Effects of Inspiratory Muscle Training using Incentive Spirometer

on Aerobic Capacity, Functional Performance, and Quality of Life

of Individuals with Chronic Paraplegia from Spinal Cord Injury:

A Pilot Study

Nita Theresia Reyne

, Farida Arisanti

, Vitriana Biben

, Indriati M. S. Tobing

, Rosiana Pradanasari

Departement of Physical Medicine and Rehabilitation, Dr. Hasan Sadikin General Hospital,

University of Padjadjaran, Bandung, Indonesia

Departement of Physical Medicine and Rehabilitation, Fatmawati General Hospital,

University of Indonesia, Jakarta, Indonesia

Keywords: Inspiratory Muscle Training, Maximal Inspiratory Pressure, Functional Capacity, Quality of Life, Paraplegia.

Abstract: In spinal cord injury (SCI), partially or fully denervated inspiratory or expiratory muscles have impaired

contractility and exhibit diminished exercise ventilation and ventilatory reserve. Inspiratory muscle

training (IMT) using an incentive spirometer (IS) improve lung functions in individuals with chronic SCI.

This study aimed to investigate the effects of IMT-using-IS on the aerobic capacity, the functional

performance, and QoL individuals with chronic paraplegia. The quasi-experimental with the pre-post

design conducted at Sasana Bina Daksa Budi Bhakti Pondok Bambu Jakarta in January-February 2019.

The outcomes were the aerobic capacity measured with the 6-Minutes Push Test (6MPT), the functional

activities daily living (ADL) performance with the Spinal Cord Independence Measure III (SCIM III), and

QoL with International SCI Data Sets-Quality of Life Basic Data Set. There were 11 individuals with

chronic paraplegia recruited. After the IMT-using-IS 5 times per weeks for 4 weeks, there were

significant increases in the 6MPT (p=0.002), and the QoL score (p=0.004), however the SCIM scores

were not significantly different (p=0.271). Individuals with chronic paraplegia, the IMT-using-IS

significantly improved aerobic capacity and QoL. There was no effect on functional performance in ADL

as individuals with chronic paraplegia had already reached their highest level in performing ADL.

1 INTRODUCTION

Respiratory dysfunction frequently occurs in

individuals with spinal cord injury (SCI) due to the

loss of autonomic and somatic nerve control

resulting in complete or partial paralysis of the

respiratory muscles. Respiratory dysfunction

resulting from SCI remains a major cause of

morbidity, mortality, and economic burden (Kumar,

2016; Schilero et al, 2009; Sheel et al, 2008; Sisto

and Evan, 2014).

Respiratory muscle dysfunction in SCI leads to

mechanical alterations in inspiration which results in

decreased compliance of the lungs and chest wall.

This is due to the disruption of muscle strength of

the primary inspiratory muscles, the diaphragm, and

external intercostal muscle. The decreased

abdominal muscle function disrupts mechanical

respiration as well. Abdominal muscles play an

important role during inspiration through their tonic

activity, directly facilitating diaphragm muscle

contraction by preventing excessive contraction

during inspiration. In addition, the increased

intraabdominal pressure yielded by the abdominal

muscle contraction during expiration prepares the

respiratory system for the next inspiration by

optimizing the diaphragm muscle length-tension

(Berlowitz and Tamplin, 2013; Galeiras, 2013;

Schilero et al, 2009; Sheel et al, 2018).

Individuals with chronic SCI frequently

experience an alteration in ventilation, becoming

restrictive. The weak abdominal muscles and the

Reyne, N., Arisanti, F., Biben, V., Tobing, I. and Pradanasari, R.

Effects of Inspiratory Muscle Training using Incentive Spirometer on Aerobic Capacity, Functional Performance, and Quality of Life of Individuals with Chronic Paraplegia from Spinal Cord

Injury: A Pilot Study.

DOI: 10.5220/0009088001970203

In Proceedings of the 11th National Congress and the 18th Annual Scientiﬁc Meeting of Indonesian Physical Medicine and Rehabilitation Association (KONAS XI and PIT XVIII PERDOSRI

2019), pages 197-203

ISBN: 978-989-758-409-1

197

inability of deep inhalation cause increased

abdominal compliance and chest cavity stiffness

which results in the formation of a restrictive

respiratory pattern. This respiratory pattern will

reduce the ability to produce maximum minute

ventilation, then inhibit maximum oxygen uptake

(VO2 max), and ultimately limit physical activity

performance (Battikha et al, 2014). In addition, SCI

causes a loading shift from lower extremity to

upper extremity during exertion. Muscles in the

upper extremity are not weight-bearing muscles and

can only bear 60% of the workload compared to

lower extremity muscles, thus, causing early fatigue

in SCI patients. Inspiratory muscle dysfunction

decreases aerobic capacity, level of physical

activity, and moreover, leads to physical

deconditioning and decreased the independence and

performance in activities daily living (ADL) among

individuals with SCI (Berlowitz and Tamplin,

2013; Sisto and Evan, 2014). Physical exercise

represents an important therapeutic part of

successful mobility advancement and contributes

greatly to a rehabilitation process aiming at self-

determination and autonomy. Therefore, it also has

a great impact on quality of life (QoL) (Anneken et

al, 2010)

Respiratory muscle training is specific training

inspiratory, expiratory, or both muscles to increase

both muscles strength and endurance. There were

numbers of respiratory muscle training using in SCI

management, one of them was resistive inspiratory

muscle training (IMT). Various systematical reviews

showed improvement in lung function and

respiratory muscle strength in individuals with SCI

after training using resistive IMT technique. The

problem is that determining the intensity of resistive

IMT requires maximum inspiratory pressure (MIP)

measurement using a respiratory pressure meter

(RPM), in which the availability in Indonesia is

scarce and the price is quite expensive. Other

respiratory training methods were using an incentive

spirometer (IS). It is a device used in inspiratory

training which provides feedback when a patient

inhales a predetermined flow or volume and

maintains inhalation for at least five seconds. This

device is inexpensive, easy to apply and superior in

providing a visual feedback during training

compared to the resistive IMT. However, there are

no specific methods, frequency, and duration of

training recommended for pulmonary rehabilitation

in SCI, and thus, further studies are required. Prior

studies investigating IMT-using-IS with a frequency

of 5 times/week and duration of 8 weeks in chronic

paraplegia and tetraplegia SCI phase had shown

improvement in lung functions; however, its effect

to functional performance remains unknown

(Berlowitz and Tamplin, 2013; Kim et al, 2017;

Paiva et al, 2015).

This study was conducted to investigate the

effects of IMT-using-IS on aerobic capacity,

performance in ADL, and QoL of individuals with

chronic paraplegia from SCI.

2 METHODS

The quasi-experimental with the pre-post design was

conducted at Sasana Bina Daksa Budi Bhakti

Pondok Bambu Jakarta in January-February 2019.

Inclusion criteria for the participants were:

individuals with paraplegia from SCI more than six

months, age around 18 to 59 years, a stable spine,

being able to sit for 30 minutes and performing

voluntary ventilation; having the MMSE score more

than 24, the Hamilton Depression score less than 19,

no history of pulmonary disease or respiratory

symptoms, no any recent or active pulmonary

infection, and not receiving medication known to

alter airway tone. They were excluded if they could

not perform deep breathing due to pain or taking an

opiate, having a vital capacity of less than 10 mL/kg.

They will be dropped out from the study if they did

not perform the exercise in 72 hours, wanted to quit

from the study, and had unstable medical conditions

(Kim et al, 2017). All participants gave written

informed consent. The protocol was approved by the

Research Ethics Committee of Universitas

Padjadjaran, Bandung, Indonesia with registration

number 0318050788.

The primary outcomes measured were aerobic

capacity, performance in ADL, and QoL. The

secondary outcomes were lung function and

inspiratory muscle strength. Measurements were

administered before and after the intervention

period.

The aerobic capacity was determined with 6MPT

based on the American Thoracic Society guidelines

(Cowan, Callahan and Nash, 2012). The participants

were tested in their wheelchair. The ability to do

ADL and the QoL were assessed with

KONAS XI and PIT XVIII PERDOSRI 2019 - The 11th National Congress and The 18th Annual Scientiﬁc Meeting of Indonesian Physical

Medicine and Rehabilitation Association

198

Figure 1: Inspiratory muscle training with incentive

spirometer.

questionnaires, the SCIM III and the International

SCI Data Sets-QoL Basic Data Set, respectively.

(Catz et al, 2007; Charlifue et al, 2012). Lung

function was measured with a spirometer MicroLab

ML3500 M5 (Amplivox, Birmingham, USA) by a

skilled nurse. Three repeated ﬂow volume curves

were performed. Outcomes that analyzed was the

score of the trial with the highest value of three close

test readings (Miller et al, 2005). Respiratory muscle

strength was determined with MIP by using a Micro

RPM (CareFusion, Yorba Linda CA, USA). The

highest value of three maneuvers that varied less

than 5% from the next value was recorded and used

for analysis (Postma et al, 2014).

In this study, an incentive spirometer (Voldyne®

5000 volumetric exerciser, Hudson RCI, Temecula

CA, USA), was used for IMT. All measurements

and exercise, except lung function, were conducted

by a physician. The participants were instructed to

hold the spirometer in an upright position, exhaled

normally, and then placed the lips tightly around the

mouthpiece. The next step was a slow inhalation to

raise the piston/plate (volume-oriented) in the

chamber to the set target (Figure 1). At maximum

inhalation, the mouthpiece is removed, followed by

a breath-hold and normal exhalation (Restrepo et al,

2011). All subjects completed 20 supervised training

sessions, 5 times a week for 4 consecutive weeks. A

total of five sets of 10 repetitions made up one

session. After each set, a one-minute rest was

allowed. If participants complained of fatigue or

dizziness during the If participants complained of

fatigue or dizziness during the respiratory exercise,

they took a short rest and then proceeded with the

exercise. If these symptoms became severe, they

were asked to stop the exercise (Kim et al, 2017).

Data were analyzed using SPSS 24.0 for

Windows (SPSS Inc., Chicago, IL, USA). The

paired T-test and the Wilcoxon signed rank test were

used for statistical analysis.

3 RESULTS

Thirteen paraplegics (12 males, 1 female)

participated in the study, however, only 11

completed the study. Two participants were

excluded because they did not want to continue the

study due to personal reason. No complication was

reported. Demographic data and characteristics of

the participans were shown in Table 1.

The demographic characteristics of this study

subjects were dominated by the male (90.9%),

underweight (63.6%), and had the same average and

median age (44 years). Other factors affecting

respiratory function assessment are cigarette

smoking, level of injury, and comorbid respiratory

system diseases, such as post-tuberculosis

obstruction syndrome, pneumonia, chronic

obstructive pulmonary disease, and asthma. About

81.8% of research subjects were smokers with

filtered cigarettes, about 4–8 cigarettes per day, for

20 years on average. Based on the Brinkmann Index,

they were classified into mild active smokers and

they did not show signs and symptoms of respiratory

obstruction at the time of the study. Their clinical

conditions were consistent with the results of

spirometry without bronchodilators: mild-moderate

or normal restrictive, averagely. Based on history

and physical examination, neither the history nor the

presence of active respiratory system diseases were

found, including subjects who had the etiology of

SCI i.e. spondylitis tuberculosis.

From table 2, the distance of 6MPT (p=0.002)

and the QoL score increased (p=0.008) are

improving, however, the SCIM III score did not

show any significant improvement (p=0.271),

although the participants mentioned that performing

ADL and work was easier, lighter and/or faster after

the study ended. There were significant

improvement on lung function, FVC (p=0.005) and

FEV1 (p=0.007), as well as the MIP (p=0.0001). It

proved that respiratory training using IS not only

improves the lung function but also able to increase

the inspiratory muscle strength.

Effects of Inspiratory Muscle Training using Incentive Spirometer on Aerobic Capacity, Functional Performance, and Quality of Life of

Individuals with Chronic Paraplegia from Spinal Cord Injury: A Pilot Study

199

Table 1: Characteristics of subjects.

Variables n=11

Age (year-old) 44.27±7.69

Gender (male/female) 10(90.9%)/1(9.1%)

Bodyweight (kilogram) 51.09±6.64

Body height (centimeter) 165.09±5.90

BMI 18.72±2.17

Underweight 7(63.6%)

Normal 3(27.3%)

Overweight 1(9.1%)

Vocational

Craftsman 10(90.9%)

Mechanic 1(9.1%)

Smoking status 9(81.8%)

Duration of SCI (months) 259.63±104.37

AIS classification (Com/Inc) 10(90.9%)/1(9.1%)

Lesion Level

T2-T11 8(72.7%)

T12-L3 3(27.3%)

Respiratory Comorbid 0(0.0%)

MMSE>24 11(100%)

Severe depression 0(0%)

Categoric data are expressed as number/frequency and percentage, numerical data as mean ± standard deviation. BMI, body

mass index; AIS, American Spinal Injury Association Impairment Scale; T, thoracic; L, lumbar.

4 DISCUSSIONS

The demographic data is consistent with the existing

epidemiology data in Indonesia that reported the

majority of SCI patients were young adult males of

productive age (Departemen Rehabilitasi Medik

RSUP Fatmawati, 2015). The National Spinal Cord

Injury Statistical Center Data in Birmingham

reported that men and women ratio was 4:1, with

average age of 27 years and highest occurrence at

the age of 19 years (National Spinal Cord Injury

Statistical Center, 2016). The results of respiratory

function are influenced by several variables such as

age, height, and sex, thus, they could become the

confounding factors in this study (Kim et al, 2017).

However, these confounding factors had been

minimized in this study. SCI lesions in this study

were dominantly complete lesions (according to the

American Spinal Injury Association Impairment

Scale criteria), most injuries were in the level of T2-

T11, and the highest is T5; or they could be

classified as high paraplegia where the nervous

system disorders affected the respiratory muscles,

both inspiratory (especially the muscles of chest

wall), and expiratory muscles (McConell, 2013).



The most frequently used method for assessing

physical activity is self-report by questionnaire.

However, the existing questionnaire is not sensitive

to the SCI population because it does not calculate

ambulation using a wheelchair as in most individuals

with SCI. The existing self-reports in the disabled

population do not assess an important part of

physical activity as well, i.e. intensity. The PARA-

SCI, a specific self-report of the SCI population, is

still developed (Ginis et al, 2005).

 The level of

activity of all research subjects tended to be similar,

i.e. ADL and working. Most of the study subjects

were craftsmen and spent their leisure time by

browsing online and singing. MMSE results showed

all the subjects could follow the instruction of the

exercise. Hamilton Depression results showed no

depression that could interfere the exercise

compliance.

Respiratory muscle dysfunction in SCI,

especially in those with tetraplegic, leads to

mechanical alteration in the inspiratory process

which results in decreased breathing efficiency,

reduced maximum static respiratory pressure, the

inability of inhalation and reduced lung volume.

These can be measured by FVC, FEV

, and MIP.

The FVC, FEV

and MIP values in tetraplegia and

paraplegia (both high and low paraplegia) were

proven to be lower than the predicted value of able-

bodied population (Berlowitz and Tamplin, 2013;

Schilero et al, 2009; Sheel et al, 2008).

KONAS XI and PIT XVIII PERDOSRI 2019 - The 11th National Congress and The 18th Annual Scientiﬁc Meeting of Indonesian Physical

Medicine and Rehabilitation Association

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Table 2: Comparison of lung function, inspiratory muscle strength, aerobic capacity, independence in ADL, and QoL pre-

and post-intervention

Variables Pre- (n=11) Post- (n=11) p value

Lung function

FVC (liter) 2.32±0.55 2.59±0.62 0.005**

FEV

(liter) 2.16±0.59 2.40±0.65 0.007**

MIP (cm H

0) 43.81±2.48 52.72±5.78 0.0001**

6MPT (meter) 390.63±57.59 477.72±76.60 0.002**

SCIM III scores

Self-care 20.00 20.00 1.000

Respiration and sphincter management 33.54±4.52 34.00±4.44 0.138

Mobility 17.72±1.55 17.72±1.61 1.000

Total 71.27±4.00 71.72±3.90 0.271

QoL

General QoL (overall well-being) 5.54±1.507 6.54±1.368 0.008**

Rating of physical health 5.27±0.786 6.63±1.026 0.004**

Satisfaction with psychological health 5.36±0.924 6.81±0.981 0.004**

Mean ± SD **p value<0,05: statistically significant different. SD: Standard Deviation; FVC: Forced Vital Capacity; FEV

Forced Expiratory Volume in 1 minute; MIP: Maximal Inspiratory Pressure; 6MPT: 6-Minutes Push Test; SCIM III:

Spinal Cord Independence Measure III; QoL: Quality of life

2013;

Similar results appeared in this study with an

average predictive value of 67% when compared to

able-bodied population. These lung function results

were following the average pre-intervention MIP.

Based on the calculation of the predictive respiratory

muscle strength in able-bodied population by Evans

and Whitelaw (2009), the predicted MIP in

individuals with SCI was shown below normal

(68.6–101.96 cmH

O). These could be influenced by

the severity (complete/incomplete) and lesion level,

duration of injury, and relatively lower (than able-

bodied individuals) physical activities. The value of

lung function and muscle strength are related to one

another. The pressure yielded during inspiration and

expiration is resulted from the activities of

respiratory, diaphragm, intercostal and abdominal

muscles. An increase in transpulmonary pressure of

1 cm H

O will increase lung volume by 200 ml

(Guyton and Hall, 2006). The increased lung volume

results from the increase in respiratory muscle

strength. This principle applies to the IMT-using-IS.

This was evidenced by the statistically significant

increase in post-intervention FVC, FEV

and MIP.

Although the current study had a shorter duration,

the results were consistent with the study conducted

by Kim et al. (2017), which reported an increase in

FVC and FEV

after administration of IMT-using-IS

and abdominal drawing-in for 8 weeks. May be the

difference is the gain of improvement of lung

function. The increased skeletal muscle strength due

to physical exercise occurs, especially, within the

first 2 weeks of exercise, precedes an increase in

muscle mass (Johnson, Sharpe and Brown, 2007).

Previous study has shown that paraplegic and

tetraplegic subjects have more restricted pulmonary

and cardiovascular responses to exercise and

significantly lower peak oxygen consumption and

minute ventilation than uninjured controls. It has

also been suggested that the loss of function of the

abdominal muscles, especially in individuals with an

injury level above T7, can limit the ability to meet

increasing expiratory requirements that occur in

moderate to intense activities. It might be the reason

that inspiratory and expiratory pulmonary deficits

consequent to SCI impair ventilation during exercise

and contribute to the lower peak oxygen

consumption

; however, it could be improved by

training (Battikha et al, 2014). Assessing the

wheeling distance for 6MPT is an easy, validated

way to measure aerobic capacity in individuals with

SCI (Cowan, Callahan and Nash, 2012). This study

showed a statistically significant increase in 6MPT

before the intervention (390.63±57.59 meters) and

after the intervention (477.72 ±76.60 meters).

The effect of IMT on exercise tolerance and/or

performance in SCI is less clear.

 In able-bodied

individuals, IMT may reduce the severity of

respiratory and/or locomotor muscle fatigue by

attenuating or delaying the respiratory muscle

metaboreflex. In SCI, it is unclear if exercise

imposes sufficient stress to induce a respiratory

muscle metaboreflex. Although the mechanisms

underlying the increase in VO

peak remain elusive,

some researchers speculate that increased aerobic

capacity may be caused by an increase in diaphragm

strength and/or a change in rib-cage configuration.

Effects of Inspiratory Muscle Training using Incentive Spirometer on Aerobic Capacity, Functional Performance, and Quality of Life of

Individuals with Chronic Paraplegia from Spinal Cord Injury: A Pilot Study

201

Conceivably, both changes may result in a greater

circulatory pump action of the diaphragm and/or

prevention of the transition to a predominant rib-

cage contribution to inspiration during the latter

stages of exercise, which may have the net effect of

increasing venous return, stroke volume, and O

delivery. It is equally possible, however, that any

improvements in aerobic performance may occur by

way of relieving the sensation of respiratory

discomfort (Taylor, 2016).

The functional ability and performance in SCI

depends on several factors, such as level of injury,

muscle strength, aerobic capacity, and motivation.

The administration of IMT is expected to increase

aerobic capacity, and ultimately improve functional

performance in individuals with SCI. The SCIM III

questionnaire is a tool for evaluating the level of

independence in ADL comprehensively in

individuals with SCI. The pre-intervention self-care

subscale of SCIM III in this study had reached the

maximum score (100%), indicating that all study

subjects had fully rehabilitated, and were able to

perform self-care independently. Respiration and

sphincter management subscale scored had reached

its maximum value, indicating that the study

subjects were breathing independently and had fully

rehabilitated for bowel bladder management.

However, the extent to which lung function, will

affect aerobic capacity in individuals with SCI is

below the normal range of able-bodied individuals.

This is primarily influenced by the severity and level

of SCI lesion, as well as relatively lower (than able-

bodied individuals) physical activities which

worsens respiratory capacity and ultimately affects

the aerobic capacity in individuals with SCI

(Anneken et al, 2010; Taylor, 2016). The mobility

subscale had reached the maximum score, while

others could still be improved by IMT intervention,

as seen in this study, although the improvements

were not statistically significant. The statistically not

significant difference in the results of SCIM III was

due to the high score of pre-intervention results,

called the ceiling effect. We propose International

Spinal Cord Injury Data Sets-Activities and

Participation Basic Data Set, which has a

performance ratings provide insight in the actual

functioning of persons with SCI in the rehabilitation

setting or in the community and

the point of view of

perceived difficulty or satisfaction with

performance; or, Comprehensive ICF Core Set for

Spinal Cord Injury-chronic situation, which has a

qualifier.

Although the results of SCIM III in this study

were statistically not significant, some subjects

reported improvement after the intervention. Most of

them found it easier, lighter and/or faster when

doing ADL, thus, they were more motivated to do

ADL. Two subjects who previously complained

neuropathic pain associated with SCI reported that

the pain was reduced by the third week of training.

A study conducted by Hicks et al. (2003) reported

that training could improve the psychological well-

being of populations with SCI, such as reducing pain

and depression. This was evidenced by the

statistically significant increase in the value of The

International SCI data sets for QoL, which consisted

of general QoL (overall well-being), rating of

physical health, and satisfaction with psychological

health. QoL is an important aspect of a complete

outcome evaluation to document the effects of

rehabilitation for persons with disabilities, including

those with SCI. SCI event is unexpected and

dramatically alters the course of an individual’s life.

It causes sudden, often devastating damage to the

central nervous system, with potential adverse

effects in multiple body systems. Individuals with

SCI must relearn basic skills such as eating, bathing,

dressing, and driving. Living with SCI may also

require the use of adaptive technologies such as

manual or power wheelchairs, all of which greatly

affect QoL. Individuals with SCI also often have to

cope with altered social roles and psychiatric

comorbidities including reactive depression and

anxiety disorders. These issues represent major

challenges to living with SCI. Therefore, anything

we can do for the QoL of an individual with SCI is

worth it (Tulsky et al, 2015). As well as the

experience in this study, although they were chronic

cases that could cope with SCI, they should be

persuaded for the exercise.

The limitation of this study was that the detailed

physical activity of subjects, as a potential

confounding factor, was not recorded and assessed

due to the lack of a questionnaire that could

accommodate the activities of individuals with SCI.

We suggest future studies with a large sample and/or

different research designs (randomized controlled

clinical trials). We also suggest future studies

focusing on subacute phase SCI to assess the effect

of IMT on improving the functional training

performance, shortening the length of stay, and

reducing treatment cost.

5 CONCLUSIONS

Individuals with chronic paraplegia from SCI often

survived with a lot of functional disabilities

KONAS XI and PIT XVIII PERDOSRI 2019 - The 11th National Congress and The 18th Annual Scientiﬁc Meeting of Indonesian Physical

Medicine and Rehabilitation Association

202

including respiratory that can lead to physical

inactivity and deconditioning that affect the QoL.

Our study shows that the inspiratory muscle training

with an incentive spirometer 5 sets of 10 repetitions

per day, 5 days per week for 4 consecutive weeks,

could improve lung function, inspiratory muscle

strength, increase aerobic capacity and quality of

life, but not functional of individuals with chronic

paraplegia from SCI that had fully rehabilitated.

Therefore, it is encouraged to add IMT-using-IS in

the management of chronic SCI to improve aerobic

capacity and QoL.

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