The Effect of Additional Inspiratory Muscle Strengtening on Aerobic

Exercise in Systemic Lupus Erythematosus: A Preliminary Study

Zayadi Zainuddin

1,2

, Marina Moeliono

, Novitri

, Laniyati Hamijoyo

3,4

, Irma Ruslina Defi

Physical Medicine and Rehabilitation Departement, Medical Faculty of Universitas Padjajaran, Bandung, Indonesia

Medical Program Study, Medical Faculty of Universitas Bengkulu, Bengkulu, Indonesia

Rheumatology Division, Internal Medicine Departement, Medical Faculty of Universitas Padjajaran, Bandung, Indonesia

Lupus Study Group, Imunology Study Centre, Medical Faculty of Universitas Padjajaran, Bandung, Indonesia

zay_adi@yahoo.co.id, mmmoeliono@yahoo.com, novitris@gmail.com, hamijoyo@yahoo.com, irmaruslina@gmail.com

Keywords: Inspiratory Muscle Strengthening, Aerobic Exercise, Systemic Lupus Erythematosus

Abstract: Background: Aerobic exercise, an effective and safe nonpharmacological treatment for systemic lupus

erythematosus (SLE), does not prevent muscle strength decline that has been proven to be predictor of

decreased functional capacity. A decrease of inspiratory muscle strength had been demonstrated in SLE.

This study aimed to explore the effect of adding inspiratory muscle strengtening (IMS) to aerobic exercise

in SLE patients. Method: A quasi experimental study with pre-post test was conducted. Study sample was

11 patients low lupus activity disease state (LLDAS), age 20-50 years, normal body mass index.

Interventions were aerobic exercise (3 times/week, moderate intensity, 20 minutes, using treadmill) and

IMS (3 times/week, low intensity, using respironic tresshold). The outcomes were inspiratory and handgrip

muscle strength, cardiopulmonal and handgrip muscle endurance. Results: The median of inspiratory

muscle strength (49.66 vs 65.00 cmH

O) and handgrip (11.00 vs 14.67 kilograms) increased (P<0.005)

significantly prior compared to after exercise. The median of cardiopulmonary endurance (432.00 vs 480.00

meters) also increased (P<0.005) significantly but not handgrip muscle endurance (1.50 vs 2.36 minutes).

Conclusion: The addition of inspiratory muscle strengtening to aerobic exercise did not only increase

cardiopulmonary function but also handgrip muscle strength which is usefull in daily activities.

1 INTRODUCTION

The decrease in physical fitness is common in

systemic lupus erythematosus (SLE). Balsamo et al.

showed that SLE patients walked shorter distances

on the six minute walking test (6MWT) and were

significantly associated with lower quality of life

(Balsamo, 2013). Another study, conducted by

Spinelli et al showed decreased in aerobic capacity

correlated with decreased cardiopulmonary

endurance of SLE patients (Spinelli et al, 2017).

Decreased skeletal muscle strength had also been

shown in SLE patients. Balsamo et al found that

premenopausal SLE patients with low disease

activity showed lower muscle strength and

functional capacity, and fatigue (Balsamo et al,

2013).

Many studies have been carried out related to

pharmacological and non-pharmacological

management strategies for SLE patients with

(Shaharir and Gordon, 2016). A systematic review

proved that aerobic exercise was an effective and

safe therapy in patients with mild to moderate

activity of SLE (Wu et al, 2017). Other study

showed that aerobic exercise was better than muscle

strengthening exercises in improving the quality of

life of SLE patients, although they still suggest the

addition of muscle strengthening exercises (Abrahão

et al, 2016). Soriano et al pointed out the importance

of muscle strengthening exercises, because lower

muscle strength has been shown to be a predictor of

decreased functional capacity over time in SLE

patients. (Soriano-Maldonado et al, 2016).

Related to the respiratory muscles, Amra et al.

mentioned a decrease in maximal inspiratory

pressure (MIP) and maximal expiratory pressure

(MEP) in SLE patients (Amra et al, 2006). Currently,

there are no study related to IMS exercises in SLE

patients. While IMS exercises has been shown to be

safe and positive effect in health and also other

chronic disease populations such as multiple

sclerosis (Ray et al, 2013), sarcoidosis (Karadall et

162

Zainuddin, Z., Moeliono, M., Novitri, ., Hamijoyo, L. and Deﬁ, I.

The Effect of Additional Inspiratory Muscle Strengtening on Aerobic Exercise in Systemic Lupus Erythematosus: A Preliminary Study.

DOI: 10.5220/0009066701620167

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 162-167

ISBN: 978-989-758-409-1

al, 2016) and chronic kidney disease (de Medeiros et

al, 2017).

This preliminary study aims to determine the

effect of additional IMS on aerobic exercise in SLE

patients.

2 METHOD

This study design was a quasi experimental with

pre-post test. The study was conducted September

2018-February 2019 at Departement of Physical

Medicine & Rehabilitation, Dr. Hasan Sadikin

General Hospital, Bandung. This study has obtained

ethical approval number

LB.04.01/A05/EC/314/XI/2018 from hospital ethics

committee.

Target population was SLE patients who had

routine medical treatment at Rheumatology Clinic,

Departement of Internal Medicine, Dr. Hasan

Sadikin General Hospital, Bandung. Sampling was

done consecutively. The sample size was obtained

by a 95% confidence level and 90% power of the

test.

Inclusion criteria were female, aged 20-50 years,

low lupus activity disease state (LLDAS) (Franklyn

et al., 2016), normal body mass index, and able to

walk independently. Exclusion criteria were history

of heart and lung disease, surgery on the thoracal

and or abdominal site, involved in aerobic exercise

and/or muscle strengthening in the last 6 months.

Elimination criteria were the subjects did not do

exercise 3 times consecutively for 1 week.

Interventions were aerobic exercise and

inspiratory muscle strengthening 3 times a week in,

12 weeks period. Aerobic exercise was given at

moderate intensity (40% of heart rate reserve/HRR),

20 minutes duration, using treadmill. IMS with a

mild intensity (30% of MIP), 5 sets, 10 repetitions

per set, using respironic tresshold.

Outcomes of this study were inspiratory and

other peripheral muscle (handgrip) strength which

represents strength output, cardiopulmonary and

peripheral muscle (handgrip) endurance which

represents endurance output. Handgrip muscle was

selected because while not directly involved in both

exercises. In addition, handgrip muscles could

represent overall body muscle performance.

Measurement of IMS was performed using a micro

respiratory pressure meter (RPM) and

cardiopulmonary endurance using a 6 minute walk

test (6MWT) while the strength and endurance of

handgrip using a jamar hand dynamometer.

Figure 1: Research Pathway.

3 RESULT

3.1 Subject Characteristics

Table 1: Subject characteristics prior to exercise.

Characteristic

n=11

Age (years)

†

33.00 (22.00-49.00)

Body mass index °

21.36±2.440

Physical activity

(MET/week)

†

1040 (693-1400)

Duration of illness (years)

†

5.50 (1.33-18.33)

Corticosteroid dose use

(miligram/day)°

2.55 ± 0.93

Inspiratory muscle

sterngth (cmH

†

49.66 (23.33-87.00)

Handgrip muscle strength

(kilograms)

†

11.00 (9.00-23.00)

Cardiopulmonal

endurance (meter)

†

432.00 (201.00-492.00)

Handgrip muscle

endurance (minute)

†

1.50 (1.09-3.18)

Note: n=number of samples; °=normal data distribution

using mean±deviation standard; †=abnormal data

distribution using median (range).

Table 1 showed the characteristics of the research

subjects were age 33.0 years with a fairly wide range

(22.00-49.00 years) and 5.50 years of duration

Assessed for eligibility (n=29)

Excluded (n=15)

Not meeting inclusion criteria (n=12)

Decline to participated (n=3)

Other reason = 0

Sample (n=14)

Allocated to intervention (n=14)

 Received allocated intervention (n=14)

 Did not received allocated intervention (n=0)

Loss of follow up (n=0)

Discontinued intervention (pregnance and

having another daily routine) (n=3)

Analysis (n=11)

The Effect of Additional Inspiratory Muscle Strengtening on Aerobic Exercise in Systemic Lupus Erythematosus: A Preliminary Study

163

disease with also wide range (1.33-18.33 years).

Range of age and duration of disease were left wide

because this study was the first study including

strengthening exercise in our hospital. At the end of

this study, these data and results will provide a basis

for future studies. In addition, based on International

Physical Activity Questionairre (IPAQ), the average

of physical activity of research subject was minimal

active.

Table 1 also showed the research subjects were

have good cardiopulmonal endurance but low

strength of the inspiratory and handgrip muscles.

These results indicate that SLE patients, although

they have good cardiopulmonary endurance, still

have low peripheral muscle strength including the

inspiratory and handgrip muscles. Good

cardiopulmonary endurance can be explained by the

fact that this group consisted of patients in LLDAS

category and minimaly active according to IPAQ.

Meanwhile, results showed low muscle strength.

Therefore, muscle strengthening is still needed in

SLE patients as an addition to aerobic exercise to

prevent decreased functional capacity.

In this study, IMS were chosen because it has

additional effect in improving oxygen supply to

peripheral muscles and also decrease the effects of

metaboreflexes on other peripheral muscles.

3.2 Effects of Additional Inspiratory

Muscles Strengthening in Aerobic

Exercise to Inspiratory and Other

Peripheral Muscle (Handgrip)

Strength

Table 2: Comparative characteristics of inspiratory and

handgrip muscle strength before and after exercise.

Note: n=number of samples; °=normal data distribution

using mean±deviation standard; †=abnormal data

distribution using median (range); *Wilcoxon test.

Table 2 showed the increase of inspiratory muscle

strength after administration of combination exercise

was significant (p <0.05). Not only inspiratory

muscle, but also other peripheral muscle such as

handgrip muscle strength increase significantly (p

<0.05) after adminsitration those combination

exercise.

3.3 Effects of Additional Inspiratory

Muscles Strengthening in Aerobic

Exercise to Cardiopulmonal and

Peripheral Muscle (Handgrip)

Endurance

Table 3: Comparison characteristics of cardiopulmonal

and handgrip muscle endurance before and after exercise.

Before

exercise

n=11

After

exercise

n=11

Cardio-

pulmonary

endurance

(meter)

†

432.00

(201.00-

492.00)

480.00

(384.00-

528.00)

0.003*

Handgrip

muscle

endurance

(minute)

††

1.50

(1.09-

3.18)

2.36

(1.37-

2.56)

0.075*

Note: n=number of samples; °=normal data distribution

using mean±deviation standard; †=abnormal data

distribution using median (range); *Wilcoxon test.

Table 3 showed the increase of cardiopulmonal

endurance was significantly (p<0.05) after

administration of combination exercise but not

significantly (p>0.05) on handgrip muscle endurance.

4 DISCUSSION

4.1 Effects of Additional Inspiratory

Muscles Strengthening in Aerobic

Exercise to Inspiratory and Other

Peripheral Muscle (Handgrip)

Strength

Muscle strength in SLE patients is generally lower

than normal. In this study, the inspiratory and

handgrip muscle strength was still low. The low

inspiratory muscle strength in our study was same

with study by Amra et al which showed low MIP

and MEP in 76 women with SLE who were followed

for 12 months (Amra et al, 2006). Another

autoimmune disease study by Weber et al,

rheumatoid atrhitis (RA), concluded that there was a

significant difference in respiratory muscle strength,

Before

exercise

n=11

After

exercise

n=11

Inspiratory

muscle

strength

(cmH

†

49.66

(23.33-

87.00)

65.00

(44.30-

115.00)

0.0001*

Handgrip

muscle

strength

(kilogram)

†

11.00

(9.00-

23.00)

14.67

(9.33-

27.00)

0.016*

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

Medicine and Rehabilitation Association

164

MIP (46.25 ± 17.67 vs 81.00 ± 19.69 cmH

O) and

MEP (58.75 ± 17.26 vs 78.00 ± 6.32 cmH

between RA patients and healthy controls (Weber et

al, 2014).

The low strength of handgrip muscle in our study

was same with study by Balsamo et al which showed

low muscle strength in 25 premenopausal SLE

women with low disease activity compared to

healthy in both handgrip (24.2 ± 4.9 kg) and

quadriceps (47.4 ± 8.1 kg) (Balsamo et al, 2013).

Andrew et al also conducted studies related to

muscle strength in 146 SLE patients showed low

handgrip (22.7 ± 6.0 kg) and extensors (44.5 ± 15.7

kg) and knee flexors (29.9 ± 11.2 kg) muscle

strength (Andrews et al, 2015).

The low muscle strength can be caused by

inactivity and corticosteroids resulting changes in

muscle pathology. Muscle pathological changes in

SLE patients include myositis, vasculitis, type 2

muscle atrophy, thickening of blood vessel walls,

and vacuolar myopathy (Jakati et al, 2015). Vascular

changes interfere oxygen (O

) transport from arteries

to muscles or from muscle capillaries to

mitochondria (Silva AG, 2015).

This study result showed significantly increasing

of the inspiratory muscle strength after

administration combination exercises. This results

can be explained by the specifics of the strengtening

exercise itself that increase muscle properties,

namely recruitment of motor units and proportion of

muscle fibers (Bausek et al, 2013; McConnell, 2013).

This study result showed significant in increasing

of the strength of handgrip muscle although no

specific exercise was given specifically. This effect

can be explained by crossover training from exercise

combination. How strengthening of certain muscles

can cause increased strength of other muscles.

Zhang et al obtained significant handgrip muscle

strength in a combination intervention of aerobic

exercise and muscle strengthening for 8 weeks

compared to aerobic exercise alone in middle-aged

and elderly women (Zhang T et al, 2015).

Another effect of additional inspiratory muscle

strengthening is improvement in pulmonary

mechanical ventilation so it enable increased lung

volume and capacity which have impact on

increasing oxygen supply in peripheral muscles. So,

the increasing of handgrip muscle strength can also

be explained as a result of increased lung function

and respiratory muscle strength. Smith and Son

study found that handgrip strength has a strong

correlation with lung function as measured by

spirometry (Smith et al, 2018; Son et al, 2018).

The mechanism which underlying the correlation

of respiratory and other peripheral muscles is the

effect of metaboreflex. This metaboreflex increased

sympathetic activity in peripheral muscles including

the handgrip muscles to be more earlier fatigue.

Decrease of this metoboreflex can prevent early

fatigue in peripheral muscles so it increase

peripheral muscle performance (Bausek et al, 2013).

4.2 Effects of Additional Inspiratory

Muscles Strengthening in Aerobic

Exercise to Cardiopulmonal and

Peripheral Muscle (Handgrip)

Endurance

Cardiopulmonary endurance in SLE patients is

generally low compared to normal, but this study

showed these patient has good cardiopulmonary

endurance prior to exercise. This study is different

from previous study by Pinto et al which showed

lower cardiopulmonary endurance values with

max (12.8±3.6 ml/kg/ min) compared to healthy

controls (14.6±4.6 ml/kg/min) (Pinto et al, 2016).

The difference probably because our research

subjects were categorized as LLDAS, who have low

disease activity and low dose of corticosteroid. The

other factor is that according to the IPAQ, subjects

in this study are categorized as minimally active, not

inactive, which could explain the state of

cardiopulmonary endurance in this study.

Low cardiopulmonary endurance depends on

multiorgan involving heart, lungs and peripheral

muscles. Disturbances in O

transport to muscle or

diffusion transport from muscle capillaries to the

mitochondria are determinants of cardiopulmonary

endurance in SLE patients. Deconditioning of

peripheral muscles is also believed to cause a

decrease in aerobic capacity in SLE patients. Other

factors such as the use of corticosteroids can

negatively impact the capillary number and

myofibril mass thereby contributing to the decrease

in aerobic capacity (Pinto et al., 2016; Silva AG,

2015).

This research showed significant result in

increase of cardiopulmonary endurance after

administration combination exercises. This study is

in line with the Miossi et al conducted study in 24

inactive SLE patients showed cardiac effect after 12

weeks of aerobic exercise with a treadmill for 30

minutes and resistance in the form of bench press,

leg press, leg extension, seated row, squat, and

crunches for 30-45 minutes (Miossi et al., 2012). In

our study, the strengthening exercise targeted only

The Effect of Additional Inspiratory Muscle Strengtening on Aerobic Exercise in Systemic Lupus Erythematosus: A Preliminary Study

165

the inspiratory muscle. Result of this study shows

that adding one exercise can benefit SLE patients.

The physiological mechanism responsible for

increasing of aerobic capacity are due to changes in

the central component (cardio-pulmonary) and

peripheral components (muscle). Cardiac output

increases after exercise through increased stroke

volume as a result of increased myocardial

contractility. Exercise can reduce the sympathetic

effect so that peripheral resistance decreases.

Exercise can also increase diffusion capacity of O

as a result of larger lung volume and alveolar-

capillary surface area that develops. The capacity of

muscle blood flow also increases with exercise due

to vascular remodeling in the form of capillary

angiogenesis and or changes in vascular resistance

(Kisner and Colby, 2012; Kraemer et al, 2012).

This study shows the increase of handgrip

muscle endurance after exercise combination.

Handgrip endurance was also assessed because the

function of the handgrip is not only measured by

handgrip strength. Handgrip function is needed for

SLE patients in daily activities besides

cardiopulmonary endurance for mobilization. The

increase of hangdrip endurance can be explained by

crossover training effect of these combination

exercise. The crossover effect showed that pasien

not only able to get results that are consistent to the

specificity of training, but also improve performance

in one type of exercise by training using another

type (Kraemer et al, 2012).

Although there is increasing of handgrip muscle

endurance, but not significantly different. This result

might be due to insufficient cross training effects of

exercise combination, because the inspiratory and

handgrip muscle strength in this study were still low

compared to normal. Another factor is sarcopenia,

which can occur in chronic inflammatory diseases

such as in SLE patients that were not measured in

this study. The diagnosis of sarcopenia should be

based on decreased muscle mass and strength

and/or lower physical performance. Therefore,

nutritional evaluation is also needed because it

affects the muscle mass itself.

Further research is needed to assess the

sarcopenia and nutritional on this new exercise

protocol in SLE patients. Another research is also

needed to define how much role of inspiratory

muscle strengthening compared to aerobic exercise

in providing a positive effect on this results.

5 CONCLUSION

The addition of inspiratory muscle strenghtening on

aerobic exercise not only increases the

cardiopulmonary function but also impacts on the

other functional performance, including handgrip

which is usefull for daily activities. Further research

is needed to explore other functional effects of this

additional inspiratory muscle strengtening to aerobic

exercise in SLE patients.

ACKNOWLEDGEMENTS

This works was supported by the Indonesia

Endownment Fund for Education, Ministry of

Finance of the Republic of Indonesia. There is no

conflict of interest, none of the authors have any

conflicts of interest to declare.

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