of diaphragm fatigue on subsequent exercise tolerance in healthy men and women. J Appl Physiol (1985). 2018;125(6):1987–96.

    Article  CAS  PubMed  Google Scholar 

  26. Ladrinan-Maestro A, Sanchez-Infante J, Martin-Vera D, Sanchez-Sierra A. Influence of an inspiratory muscle fatigue protocol on healthy youths on respiratory muscle strength and heart rate variability A randomized controlled trial. Front Physiol. 2024;15:1457019.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Cardenas LZ, Santana PV, Caruso P. Ribeiro de Carvalho CR, Pereira de Albuquerque AL: Diaphragmatic Ultrasound Correlates with Inspiratory Muscle Strength and Pulmonary Function in Healthy Subjects. Ultrasound Med Biol. 2018;44(4):786–93.

    Article  PubMed  Google Scholar 

  28. Koco E, Soilemezi E, Sotiriou P, Savvidou S, Tsagourias M, Pnevmatikos I, Matamis D: Ultrasonographic assessment of diaphragmatic contraction and relaxation properties: correlations of diaphragmatic displacement with oesophageal and transdiaphragmatic pressure. BMJ Open Respir Res 2021;8(1).

  29. Sarwal A, Walker FO, Cartwright MS. Neuromuscular ultrasound for evaluation of the diaphragm. Muscle Nerve. 2013;47(3):319–29.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Chen Y, Liu Y, Han M, Zhao S, Tan Y, Hao L, Liu W, Zhang W, Song W, Pan M, et al. Quantification of diaphragmatic dynamic dysfunction in septic patients by bedside ultrasound. Sci Rep. 2022;12(1):17336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Enoka RM, Duchateau J. Muscle fatigue: what, why and how it influences muscle function. J Physiol. 2008;586(1):11–23. https://doiorg.publicaciones.saludcastillayleon.es/10.1113/jphysiol.2007.139477.

    Article  CAS  PubMed  Google Scholar 

  32. Zacarias Rondinel T, Bocchi L, Cipriano Junior G, Chiappa G, Martins GS, Mateus SRM, Cahalin LP, Cipriano GFB. Diaphragm thickness and mobility elicited by two different modalities of inspiratory muscle loading in heart failure participants: A randomized crossover study. PLoS ONE. 2024;19(5):e0302735.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cirino C, Marostegan AB, Hartz CS, Moreno MA, Gobatto CA, Manchado-Gobatto FB: Effects of Inspiratory Muscle Warm-Up on Physical Exercise: A Systematic Review. Biology (Basel) 2023;12(2).

  34. Gandia-Soriano A, Salas-Montoro JA, Javaloyes A, Lorente-Casaus C, Zabala M, Priego-Quesada JI, Mateo March M. Validity and reliability of two near-infrared spectroscopy devices to measure resting hemoglobin in elite cyclists. Int J Sports Med. 2022;43(10):875–80.

    Article  CAS  PubMed  Google Scholar 

  35. St Croix CM, Morgan BJ, Wetter TJ, Dempsey JA: Fatiguing inspiratory muscle work causes reflex sympathetic activation in humans. J Physiol 2000, 529 Pt 2(Pt 2):493–504.

  36. Sheel AW, Boushel R, Dempsey JA. Competition for blood flow distribution between respiratory and locomotor muscles: implications for muscle fatigue. J Appl Physiol (1985). 2018;125(3):820–31.

    Article  CAS  PubMed  Google Scholar 

  37. Sheel AW, Derchak PA, Morgan BJ, Pegelow DF, Jacques AJ, Dempsey JA. Fatiguing inspiratory muscle work causes reflex reduction in resting leg blood flow in humans. J Physiol. 2001;537(Pt 1):277–89.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hearon CM Jr, Dinenno FA. Regulation of skeletal muscle blood flow during exercise in ageing humans. J Physiol. 2016;594(8):2261–73.

    Article  CAS  PubMed  Google Scholar 

  39. DeLorey DS, Kowalchuk JM, Paterson DH. Effect of age on O(2) uptake kinetics and the adaptation of muscle deoxygenation at the onset of moderate-intensity cycling exercise. J Appl Physiol (1985). 2004;97(1):165–72.

    Article  PubMed  Google Scholar 

  40. Dominelli PB, Archiza B, Ramsook AH, Mitchell RA, Peters CM, Molgat-Seon Y, Henderson WR, Koehle MS, Boushel R, Sheel AW. Effects of respiratory muscle work on respiratory and locomotor blood flow during exercise. Exp Physiol. 2017;102(11):1535–47.

    Article  CAS  PubMed  Google Scholar 

  41. Barry E, Galvin R, Keogh C, Horgan F, Fahey T. Is the Timed Up and Go test a useful predictor of risk of falls in community dwelling older adults: a systematic review and meta-analysis. BMC Geriatr. 2014;14:14.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Albarrati AM, Gale NS, Munnery MM, Reid N, Cockcroft JR, Shale DJ. The Timed Up and Go test predicts frailty in patients with COPD. NPJ Prim Care Respir Med. 2022;32(1):24.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Albalwi AA, Alharbi AA. Optimal procedure and characteristics in using five times sit to stand test among older adults: A systematic review. Medicine (Baltimore). 2023;102(26):e34160.

    Article  PubMed  Google Scholar 

  44. Kilding AE, Brown S, McConnell AK. Inspiratory muscle training improves 100 and 200 m swimming performance. Eur J Appl Physiol. 2010;108(3):505–11.

    Article  PubMed  Google Scholar 

  45. Lee HJ, Kang TW, Kim BR. Effects of diaphragm and deep abdominal muscle exercise on walking and balance ability in patients with hemiplegia due to stroke. J Exerc Rehabil. 2018;14(4):648–53.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Koizumi J, Ohya T. Effects of high-intensity inspiratory muscle warm-up on inspiratory muscle strength and accessory inspiratory muscle activity. Respir Physiol Neurobiol. 2023;313: 104069.

    Article  PubMed  Google Scholar 

  47. Cheng CF, Tong TK, Kuo YC, Chen PH, Huang HW, Lee CL. Inspiratory muscle warm-up attenuates muscle deoxygenation during cycling exercise in women athletes. Respir Physiol Neurobiol. 2013;186(3):296–302.

    Article  PubMed  Google Scholar 

  48. Tong TK, Fu FH. Effect of specific inspiratory muscle warm-up on intense intermittent run to exhaustion. Eur J Appl Physiol. 2006;97(6):673–80.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Author information

Authors and Affiliations

Authors

Contributions

ALM and ASS carried out the design and idea of the project, ASS and ALM and DMV wrote the introduction to the manuscript, DMV and ALM wrote the methodology and JSI statistics part, and ASS, JSI and ALM wrote the Discussion and conclusions part. ASS, DMV and JSI reviewed the manuscript.

Corresponding author

Correspondence to Alberto Sánchez-Sierra.

Ethics declarations

Ethics approval and consent to participate

The current study was approved by the Research Ethics Committee of Toledo University Hospital Complex.

(Spain). In addition, written informed consent was obtained from the participants.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ladriñán-Maestro, A., Sánchez-Infante, J., Martín-Vera, D. et al. Influence of an inspiratory muscle fatigue protocol on older adults on respiratory muscle strength, muscle oxygen saturation, and functional capacity: a randomized controlled trial. BMC Geriatr 24, 1015 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12877-024-05610-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12877-024-05610-0

Keywords