Effects of Incentive Spirometry Breathing Exercise on Lung

Function, C-Reactive Protein Level and Lipid Ratio in Individuals

with Chronic Spinal Cord Injury

Meinar Ferryani

, Nita Theresia Reyne S

, Vitriana Biben

, Farida Arisanti

, Indriati M.S Tobing

Rosiana Pradanasari

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

University of Padjadjaran, Bandung, Indonesia

Departement of Physical Medicine and Rehabilitation, Fatmawati General Hospital, Faculty of Medicine,

University of Indonesia, Jakarta, Indonesia.

Keywords: Chronic Spinal Cord Injury, Inflammation, Incentive Spirometry, Lung Function, Lipid Ratio, C-reactive

Protein

Abstract: Spinal cord injury (SCI) is an inflammatory process caused by axon and cell membrane damages, cell

death, leukocyte migration and degradation of the myelin layer. Inflammatory diseases are particularly

associated with cardiovascular disease. The SCI patients can experience decreased sympathetic activity

which influences carbohydrate and fat metabolisms. Decreased catecholamine release which plays a

role in the process of lipolysis and glycogenolysis can increase levels of low-density lipoprotein (LDL)

cholesterol, decreased high-density lipoprotein (HDL) cholesterol. Since the SCI often causes

respiratory problems due to reduced respiratory muscle conservation, the study was conducted to find

out the impact of sustained maximum inspiration with Incentive Spirometer (IS) to CRP level and lipid

ratio in chronic SCI patient. Methods: A quasi interventional design with a pre- and post-test approach

was done to eleven patients with chronic phase of SCI. Conclusion: These findings show although

incentive spirometry breathing exercise after 4 weeks can improve lung function and lipid ratio, it has

not decreased the systemic inflammatory levels in individuals with chronic SCI. Improvement in lung

function has not influenced the systemic inflammatory level (CRP), although a beneficial influence on

LDL/HDL ratio was recorded.



1 INTRODUCTION

Spinal cord injury (SCI) referred to spinal cord

damage due to trauma or particular diseases such as

infections, neoplasms and degenerative processes.

The Global prevalence of SCI demonstrated that 40

to 80 new cases had been discovered per one million

populations every year (WHO, 2013). In worldwide,

SCI patients had been reportedly increasing recently.

Based on the data released by World Health

Organization (WHO) 250,000 to 500,000 SCI

patients were reported per year (WHO, 2013). Data

published by the Fatmawati General Hospital in

2014 presented that there were 104 cases of new SCI

(37 traumatic cases and 67 non-traumatic cases)

(Tulaar, 2017).

The SCI has caused axon and cell membranes

damages, cell deaths, leukocyte migration, and

myelin deterioration. Damages in nerve cells can

activate the immune system response and

inflammation process (Alves, 2013). The continuous

occurrence of inflammation process in SCI leads to

chronic tissue damage. (Alves, 2013).

The inflammation process can be detected by

increasing C-reactive protein (CRP) which is one of

the cytokines that play roles in several inflammatory

responses. The production of CRP from the liver is

controlled by interleukin-6 (IL-6) (Pederson, 2006).

Chronic SCI is commonly associated with increased

CRP serum concentrations defining as an

inflammatory marker of several phases such as

220

Ferryani, M., S, N., Biben, V., Arisanti, F., Tobing, I. and Pradanasari, R.

Effects of Incentive Spirometry Breathing Exercise on Lung Function, C-Reactive Protein Level and Lipid Ratio in Individuals with Chronic Spinal Cord Injury.

DOI: 10.5220/0009088402200226

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 220-226

ISBN: 978-989-758-409-1

acute and chronic inflammatory, and endothelial

activation (Wang, 2007).

Inflammatory diseases are distinctively

associated with cardiovascular diseases. An

epidemiological study in normal population stated

that high levels of CRP become a predictor of

cardiovascular diseases. The

 CRP values in adults’

chronic SCI were consistent with the AHA

classification of high CVD risk, especially those of

persons with tetraplegia (Gibson, 2008). Therefore

cardiovascular disease has become one of many

causes of deaths besides respiratory system disorders

(Zonneveld, 2014).

The SCI patients can experience decreased

sympathetic activity which influences carbohydrate

and fat metabolisms. Decreased catecholamine

release plays a role in the process of lipolysis and

glycogenolysis that can increase levels of low-

density lipoprotein (LDL) cholesterol, decreased

high-density lipoprotein (HDL) cholesterol, and 8–

18% fat mass which is higher than healthy people

(Gibson, 2008). Dyslipidemia is observed in a large

number of individuals with chronic SCI. The risk of

dyslipidemia was seen to have increased in motor

complete SCI patients and patients who could not be

community ambulated (Koyunchu, 2017). The high

percentage of dyslipidemia found in chronic SCI

supports the increased risk of coronary heart disease

(Vichiansiri, 2012). The LDL/HDL ratio is an

indicator of sudden death risk due to cardiac

abnormality (sudden cardiac death/SCD). A high

LDL/HDL ratio (> 4,22) in blood is in accordance

with an increased risk of SCD (Kunutsor, 2017).

Exercise is an important rehabilitation therapy

for SCI patients because it can improve sympathetic

response by increasing catecholamines, inducing the

process of lipolysis and activation of immune cells

in the blood (Alves, 2013). This condition leads to

decreased body fat, especially visceral fat, and

decreased inflammatory cytokines in the blood so

that it will reduce the chronic inflammatory response

in SCI patients (Alves, 2013).

Systemic inflammation has been associated with

decreased lung function in individuals with or

without chronic medical conditions. Individuals with

chronic SCI have clinical characteristics that can

cause systemic inflammation and decreased lung

function. Plasma CRP and IL-6 in individuals with

chronic SCI are inversely related to forced

expiratory volume in one second (FEV1) and forced

vital capacity (FVC) (Hart, 2017). Systemic

inflammation associated with chronic SCI can

contribute to decreased lung function (Hart, 2017).

In patients with spinal cord injury (SCI), the

respiratory function may be affected due to complete

or partial paralysis of the respiratory muscles and

abdominal muscles leading to a reduction in the

ability to breathe (Kim, 2017). Improved inspiratory

muscle strength and endurance could potentially

improve cough and maximal exercise ventilation in

addition to decreasing dyspnea (Sheel, 2007).

The advantages of using an incentive spirometer

are: 1) it is easy to learn how to use the instrument;

2) it is economical, and 3) patients can be motivated

to use it, as it produces a visible improvement. Its

visual feedback helps to train patients to use the

instrument independently and freely and it

maximizes their respiratory motivation (Kim, 2017).

Incentive spirometer can be used to maintain

maximum inspiration by providing predetermined

volume feedback (Restrepo, 2011). The IS enables

the mobilization of large lung volumes and the

increased intra-alveolar pressure at the end of

inspiration. This condition improves breathing

capacity, and challenges the patient with the visual

stimulus generated by the device (Paiva, 2015).

The intervention of inspiratory muscle training

(IMT) in chronic heart failure (CHF) patients have

shown to reduce CRP levels (Adamopoulos, 2014).

Giving IS exercise to patients with chronic

obstructive lung disease (COPD) for 4 weeks also

can reduce inflammatory cytokines of IL-6 and

TNF-α. (Leelarungrayub, 2018).

The effect of IMT on CRP levels and lipid ratio in

chronic SCI patients has not been clearly studied.

Therefore, this study aimed to determine the effect

of inspiratory muscle training with IS on CRP levels

and lipid ratio in chronic SCI.

2 METHODS

This study used a quasi-interventional research

design with a pre- and post-test approach. The

population in the study was all chronic phase of SCI

patients who occupied in the Social Care Center of

Bina Daksa Pondok Bambu, West Jakarta,

Indonesia.

The samples were recruited based on the

inclusion criteria, that were chronic SCI, aged 18 –

59 years old, paraplegic, no acute infection, stable

spinal structure, able to perform breathing muscle

training inspiration procedure for 30 minutes,

Hamilton Depression Score (HDS) less than 20,

Mini Mental State Examination (MMSE) score

between 22–30. Exclusion criteria unable to take a

deep breath due to pain, taking analgesic opiates and

patients with vital capacity <10 mL/kg. The subjects

Effects of Incentive Spirometry Breathing Exercise on Lung Function, C-Reactive Protein Level and Lipid Ratio in Individuals with Chronic

Spinal Cord Injury

221

signed an informed consent to be included in the

study. After each set, a one-minute rest was allowed.

The IS training program was conducted after the

subjects were given explanations of the exercise

device, watched a video about the use of the exercise

and familiarizing the device for 2 consecutive days.

The subjects maintained a maximal inspiration for 3

to 5 seconds, and then performed maximal

expiration. This exercise was performed for a total

of five sets, with 10 repetitions making up one set.

After each set, a one-minute rest was allowed (Kim,

2017).

The CRP levels and LDL/HDL ratio were

examined 24 hours before the IS training begin and

after the study ended. The study measured CRP

levels by using hs-CRP which has sensitivity range

0.01 to 10 mg/L so that levels of lower systemic

inflammations were able to be measured even in the

absence of clear systemic inflammatory or

immunological disorders (Kamath, 2015).



Lung function was measured with a

computerized spirometer during maximal voluntary

ventilation maneuvers. As the maneuvers were being

measured, the subjects were asked to sit upright and

make sure nothing was restricting chest movement

or airflow. The subjects started the test by breathing

normally through the mouthpiece, followed by

breathing as deeply and rapidly possible for 20

seconds. At the end of the measurement interval, the

subjects were asked to resume normal breathing and

the mouthpiece was removed. Three trials of the

maneuvers were performed, separated by a five-

minute rest, and the average of the results was taken.

The measured values included forced vital capacity

(FVC) and forced expiratory volume in 1 second

(FEV1), and the lung function indices were

calculated automatically by the computer (Kim,

2017).

Continous data including age were presented with

mean values and standard deviations (SD),

maximum and minimum values. The subjects’

characteristic data were presented in frequency

distribution. Categorical variables were presented in

percentage (%). Statistical analysis was carried out

by performing a normality test to determine that the

data were normally distributed or not normally

distributed.

Data distribution was discovered using the

Shapiro Wilks test since the samples were less than

50. Paired t test was used to compare numerical

variables between before and after the intervention if

the data were normally distributed and the Wilcoxon

test if the data were not distributed normally.

 The

study was conducted to find out the impact of

sustained maximum inspiration with Incentive

Spirometer (IS) in improving lung function and

decreasing CRP level and lipid ratio in chronic SCI

patients. Significance of the statistical test results

was determined based on p-value (<0.05). All

procedures were performed using the SPSS for

Windows version 24.0.

The study was approved by the Ethics Committee

of Padjadjaran University, Bandung, Indonesia with

ethical numbers of 0318050786. All subjects signed

an informed consent form. The subjects could leave

the study at any time without giving any reason. All

data and information of the subjects will be kept

confidentially.

3 RESULTS

The study enrolled 11 chronic phase of SCI patients.

The mean age of the subjects was 44 years old. The

number of male subjects (90.9 %) was higher than

female subjects. The subjects had SCI

approximately 260 months (mean) due to trauma

(90. 9%) (Table 1). Most of the subjects had

complete SCI (81.8 %) with the body mass index

(BMI), the subjects were mostly underweight, below

18,5, (63.6 %) without any other complications of

chronic SCI. Occupation of the subjects was mostly

as a craftsman. None of the subjects had smoking

history. Also, the subjects did not consume

medicines that could influence CRP levels such as

statins, SSRI (selective serotonin uptake inhibitors),

and aspirin.

The differences between pre- and post-test values

for FVC (2.32 ±0.557 and 2.59 ±0.625) and FEV1

(2.16 ±0.596 and 2.40 ±0.654) was statistically

significant increased (p=0.005 and p=0.007).

However, there are no significant mean differences

between CRP level (p=0.229), before and after

practicing IS exercise (Table 2). The study also

showed that there was a significant mean difference

in LDL/HDL ratio (p=0.007) before and after IS

exercise(Table2)

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

Medicine and Rehabilitation Association

222

Table 1: Subject’s Characteristics

Variables Total (n=11) Mean (SD) Median

Age (Years old) 44.27±7.695 44

Sex

Male 10 (90.9%)

Female 1 (9.1%)

Body mass index category

Underweight (< 18,5) 7 (63.6%)

Normal 3 (27.3%)

Overweight (≥ 25) 1 (9.1%)

Occupation

Craftsman 10 (90.9%)

Mechanic 1 (9.1%)

Period of injury (months)

259.63±104.375 228

Etiology

Trauma 10 (90.9%)

Spondylitis TB

(inactive)

1 (9.1%)

Pressure sores

(+) 0 (0.0%)

(-) 11 (100.0%)

Medication

Mecobalamin, yes

1 (9.1%)

(-) 10 (90.9%)

Smoking history

Yes 9 (81.8%)

Normal 2(18.2%)

AIS classification

Complete 10 (90.9%)

Incomplete 1 (9.1%)

MMSE Category

Able (score 22-30) 11 (100.0%)

Unable 0 (0.0%)

HAMILTON Depression

Rating Scale Category

Yes 0 (0.0%)

11(100.0%)

Effects of Incentive Spirometry Breathing Exercise on Lung Function, C-Reactive Protein Level and Lipid Ratio in Individuals with Chronic

Spinal Cord Injury

223

Table 2 : C-reactive Protein (CRP), LDL/HDL Ratio, Total Leucocyte Comparison, FVC and FEV1 Before and After

Variables

Groups

p Value

Before After

n=11 n=11

CRP (mg/dL) 0.229

Mean+SD 0.44±0.750 0.61±1.073

Median 0.23 0.19

LDL/HDL ratio 0.007**

Mean+SD 3.36 ±0.429 3.04 ±0.603

Median 3.30 3.00

Total leukocytes (/µL) 0.629

Mean+SD 7250.90±1716.347 7022.72±1645.849

Median 6770.00 7360.00

FVC 0.005**

Mean+SD 2.32 ±0.557 2.59 ±0.625

Median 2.24 2.70

FEV1 0.007**

Mean+SD 2.16 ±0.596 2.40 ±0.654

Median 2.20 2.76

the value presented is the mean value + SD. Numerical data the p value is tested by paired T test if the data is normally

distributed with the alternative Wilcoxon test if the data is not normally distributed. Significance value based on the value

of p <0.05. Sign * indicates the value of p <0.05 means significant or statistically significant.

4 DISCUSSIONS

The subjects of the study were mostly men (90,9%).

Although women could have higher CRP levels than

men due to hormonal factors (O’Connor, 2009),

this condition may not significantly influence the

CRP results.

CRP levels did not change significantly due to

several factors, one of them is the high CRP level

since the beginning, although there was no sign of

infection during the study since the leucocyte count

did not increase. The CRP level could be influenced

by BMI, the level and severity of the lesion and

smoking habits. Most of the subjects in this study

were included in the underweight category with an

average BMI was 18.72 ± 2.173 kg/m2. The BMI

values are related to body fat composition. Low BMI

could be caused by decreased fat-free muscle mass

due to reduction in physical activity and atrophy

caused by paralysis. Greater adipose tissue

composition due to impaired fat and carbohydrate

metabolisms can lead to increased CRP levels

(Wang, 2007).

Lesion levels and severity of SCI itself can

influence the CRP levels. The higher lesion levels

and severe SCI indicate higher CRP levels. Those

with tetraplegia have a greater risk of CVD

compared to those with paraplegia in chronic SCI

Gibson, 2008). SCI lesions of the subjects in this

study were as high as the thoracic cord. Since most

of the subjects had complete SCI, high CRP levels

of the subjects were discovered since the beginning.

The smoking habits were not limited during the

study, these may cause a high of CRP level.

Smoking can increase the release of

proinflammatory cytokines in the blood and lung

circulation. It also can cause oxidative stress and

vascular inflammation occurs marked by increased

IL-6 and CRP levels. A previous study presented

that higher CRP levels were mostly found in the

subjects who smoked (O’Connor, 2009).

Unfortunately, this study did not have any data to

analyaze the correlation between the number of

cigarettes (packs per year) and nicotine levels with

distinctive measurements in each subject.

Exercise can decrease inflammatory cytokines in

the blood (Alves, 2013). Muscle contractions can

stimulate the release of IL-6 from muscle cells,

namely muscle derived IL-6.

 IL-6 has important

anti-inflammatory effects since it plays a role in the

formation of anti-inflammatory cytokines such as

interleukin-1 receptor antagonist (IL-1ra) and

interleukin-10 (IL-10).

The appearance of IL-10 and

IL-1ra in the circulation contributes to mediating the

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

Medicine and Rehabilitation Association

224

anti-inflammatory effects of exercise and induces a

reduction in CRP levels and suggests that physical

activity may suppress systemic low-grade

inflammation.

The increased plasma IL-6 is related to exercise

intensity, duration, the mass of muscle recruited and

one’s endurance capacity (Peterson, 2005). Physical

activities with moderate intensity are recommended

to reduce CRP levels (Zonneveld, 2014). IS exercise

in this study counted as moderate intensity based on

Borg scale 11-13. Most of the subjects had the same

occupation as a craftsman and did their daily

activities independently, but still there were no

complete data and objective assessment of physical

activities collected.

The IS exercise given in this study had not

decreased the inflammation marker of CRP. This

study given different result from the previous studies

that after 4 weeks of physical training was

associated with significantly improved plasma

concentrations of adiponectin and CRP (Oberbach,

2006), IS exercise for 4 weeks (twice daily, 30

breaths a set for 30 days) in COPD patients was

already showed a significant result in reducing IL-6

and TNF-α inflammatory cytokines

(Leelarungrayub, 2017), IMT combined with aerobic

training provides additional benefits in functional

and serum biomarkers of inflammation (CRP) in

patients with moderate CHF (Adamapoulos, 2014).

The differences in the type of exercise, the mass of

muscle recruited, the intensity and duration of

exercise compared with the previous study, the

markers of inflammation which had been examined

may make the differences of the result.

The study has shown that IS exercise can

improve lung function in an individual with chronic

SCI. The similar results showed in another previous

study (Kim, 2017). The study has not shown

significant change in the circulating level of CRP

however, a potential local effect of IS on

diaphragmatic myocyte cytokine production cannot

be excluded. Whether there was a reduction in local

diaphragmatic muscle inflammation marker after IS

was not tested in this study.

The IS exercise given in this study had influenced

fat metabolism marked by the significant reduction

of LDL/HDL ratio. IL-6 is the first cytokine

released into the circulation during exercise, derived

from the contracting muscle. This cytokine will

activate lipolysis independently of elevations in

Growth Hormone (GH) and/or cortisol and become a

potent catalyst for fat oxidation in muscle cells

(Peterson, 2005). The present study was given

different result from the previous studies that IMT

with low inspiratory loading fails to demonstrate any

significant improvements in blood glucose levels,

serum lipids, and/or HOMA-IR in female patients

with type 2 diabetes (Ahmad, 2017) and after 7 days

of IMT had not able to change metabolic variables

(blood glucose and lipid profile) in women with

metabolic syndrome (Feriani, 2017).

There are some limitations to this study that can

be improved in future research. Firstly, the present

study did not measure other cytokines, such as IL-10

and IL-1ra may be needed to confirm that the

observed increase in IL-6 is muscle derived and not

due to other factors, such as the existence of a

catabolic/inflammatory state due to exercise training

(Peterson, 2005). Secondly, this study did not have

any data regarding the number of cigarettes (packs

per year) and nicotine levels with distinctive

measurements in each subject which can correlate

with the inflammatory state. Thirdly,

 there was no

complete data and objective assessment of physical

activities and nutritional intake collected.

Further study can be conducted by giving longer-

term IS exercise intervention or with other exercise

combinations including aerobics. Assessment of

detail physical activity level, other routine activity

(such as smoking), nutritional status and other anti-

inflammatory cytokine levels should be done in

further study.

5 CONCLUSIONS

A 4 weeks incentive spirometry breathing exercise

resulted in improvement in lung function and lipid

ratio. Improvement in lung function has not

influenced the systemic inflammatory level (CRP),

although a beneficial influence on LDL/HDL ratio

was recorded. Further follow up and studies are

required to establish the role of inspiratory muscles

in improving the systemic inflammatory status of

patients with chronic spinal cord injury.

REFERENCES

Adamopoulos S, Schmid JP, Dendale P, Poerschke D,

Hansen D, Dritsas A et al. 2014. Combined

aerobic/inspiratory muscle training vs. aerobic training

in patients with chronic heart failure. European

journal of heart failure ; 16(5) : 574-82.

Ahmad AM, Abdelsalam HM, Lotfy AO. 2017. Effect of

Inspiratory Muscle Training on Blood Glucose Levels

and Serum lipids in female patients with type 2

diabetes. International Journal of ChemTech Research

; 10(4): 703-709

Effects of Incentive Spirometry Breathing Exercise on Lung Function, C-Reactive Protein Level and Lipid Ratio in Individuals with Chronic

Spinal Cord Injury

225

Alves E, Lemos V, Silva F, Lira FS, Santos RVT, Rosa

JPP et al. 2013. Low-grade inflammation and spinal

cord injury: exercise as therapy? Mediators of

inflammation; 1-8.

Feriani DJ, Coelho-Júnior HJ, Scapini KB, de Moraes OA,

Mostarda C, Ruberti OM. 2017. Effects of inspiratory

muscle exercise in the lung function, autonomic

modulation, and hemodynamic variables in older

women with metabolic syndrome. Journal of Exercise

Rehabilitation ;13(2):218-226

Gibson A, Buchholz A, Ginis KM. 2008. C-Reactive

protein in adults with chronic spinal cord injury:

increased chronic inflammation in tetraplegia vs

paraplegia. Spinal Cord.;46(9):616-21.

Groah SL, Weitzenkamp D, Sett P, Soni B, Savic G. 2001.

The relationship between neurological level of injury

and symptomatic cardiovascular disease risk in the

aging spinal injured. Spinal Cord ; 39: 310–317.

Hart JE, Goldstein R, Walia P, Teylan M, Lazzari A, Tun

CG, et al. 2017. FEV1 and FVC and systemic

inflammation in a spinal cord injury cohort. BMC

Lung Medicine ; 17: 1-9.

Kamath DY, Xavier D, Sigamani A, Pais P. 2015. High

sensitivity C-reactive protein (hsCRP) &

cardiovascular disease: An Indian perspective. Indian

J Med Res ; 142: 261-268.

Kunutsor SK, Zaccardi F, Karppi J, Kurl S, Laukkanen

JA. 2017. Is High Serum LDL/HDL Cholesterol Ratio

an Emerging Risk Factor for Sudden Cardiac Death?

Findings from the KIHD Study. J Atheroscler

Thromb; 24: 600-608.

Koyuncu E, Yüzer GFN, Yenigün D, Özgirgin N. 2017.

The analysis of serum lipid levels in patients with

spinal cord injury. The Journal of Spinal Cord

Medicine; 40 (5) : 567-572.

Kim CY, Lee JS, Kim HD, Lee DJ. 2016. Short-term

effects of respiratory muscle training combined with

the abdominal drawing-in maneuver on the decreased

lung function of individuals with chronic spinal cord

injury: A pilot randomized controlled trial. The

Journal of Spinal Cord Medicine; 1-9.

Leelarungrayub J, Puntumetakul R, Sriboonreung

T,Pothasak Y,Klaphajone J. 2018. Preliminary study:

comparative effects of lung volume therapy between

slow and fast deep breathing techniques on lung

function, respiratory muscle strength, oxidative stress,

cytokines, 6-minute walking distance, and quality of

life in persons with COPD. International Journal of

COPD ; 13: 3909–3921.

Manns PJ, McCubbin JA,Williams DP. 2005. Fitness,

inflammation, and the metabolic syndrome in men

with paraplegia. Arch Phys Med Rehabil ;86: 1176–

1181.

Ma JK, McCracken LA, Voss C, Chan FH, West CR,

Ginis KM. 2018. Physical activity measurement in

people with spinal cord injury: comparison of

accelerometry and self-report (the Physical Activity

Recall Assessment for People with Spinal Cord

Injury). Disability and Rehabilitation ; 1-7.

O’connor MF, Bower JE, Cho HJ, Creswell JD, Dimitrov

S, Hamby ME, et al. 2009. To assess, to control, to

exclude : Effects of biohavioral factors on circulating

inflammatory markers. Brain, Behavior, and

Immunity; 23 : 887-897.

Oberbach A, Anjes A, Kloting N, Fasshauer M, Kratzsch

J, Busse MW, et al. 2006. Effect of a 4 week physical

training program on plasma concentrations of

inflammatory markers in patients with abnormal

glucose tolerance. European Journal of

Endocrinology; 154 : 577–585.

Petersen AM, Pedersen BK. 2005. The anti-inflammatory

effect of exercise. J Appl Physiol ; 98: 1154–1162.

Petersen EW, Carey AL, Sacchetti M, Steinberg GR,

Macaulay SL, Febbraio MA, et al. 2005. Acute IL-6

treatment increases fatty acid turnover in elderly

humans in vivo and in tissue culture in vitro. Am J

Physiol Endocrinol Metab; 288(1):E155-62.

Pedersen BK. 2006. The anti-inflammatory effect of

exercise : its role in diabetes and cardiovascular

disease control. The Biochemical Society; 42 : 105-

115.

Plaisance EP and Grandjean PW. 2006. Physical Activity

and High-Sensitivity C-Reactive Protein. Sports Med;

36 (5): 443-458.

Paiva DN, Assmann LB, Bordin DF, Gass R, Jost RT,

Filhod MB, et al. 2015. Inspiratory muscle training

with threshold or incentive spirometry: Which is the

most effective?Rev Port Pneumol; 21(2):76-81.

Restrepo RD, Wettstein R, Wittnebel L, Tracy M.

Incentive spirometry: 2011. 2011. Respiratory care ;

56(10) : 1600-4.

Tulaar ABM, Karyana M, Wahyuni LK, Paulus AFS,

Tinduh D, Anestherita F et al. 2017. People with

spinal cord injury in Indonesia. Am J Phys Med

Rehabil ; 96(2) : S74-S77.

Vichiansiri R, Saengsuwan J, Manimmanakorn N, Patpiya

S, Preeda A, Samerduen K, et al. 2012. The

Prevalence of Dyslipidemia in Patients with Spinal

Cord Lesion in Thailand. Cholesterol; 2012: 1-6.

World Health Organization. 2013. International

perspective on spinal cord injury. Malta: WHO

Library Cataloguing-in-Publication Data.

Wang T. D., Wang Y. H., Huang T. S., Su T. C., Pan S.

L., and Chen S. Y. 2007. Circulating levels of markers

of inflammation and endothelial activation are

increased in men with chronic spinal cord injury.

Journal of the Formosan Medical Association ; 106

(11) : 919–928

Zonneveld CN, Bakkum AJ, Bishop NC, Van Tulder MW,

Janssen TW. 2014. Effect of Long-Term Physical

Activity and Acute Exercise on Markers of Systemic

Inflammation in Persons With Chronic Spinal Cord

Injury: A Systematic Review. Archives of Physical

Medicine and Rehabilitation; 1-13.

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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