Respiratory muscle training in non-athletes and athletes with spinal cord injury: A systematic review of the effects on pulmonary function,respiratory muscle strength and endurance,and cardiorespiratory fitness based on the FITT principle of exercise prescription

Abstract

BACKGROUND:

Respiratory muscle training (RMT) has been recommended to mitigate impacts of spinal cord injuries (SCI), but the optimal dosage in terms of the frequency, intensity, time, and type (FITT principle) to promote health in SCI individuals remains unclear.

OBJECTIVE:

To discuss research related to the effects of RMT on pulmonary function, respiratory muscle strength and cardiorespiratory fitness in athletes and non-athletes with SCI, presenting the FITT principle.

METHODS:

We performed a systematic review. PubMed, Lilacs, Scopus, Web of Science, PEDro, SciELO and Cochrane databases were searched between 1989 and August 2018. Participants were athletes and non-athletes with SCI.

RESULTS:

4,354 studies were found, of which only 17 met the eligibility criteria. Results indicated that RMT is associated with beneficial changes in pulmonary function and respiratory muscle strength and endurance among athletes and non-athletes, whereas no effect was reported for maximal oxygen uptake. It was not possible to establish an optimal RMT dose from the FITT principle, but combined inspiratory/expiratory muscle training seems to promote greater respiratory changes than isolated IMT or EMT.

CONCLUSION:

The use of RMT elicits benefits in ventilatory variables of athletes and non-athletes with SCI. However, it remains unclear which RMT type and protocol should be used to maximize benefits.

Keywords

Rehabilitation breathing exercises sports oxygen consumption paraplegia quadriplegia

1. Introduction

Spinal cord injury (SCI) is among the most common types of physical disabilities and may be congenital or acquired [1]. The causes of acquired SCI are automobile accidents, shallow water dives, firearm injuries, tumors, infections, and other diseases that may compromise the integrity of the spinal cord, whereas the congenital SCI mainly involves degenerative diseases, malformations of the central nervous system (CNS) and spina bifida [1, 2].

The limitations related to SCI include total or partial loss of movement and sensitivity below the injury level, loss of sphincter control, thermoregulation dysfunctions, and musculoskeletal changes, which vary according to the level of injury [3, 4, 5]. Postural changes, respiratory center impairment and abdominal muscle weakness, are some factors that commonly lead to cardiovascular and ventilatory deficits, negatively influencing exercise tolerance and cardiorespiratory fitness in people with SCI, especially in tetraplegic or quadriplegic individuals [6, 7, 8]. In cases of cervical SCI, interruption of the bulbar-spinal pathway frequently occurs, which causes paresis or paralysis of the respiratory muscles [7, 9, 10]. Both inspiration and expiration are affected in quadriplegic individuals, leading to loss of capacity for deep respiratory incursions, commonly leading to atelectasis and dyspnea, which hinders effective coughing and causes recurrent respiratory tract infections [11, 12, 13]. These adverse manifestations are accentuated by sedentary behaviors, which increase disease mortality risk.

In this context, regular physical activity has been widely recommended to improve pulmonary function, respiratory muscle strength and endurance, cardiorespiratory fitness, and cardiometabolic health outcomes in adults with chronic SCI [14, 15, 16]. To promote health outcomes, for instance, an exercise training program depends largely on the frequency (how often?), intensity (how hard?), time (how long?), and type (what kind?) of physical activity, also known as the FITT principle [17]. On the other hand, owing to the physical, psychosocial and environmental challenges to participating in physical activity programs [18, 19], the prevalence of sedentary behavior or low levels of physical activity and deconditioning among SCI individuals is higher than in the general population [20].

One strategy that has been identified as an ideal setting to promote physical activity in adults with chronic SCI is adapted sports, which initially was as a type of physical and psychological rehabilitation [21]. Individuals with SCI can participate in a variety of team sports, such as wheelchair rugby and wheelchair basketball, as well as individual sports, such as para athletics and para swimming, in a recreational or competitive way. Each sport has its own rules and for competition, athletes are grouped according to the degree of limitation resulting from their impairment – called classification – in order to make competition fairer [22]. Over time, high-performance sports for people with disabilities have become reality and have been gaining greater visibility and a number of fans around the world [23, 24]. Not only the quantity, but also the technical quality of the athletes has grown significantly and most of them want to make their history in the sport: reaching better results, breaking records and gaining medals [25]. Therefore, it is necessary for athletes to increase training loads, improve physical preparation, seek the help of health staff and logistic support, and to adopt different training strategies [26] in order to improve sports performance. Each detail is important for optimising performance.

Within this context, some strategies have been proposed and applied with the objective of improving the physical conditioning, functionality and general health status of individuals with SCI, including athletes and non-athletes (i.e. individuals who are not engaged in any kind of recreational or competitive adapted sport, and also sports performance for athletes), as for example, respiratory muscle training (RMT) [27, 28, 7, 8]. This type of training consists of providing resistance to the incoming airflow during the inspiration and/or expiration through a specific equipment [29]. Systematic reviews about the chronic effect of RMT techniques on respiratory muscle strength, pulmonary function, exercise tolerance and life-quality people with SCI have been performed by Brooks et al. [29], Van Houtte et al. [30], and Sheel et al. [31]; however, the findings regarding effectiveness of RMT intervention on the main approached outcomes are controversial. Moreover, there is a lack of knowledge regarding appropriate RMT prescription for SCI individuals in light of the potential benefits to health in terms of the FITT principle, and evidence is even more limited when the population of the studies are athletes with SCI [28, 7, 8], which may hamper the use of this intervention during the athlete’s preparation, especially regarding the type of stimulus, training protocols and equipment.

Thus, the aim of the present review was to discuss new and emerging research related to the effects of RMT on pulmonary function, respiratory muscle strength and endurance, and cardiorespiratory fitness of athletes and non-athletes with SCI, and present an updated FITT principle to RMT that integrates the existing recommendations with new and emerging research.

2. Methods

2.1 Protocol

This systematic review followed the guidelines of PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses; www.prisma-statement. org/) [32].

2.2 Eligibility criteria

The search descriptors were determined after the formulation of the research question, based on the PICO protocol [33]. The question was: “Is there evidence that RMT influences pulmonary function, respiratory muscle strength and endurance, and cardiorespiratory fitness in athletes and non-athletes with SCI? And considering the FITT principle for exercise prescription, what is the minimum dose of RMT necessary to improve respiratory outcomes and cardiorespiratory fitness among SCI individuals?”

Experimental studies were included in the Portuguese, English and Spanish languages, which had applied some type of RMT involving athletes and non-athletes with SCI and investigated outcomes related to ventilatory variables (pulmonary volumes and flows) and/or metabolic variables (e.g. maximal oxygen uptake, VO ${}_{\text{2max}}$ ). We excluded studies involving other types of diseases or disabilities other than SCI, monographs, master’s dissertations, doctoral theses, case series studies and case reports.

2.3 Information sources

The initial search was carried out in March 2017 and December 2017 and was completed with a new search to update the review in August 2018. PubMed, Lilacs, Scopus, Web of Science, PEDro, SciELO and Cochrane databases were searched.

2.4 Search

The following search terms were used from different combinations, in addition to corresponding descrip- tors in the Portuguese and Spanish languages: “breathing exercises”, “respiratory muscle training”, “spinal cord injury” (and synonyms), “athletes”, “sports”, “Paralympic”, “cardiorespiratory fitness”, “physical fitness”, “aerobic capacity” “exercise test”,“oxygen consumption”, “lung function test”, “respiratory function tests” and “pulmonary function test”. For this selection, the MeSH Database (Medical Subject Headings) was used, with the exception of the term “Paralympic”, which was not in the database.

2.5 Studies selection

Initially, the analysis was performed by two reviewers, through the title and the abstract, which was defined as a pre-selection according to the established inclusion criteria. Subsequently, the reviewers obtained access to the full reading of potentially eligible articles, and then a detailed analysis was performed. If there was disagreement between the reviewers, regarding the inclusion or exclusion of the studies, a third reviewer was asked to evaluate it.

2.6 Data collection process

The data extraction was performed in a standardized way, according to a previously created spreadsheet, containing the following information: authors, title, year of publication, scientific journal, study objectives, sample characteristics, sample size, RMT protocol applied, validation of instruments, variables evaluated, outcomes and results found.

2.7 Risk of bias in each study

For the assessment of risk of bias, factors such as sample size, control and randomization of the studies, sample homogeneity, RMT protocols, and cardiopulmonary exercise test (CPET) protocols were observed. Other characteristics of the studies that could generate bias were the RMT follow-up methods, as well as the frequency and intensity of the RMT.

Figure 1.

Flowchart illustrating the details of the search strategy, screening of potentially qualifying reports (n), selection of the included trials, and reasons for study exclusion. RMT $=$ respiratory muscle training.

2.8 Additional analyses

The PEDro scale (http://www.pedro.fhs.usyd.edu. au) was applied to evaluate the methodological quality of the studies, which has been shown to have good reliability and validity [34]. The PEDro scale has 11 points that examine external validity (criterion 1) and internal validity (criteria 2–9) of controlled trials and whether there is sufficient statistical information for interpreting results (criteria 10–11). The items of the scale are: specification of the eligibility criteria; randomized distribution of subjects by groups; secret allocation; similarity between groups with regard to the most important prognostic indicators; blindness of the subjects, therapists and evaluators; measurements of at least one key outcome in more than 85% of randomized subjects; treatment or control condition received according to allocation or data analysis by intention to treat; results of the statistical intergroup comparisons described for at least one key outcome and presentation of measures of accuracy and variability for at least one key outcome [35]. The scale criteria were filled by two researchers. In the case of disagreement, a third researcher was consulted.

3. Results

3.1 General characteristics

The search strategies and study selection are presented in Fig. 1. Initially, 4,354 studies were identified. After duplicate removal ( $n=$ 2,131) and eligibility criteria verification, 17 studies were included [36, 37, 38, 39, 40, 41, 28, 42, 43, 44, 45, 46, 8, 47, 48, 49, 50]. All included studies were clinical trials published in English, between 1989 and 2018, distributed as follows: fourteen controlled (i.e. eleven with other intervention [36, 37, 38, 41, 28, 44, 45, 46, 47, 50, 49], and three with placebo [43, 8, 48]); two studies without control group [40, 42]; and one cross-over study [39], which applied three interventions at the same group, for a four-week period each intervention. Most of the studies were conducted in Europe ( $n=$ 8; [39, 28, 42, 44, 45, 46, 8, 49]). Five studies were conducted in North America [36, 38, 40, 43, 48], three in Asia [41, 47, 50], and one in South Africa [37]. Among these, three investigated athletes [28, 45, 8].

Regarding the type of intervention, it was observed that studies presented a huge variety of training methods (6 methods) and five studies applied more than one type (Table 1). Ten studies adopted the inspiratory muscle training (IMT) [36, 38, 39, 41, 44, 46, 8, 50, 49, 48]; six studies used the RMT with bidirectional resistance [40, 28, 43, 45, 47, 49], one of which was associated with deep abdominal contraction [47]; three studies had the expiratory muscle training (EMT) [37, 39, 48], one of which was associated with abdominal electrostimulation [39]; and two studies applied normocapnic hyperpnoea training – NHT [42, 44].

Overall, the experimental groups investigated by the studies presented small sample sizes (i.e. between 5 and 42 participants), mostly composed of men. Neurological injuries were included between the second cervical vertebra (C2) and the third lumbar vertebra (L3). The mean injury time was 4.5 years (minimum: 2 months; maximum: 30 years). In the studies involving athletes, the following types of exercise were included: handbike [45], wheelchair racing [28], and wheelchair rugby [8].

Table 1
Characteristics of the RMT experimental groups’ protocols, considering the FITT principle for exercise prescription in athletes and non-athletes with SCI

Study	PEDro	Sample	Age	SCI	Time	RMT protocol and FITT principle
	scale	size M/F	(years)	levels	postinjury	Follow-up	Frequency	Intensity	Time	Type
							(days $\cdot$ week ${}^{-1}$ )		(min $\cdot$ bout ${}^{-1}$ )
Loveridge et al. [36]	4	6	31.0	C6–C7	At least 1 year	8-week	5	85%MIP ( $\uparrow$ every 2-week)	15 (2x a day)	IMT
Gounden [37]	4	17M/3F	27.8	C5–C7	27.4 months	8-week	6	60%MEP ( $\uparrow$ 5–10% every 2-week)	5–8 (5x a day)	EMT
Derrickson et al. [38]	4	6M (G1)	28.5	C4–C7	2–30 days	7-week	5	NR	15 (3x a day)	IMT
		3M/2F (G2)	27.0		2–74 days			10 sustained maximal inspiration with 11.34 kg placed on the abdomen	NR (4x a day)	AbWts
Zupan et al. [39]	4	11M/2F	26.9	C4–C7	7 months	4-week plus 4-week	6	75%MIP EMT NR AFES up to 110 Volts	20–30 (2x a day)	IMT and EMT plus AFES
Rutchik et al. [40]	2	10M	37.5	C4–C7	2–19 years	8-week	7	Resistance level (1 to 6)	15 (2x a day)	RMT with bidirectional resistance
Liaw et al. [41]	4	8M/2F	30.9	C4–C7	30–120 days	6-week	7	Started at inspiratory resistance of 7 mm	15–20 (2x a day)	IMT
Mueller et al. [28]	6	4M/2F	29	T4–L3	1.5–26 years	6-week	5	65–75%MVV	30	RMT with bidirectional resistance
Van Houtte et al. [42]	6	5M/2F	44.2	C4–T10	2–6 months	8-week	4	30–40%FVC	30	NHT
Roth et al. [43]	6	13M/3F	31.1	C4–T1	Within 6 months	6-week	5	NR	3–5 (2x a day)	RMT with bidirectional resistance
Mueller et al. [44]	7	6M/2F	35.2	C5–C8	6–8 months	8-week	4	80–100%MVV	40	IMT
		6M/2F	33.5					40–50%MVV		NHT
		6M/2F	41.6					NR		Incentive spirometry
Fischer et al. [45]	5	6M/1F	43	T2–T8	11–26 years	4-week	5	NR	30	RMT with bidirectional resistance
Postma et al. [46]	7	18M/1F	47.1	Above T9	57–109 days	8-week	5	60%MIP	$\sim$ 21 ( $\uparrow$ 30–42 min in the first eek)	IMT
West et al. [8]	5	5M	30.5	C5–C7	3–13 years	6-week	5	50–60%MIP	30 dynamic inspiratory maneuvers (2x a day)	IMT
Kim et al. [47]	7	7M/6F	40.0	C4–T6	4.2 years	8-week	3	5 $\times$ 10 SMI for 3–4 seconds followed by a maximal expiration	NR	RMT with bidirectional resistance plus ADIM
		7M/5F	41.5		4.3 years				NR	RMT with bidirectional resistance
Legg Ditterline et al. [48]	4	18M/6F	40	C2–T11	4-532 months	4-week	5	60%MIP and MEP	45	RMT with bidirectional resistance

Table 1, continued
Study	PEDro	Sample	Age	SCI	Time	RMT protocol and FITT principle
	scale	size M/F	(years)	levels	postinjury	Follow-up	Frequency	Intensity	Time	Type
							(days $\cdot$ week ${}^{-1}$ )		(min $\cdot$ bout ${}^{-1}$ )
Raab et al. [49]	5	32M/10F	30–73	C4–T12	$\sim$ 36–109 days	7-week	$\sim$ 3	33%MIP	$\sim$ 57 repetitions per training and $\sim$ 7 trainings per week	IMT
		32M/5F	30–72.5		$\sim$ 36–73 days	13-week		39%MIP and 27%MEP	$\sim$ 88 repetitions per training and $\sim$ 13 trainings per week	RMT with bidirectional resistance
Soumyashree and Kaur [50]	10	13M/2F	29	T1–T12	$\sim$ 8 months	4-week	5	$\sim$ 40%MIP	15	IMT

PEDro scale physiotherapy evidence database scale. M $=$ male; F $=$ female; RMT $=$ respiratory muscle training; IMT $=$ inspiratory muscle training; EMT $=$ expiratory muscle training; AbWts $=$ abdominal weights; AFES $=$ abdominal functional electrical stimulation; MVV $=$ maximal voluntary ventilation; FVC $=$ forced vital capacity; NHT $=$ normocapnic hyperpnoea training; SMI $=$ sustained maximal inspiration; IRS $=$ incentive respiratory spirometer; ADIM $=$ abdominal drawing-in maneuver; MIP $=$ maximal inspiratory pressure; MEP $=$ maximal expiratory pressure; NR $=$ not reported; $\uparrow$ $=$ increase.

Table 2

Relative changes (post-minus pre-intervention data) on respiratory muscle strength, pulmonary function, and cardiorespiratory fitness outcomes after RMT

Study	MIP	MEP	RMV	DT	RMS	FVC	MVV	PEF	VC	FEV ${}_{1}$	TLC	FRC	VO ${}_{\text{2max}}$
Loveridge et al. [36]	$\uparrow$ 29%	NE	NE	NE	NE	$\uparrow$ 1%	NE	NE	NE	NE	$\uparrow$ 5%	$\uparrow$ 5%	NE
Gounden [37]	NE	$\uparrow$ 55%	NE	NE	NE	NE	NE	NE	$\uparrow$ 34%	NE	NE	NE	NE
Derrickson et al. [38]	$\uparrow$ 67%	NE	NE	NE	NE	$\uparrow$ 96%	$\uparrow$ 39%	$\uparrow$ 126%	NE	NE	NE	NE	NE
Zupan et al. [39]	NE	NE	NE	NE	NE	$\uparrow$ 19% ${}^{\text{a}}$ $\uparrow$ 17.5% ${}^{\text{a}}$ $\uparrow$ 17% ${}^{\text{b}}$	NE	NE	NE	$\uparrow$ 20.5% ${}^{\text{a}}$ $\uparrow$ 16% ${}^{\text{a}}$ $\uparrow$ 16% ${}^{\text{b}}$	NE	NE	NE
Rutchik et al. [40]	$\uparrow$ 24%	$\uparrow$ 51%	NE	NE	NE	$\uparrow$ 11%	NE	NE	$\uparrow$ 8%	$\leftrightarrow$	$\uparrow$ 12%	$\uparrow$ 15%	NE
Liaw et al. [41]	$\uparrow$ 29%	$\uparrow$ 42%	NE	NE	NE	$\uparrow$ 66%	NE	$\uparrow$ 39%	$\uparrow$ 78%	$\uparrow$ 63%	$\uparrow$ 21%	$\leftrightarrow$	NE
Mueller et al. [28]	$\leftrightarrow$	$\uparrow$ 13%	$\leftrightarrow$	NE	NE	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	NE	$\leftrightarrow$	$\leftrightarrow$	NE	$\leftrightarrow$
Van Houtte et al. [42]	$\uparrow$ 28%	$\uparrow$ 25%	$\uparrow$ 10%	NE	NE	$\uparrow$ 6%	$\uparrow$ 9%	NE	NE	NE	NE	NE	NE
Roth et al. [43]	$\uparrow$ 51%	$\uparrow$ 56%	NE	NE	NE	$\uparrow$ 15%	NE	NE	NE	$\uparrow$ 15%	NE	$\leftrightarrow$	NE
Mueller et al. [44]	$\uparrow$ 298% ${}^{*}$	$\leftrightarrow$	NE	NE	NE	NE	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	NE	NE
Fischer et al. [45]	NE	NE	$\uparrow$ 23%	NE	$\uparrow$ 27%	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	NE	NE	$\leftrightarrow$
Postma et al. [46]	$\uparrow$ 47%	$\leftrightarrow$	NE	NE	NE	$\leftrightarrow$	$\leftrightarrow$	$\leftrightarrow$	NE	$\leftrightarrow$	NE	NE	NE
West et al. [8]	$\leftrightarrow$	$\leftrightarrow$	NE	$\leftrightarrow$	NE	$\leftrightarrow$	$\uparrow$ 12%	NE	NE	$\leftrightarrow$	NE	NE	$\leftrightarrow$
Kim et al. [47]	NE	NE	NE	NE	NE	$\uparrow$ 27% ${}^{\text{a}}$ $\uparrow$ 9% ${}^{\text{b}}$	NE	NE	NE	$\uparrow$ 39% ${}^{\text{c}}$ $\uparrow$ 10% ${}^{\text{d}}$	NE	NE	NE
Legg Ditterline et al. [48]	NE	NE	NE	NE	NE	$\uparrow$ 6%	NE	NE	NE	$\uparrow$ 8%	NE	NE	NE
Raab et al. [49]	$\uparrow$ 31% ${}^{\text{e}}$ $\uparrow$ 41% ${}^{\text{g}}$	$\uparrow$ 42% ${}^{\text{f}}$ $\uparrow$ 51% ${}^{\text{h}}$	NE	NE	NE	$\uparrow$ 16% ${}^{\text{e}}$ $\uparrow$ 37% ${}^{\text{g}}$	NE	$\uparrow$ 13% ${}^{\text{f}}$ $\uparrow$ 23% ${}^{\text{i}}$	NE	$\uparrow$ 22% ${}^{\text{e}}$ $\uparrow$ 28% ${}^{\text{g}}$	NE	NE	NE
Soumyashree and Kaur [50]	$\uparrow$ 35%	$\uparrow$ 51%	NE	NE	NE	NE	NE	NE	NE	NE	NE	NE	$\uparrow$ 101%

MIP $=$ maximal inspiratory pressure; MEP $=$ maximal expiratory pressure; RMV $=$ respiratory minute volume; DT $=$ diaphragm thickness; RMS $=$ respiratory muscle strength; FVC $=$ forced vital capacity; MVV $=$ maximal voluntary ventilation; PEF $=$ peak expiratory flow; VC $=$ vital capacity; FEV ${}_{1}$ $=$ forced expiratory volume in the first second; TLC $=$ total lung capacity; FRC $=$ functional residual capacity; VO ${}_{\text{2max}}$ $=$ maximal oxygen uptake; NE $=$ not evaluated. $\downarrow$ $=$ significant decrease in the mean value; $\leftrightarrow$ $=$ no significant change in the mean value; $\uparrow$ $=$ significant increase in the mean value. ${}^{*}$ Significant effect of IMT vs. placebo ( $P=$ 0.016). ${}^{\text{a}}$ significant changes in sitting and lying positions after IMT; ${}^{\text{b}}$ significant changes in lying position after EMT; ${}^{\text{c}}$ respiratory muscle training with bidirectional resistance combined with the abdominal drawing-in maneuver; ${}^{\text{d}}$ respiratory muscle training with bidirectional resistance; ${}^{\text{e}}$ average calculated from either changes observed in subjects with motor complete and incomplete lesion after IMT; ${}^{\text{f}}$ significant changes in subjects with motor incomplete lesion after IMT; ${}^{\text{g}}$ average calculated from either changes observed in subjects with motor complete and incomplete lesion after combined IMT and EMT; ${}^{\text{h}}$ significant changes in subjects with motor complete lesion after combined IMT and EMT; ${}^{\text{i}}$ significant changes in subjects with motor incomplete lesion after combined IMT and EMT.

The main reasons for studies’ ineligibility were the following: investigation of outcomes other than those that were the focus of the present study; application of interventions other than RMT; and investigation of populations without disabilities, or with health conditions other than SCI. Baseline experimental groups’ characteristics for age, sex, SCI levels and time postinjury are presented in Table 1. The characterization of the participants of the selected studies is shown in Table 1.

3.2 Studies’ methodological quality

Among the 17 included studies, only seven presented scores $\geqslant$ 6 in the PEDro scale [28, 42, 41, 44, 46, 47, 50], emphasizing that most of these studies had methodological limitations that may compromise the findings. It was observed that the studies with higher scores and with larger sample sizes were published from 2008, highlighting the randomized controlled trial by Soumyashree and Kaur [50] that achieved the highest quality score on the PEDro scale, and a study by Raab et al. [49] involving a total of 79 participants (i.e. the highest sample size). The PEDro scale items that presented the highest negative evaluation frequency were the following: blinding of therapists ( $n=$ 14); presentation of precision and variability measurements ( $n=$ 12); blinding of subjects ( $n=$ 11); blinding of evaluators ( $n=$ 11); and concealed allocation of research subjects ( $n=$ 11).

3.3 Analysis through FITT principle

3.3.1 Inspiratory muscle training (IMT)

The nine studies that applied the IMT presented vast heterogeneity with regard to frequency, intensity and time components of exercise prescription [36, 38, 39, 41, 44, 46, 8, 49, 50]. The average of weekly frequency was 5.3 $\pm$ 1.0 (ranging from 4 to 7) days $\cdot$ week ${}^{-1}$ , whereas most of the experimental groups underwent twice sessions per day [36, 38, 39, 41, 8]. The IMT intensity prescription ranged from $\sim$ 33% to 85% of maximal inspiratory pressure (MIP) [44, 46, 49, 50, 39]. Three studies did not report this information [38, 41, 8]. The average follow-up training period was 6.7 $\pm$ 1.5 (ranging from 4 to 8) weeks. Six studies prescribed continuous training, ranging from 10 to 30 min [36, 38, 39, 41, 44, 50]. The main investigated outcomes were pulmonary function outcomes [36, 38, 39, 41, 44, 46, 8, 49] and cardiorespiratory fitness [8, 50].

Table 2 presents the main physiological outcomes from the included studies by the present systematic review. The changes in physiological parameters after RMT are presented in relative values (i.e. average post-RMT minus average pre-RMT). For athletes, the findings of West et al. [8] from five Paralympic wheelchair rugby players (age, 30.5 $\pm$ 2.2 years) with motor-complete SCI (C5-C7) showed that IMT significantly improves diaphragm thickness – DT ( $\uparrow$ 21%), maximal voluntary ventilation – MVV ( $\uparrow$ 12%), and maximal work rate ( $\uparrow$ 15%), whereas a strong trend effect towards an increase in VO ${}_{\text{2max}}$ ( $\uparrow$ 18%, $P=$ 0.077) and a decrease in respiratory rate – $f$ R ( $\downarrow$ 12%, $P=$ 0.081) were also observed after 6-week of IMT. For non-athletes, IMT promoted significant increases in pulmonary function parameters, such as: forced vital capacity – FVC [38, 39, 41]; forced expiratory volume in the first second – FEV ${}_{1}$ [39, 41]; MVV [38]; peak expiratory flow – PEF [38, 41]; total lung capacity – TLC [41]; MIP [36, 38]; maximal expiratory pressure – MEP [41]; and respiratory muscle strength – RMS [44]. However, the findings of Loveridge et al. [36] and Liaw et al. [41] revealed similar and significant changes to either the experimental or the control groups, which limits understanding regarding the efficacy of IMT on physiological parameters. The study of Postma et al. [46], for example, did not observe any physiological change after an 8-week IMT intervention in nineteen SCI individuals.

3.3.2 Respiratory muscle training (RMT) with bidirectional resistance

Seven studies used RMT with bidirectional resistance [40, 28, 43, 45, 47, 48, 49]. Kim et al. [47], for example, investigated the effects of RMT combined with the abdominal drawing-in maneuver (ADIM) on pulmonary function in one of the intervention groups. On average, the follow-up period and the weekly frequency were 6.4 $\pm$ 1.7 weeks and 5.0 $\pm$ 1.4 (ranging from 3 to 7) days $\cdot$ week ${}^{-1}$ , respectively. Regarding daily frequency, four studies prescribed once a day [28, 45, 47, 49] and three studies twice a day [40, 43, 48].

None of the seven studies provided details about the methods used to calculate the initial training intensity. Three studies prescribed continuous training, ranging from 15 to 30 min [40, 28, 45, 48], while one study used 1 set of 10 repetitions [43]. The study of Kim et al. [47] adopted 5 sets of 10 MIP sustained for 3–4 seconds.

The main physiological outcomes investigated by the studies that adopted RMT with bidirectional resistance were pulmonary function [40, 43, 45, 47, 49], respiratory muscle resistance [45], respiratory muscle strength [40, 49], cardiorespiratory fitness [28, 45, 50], and spontaneous baroreflex sensitivity and cardiac autonomic control [48]. For athletes, RMT with bidirectional resistance was able to improve minute ventilation [45], MEP [28], respiratory muscle resistance [28], dyspnea [45], while no significant difference was observed after the interventions for VO ${}_{\text{2max}}$ [28]. In those who were non-athletes, significant increases were observed in FVC [40, 47, 48], FEV ${}_{1}$ [47, 48], MIP [40, 43, 49], MEP [43, 49], TLC and functional residual capacity – FRC [40].

3.3.3 Expiratory muscle training (EMT)

Two studies applied EMT [37, 39], while one of them combined EMT with abdominal electrostimulation [39]. Both studies were conducted with non-athlete SCI individuals and had pulmonary function [37, 39] and cough efficacy as outcomes [39]. The study of Gounden [37], for example, observed a significant increase in vital capacity (VC) and in MEP after 8-week of EMT at 60% MEP (6 days $\cdot$ week ${}^{-1}$ , 5 times.day ${}^{-1}$ , totaling 30 min.day ${}^{-1}$ ). The authors highlighted the effort intensity progression of 5 to 10% MEP at two weekly intervals to ensure optimal intensity throughout the training period. Zupan et al. [39] prescribed 8-week of RMT (i.e. 4-week of IMT, followed by 4-week of EMT, and 4-week without training) accompanied by electrical stimulation (ES) of the abdominal muscles in 13 tetraplegic patients. The IMT approach apparently showed a slightly greater effect on FVC and FEV ${}_{1}$ than EMT (see Table 2). Besides that, changes in FVC and FEV ${}_{1}$ were improved when RMT was combined with ES of abdominal muscles, improving coughing in tetraplegic patients.

3.3.4 Normocapnic hyperpnoea training (NHT)

Two studies evaluated the effects of NHT in non-athlete SCI individuals [42, 44]. Van Houtte et al. [42] investigated the effect of 8-week of NHT at 30 to 40% MVV [i.e. (4 days $\cdot$ week ${}^{-1}$ , once a day, 30 min $\cdot$ day ${}^{-1}$ ) with respiratory rate (RR) maintained between 30 and 45 respiratory incursions per minute] on pulmonary function parameters of seven patients with acute SCI. Compared to the control group, significant and positive changes were observed for MVV, MIP, MEP and respiratory minute volume (RMV) after NHT. On the other hand, the NHT protocol adopted by Mueller et al. [44] in eight individuals with tetraplegia was able to induce only a significant change in MIP after 8-week at 40–50% MVV (4 days $\cdot$ week ${}^{-1}$ , once a day, 10 min $\cdot$ day ${}^{-1}$ ).

4. Discussion

Several studies have shown the effectiveness of RMT interventions in different diseases, such as heart failure [51, 52], chronic obstructive pulmonary disease [53], multiple sclerosis [54] and asthma [55], as well as in some sports modalities [56, 57, 58, 59]. This type of training induces benefits in respiratory muscle strength and resistance and, consequently, in pulmonary ventilation. Hence, it may improve the overall functioning of organic systems, especially for individuals with cardiorespiratory limitations during exercise [51, 13]. Individuals with SCI are an example of people who present cardiopulmonary limitations, due to postural changes, abdominal muscle weakness, thoracic hypomobility, impairment of the respiratory center or phrenic nerve (in the case of high cervical injuries), among other reasons [60, 10]. Improvements in respiratory muscle strength and resistance may blunt these limitations, providing a better overall health status, particularly of the respiratory system. Compared to baseline or intergroups, all 17 studies investigated by the present systematic review showed significant and beneficial differences in at least one of the resting ventilatory variables considered after the use of RMT. Therefore, the use of RMT should be considered for SCI individuals, regardless of fitness status (i.e. athletes or non-athletes).

The main positive findings for non-athlete populations were related to pulmonary function. This may be explained by the inspiratory muscle metaboreflex mechanism, which is altered in SCI individuals due to partial or total interruption of afferent and efferent pathways and physiological changes in autonomic nervous system (ANS) [61, 62]. According to Dempsey et al. [63], the metaboreflex mechanism occurs during high-intensity physical activities with sustained exercise (e.g. VO ${}_{\text{2max}}$ $>$ 80%), when the diaphragmatic muscle recruitment is greater, provoking central fatigue. At this moment, there is an afferent activation of type IV phrenic pathways, leading to sympathetic vasoconstriction activity in the skeletal muscle. This system regulates the blood circulation competition between the respiratory and skeletal muscles during exercise in healthy individuals [63]. It is known that the inspiratory pressure reached during high-intensity exercise is substantially lower than normal levels due to the mentioned metaboreflex mechanisms and neural control. Thus, the pulmonary volumes also do not reach their maximal capacity [63].

SCI individuals present particular characteristics with regards to respiratory physiology and ANS, in relation to sympathetic and parasympathetic activity [10]. Such particularities preclude the metaboreflex mechanism from acting in the same way as in individuals with no disabilities [61, 62]. The neurological level of SCI is also a determinant of respiratory capacity deficits. Paraplegic individuals normally present expiratory muscles (abdominal) limitations, while quadriplegics are affected by inspiratory deficits [64]. Haisma et al. [65] demonstrated that FEV ${}_{1}$ in paraplegics may reach 90% of the volume reached by healthy individuals of the same age and body composition. On the other hand, in quadriplegics FEV ${}_{1}$ reaches only 60% of the level observed by people with no disability. Respiratory limitations during physical exercise associated with SCI can lead to clinical complications and to a drop in sports performance. In view of this, RMT could increase exercise tolerance and minimize common respiratory complications in people with SCI, since this type of training is able to delay the occurrence of diaphragmatic fatigue [66].

Notwithstanding, after this review, it was not possible to conclude what would be the most appropriate protocol and type of RMT to maximize improvements in respiratory capacity. Table 1 demonstrates that there is a huge variety in the components of the FITT principle applied to the RMT, which may hamper comparisons between the methods. In addition, the variables used to investigate similar outcomes were different, and it was not possible to compare some of the results of the studies.

Some studies already evidenced that RMT may improve the athletic performance in several sport modalities among individuals without disabilities [67, 68, 58]. In this context, exercise tolerance [67, 69, 68, 70, 71] and reduced incidence of respiratory diseases [71] have been described in the scientific literature. However, the most recent findings are controversial regarding the real benefits of RMT on cardiorespiratory fitness (i.e. VO ${}_{\text{2max}}$ ). HajGhanbari et al. [72], for example, performed a systematic review that identified 13 meta-analyses indicating that there was no positive effect on VO ${}_{\text{2max}}$ in non-disabled athletes after the use of RMT. Some authors have also found minimal [73] or no difference [56] in VO ${}_{\text{2max}}$ , which shows divergences about the effectiveness of RMT on the cardiorespiratory fitness improvement in non-disabled athletes.

With respect to SCI athletes, especially the ones who compete in sports in which optimum cardiorespiratory fitness is associated with better performance, it would be feasible to suppose that improvements in respiratory musculature could influence their performance. In the present systematic review, it was possible to observe that only studies involving SCI athletes assessed the cardiorespiratory fitness and none of them have found significant differences in VO ${}_{\text{2max}}$ after RMT [28, 45, 8]. The study of West et al. [8] was the only one to find an increased trend in VO ${}_{\text{2max}}$ ( $+$ 14%, $P=$ 0.077) after 6-week of RMT in wheelchair rugby athletes with C5 to C7 SCI levels.

The studies adopted distinct types of protocol and ergometers to evaluate cardiorespiratory fitness in SCI athletes, which may hamper comparisons and conclusions between results of the aforementioned studies regarding the effects of RMT on VO ${}_{\text{2max}}$ [28, 45, 8]. In this sense, Mueller et al. [28] evaluated the VO ${}_{\text{2max}}$ on an adapted treadmill using a continuous step-incremented protocol, where the athletes performed the 10-km time trial on their own racing wheelchair (i.e. initial work rate: 10 km/h and slope of 0.7%; increment ratio of 2 km/h every 3-min until volitional exhaustion), while Fischer et al. [45] and West et al. [8] adopted, respectively, a ramp protocol (i.e. initial work rate: women 30 W and men 50 W, increment ratio of 1 W each 6 s and 4 s, respectively), and continuous step-incremented protocol (i.e. initial work rate: 20 to 45 W, increment ratio of 5 W each 2-min), using the arm-crank ergometer. Furthermore, it is important to acknowledge the heterogeneity of the samples, since the functionality of the SCI individuals varies according to the neurological level. It is noteworthy, however, that respiratory muscles act simultaneously in the work of breathing and in exercises that require upper body movements, as during wheelchair propulsion [74]. Therefore, athletes with SCI who compete in modalities that require wheelchair propulsion can also benefit from the strengthening of respiratory muscles, even without significant gains in VO ${}_{\text{2max}}$ . Since inspiratory muscle fatigue may lead to impaired blood flow and blood perfusion in locomotor muscles, and earlier activation of the respiratory metaboreflex [75], limiting sports performance, the strengthening of respiratory muscles would be beneficial for athletes in this regard. Whereas sports performance is multifactorial, any adjustment that directly or indirectly influences the result in any magnitude is valid.

Finally, no study involving non-athletes with SCI evaluated the cardiorespiratory fitness – since VO ${}_{\text{2max}}$ is the best measure of long-term morbidity and mortality in able-bodied populations [76], and widely used to evaluate cardiorespiratory fitness and prescribe aerobic exercise programs in different populations [17], further research should evaluate the effect of RMT on VO ${}_{\text{2max}}$ in non-athletes with SCI.

This review presents limitations regarding the low number of experimental studies involving the target population. The scientific literature presents several gaps, especially concerning athletes, even though a robust bibliographical search was made. In addition to the small number of available studies, low methodological quality was observed in most of them. Studies involving athletes were more recent, but still presented with several methodological limitations, such as small sample size, heterogeneity of the sample, and blindness of the participants. Such limitations slow down the growth of scientific knowledge, preclude the verification of associations between RMT and the studied outcomes, and make it difficult to make inferences in reality.

5. Conclusion

This systematic review suggests that RMT improves pulmonary function and respiratory muscle strength and endurance, thereby deserving consideration as an additional intervention in athletes and non-athletes with SCI, although no associations were found between the RMT and cardiorespiratory fitness (i.e. VO ${}_{\text{2max}}$ ). However, considering the methodological quality of the articles included, the small sample sizes, short-term interventions, and the lack of a standardization in the experimental protocols from the FITT principle for RMT, it is feasible to think that new randomized controlled trials are needed on this subject, in order to elucidate the effectiveness of the RMT on health outcomes in athletes and non-athletes SCI individuals, according to the neurological level of the injury and the individual functionality, providing more subsidies for the specific work of coaching staff and health professionals, responsible for the physiotherapeutic treatment of this population. With the formulation of guidelines for more specific prescriptions, it is possible that the effects will be more consistent.

Footnotes

Acknowledgments

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001, the Carlos Chagas Filho Foundation for the Research Support in Rio de Janeiro State (FAPERJ) and the Brazilian Council for the Technological and Scientific Development (CNPq).

Conflict of interest

None to report.

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Respiratory muscle training in non-athletes and athletes with spinal cord injury: A systematic review of the effects on pulmonary function,respiratory muscle strength and endurance,and cardiorespiratory fitness based on the FITT principle of exercise prescription

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Protocol

2.2 Eligibility criteria

2.3 Information sources

2.4 Search

2.5 Studies selection

2.6 Data collection process

2.7 Risk of bias in each study

3. Results

3.1 General characteristics

Table 1 Characteristics of the RMT experimental groups’ protocols, considering the FITT principle for exercise prescription in athletes and non-athletes with SCI

3.3 Analysis through FITT principle

3.3.1 Inspiratory muscle training (IMT)

3.3.2 Respiratory muscle training (RMT) with bidirectional resistance

3.3.3 Expiratory muscle training (EMT)

3.3.4 Normocapnic hyperpnoea training (NHT)

4. Discussion

5. Conclusion

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Characteristics of the RMT experimental groups’ protocols, considering the FITT principle for exercise prescription in athletes and non-athletes with SCI