correlation between pulmonary function, posture, and body composition in patients with asthma

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Rev Port Pneumol. 2013;19(5):204---210 www.revportpneumol.org ORIGINAL ARTICLE Correlation between pulmonary function, posture, and body composition in patients with asthma V.P. Almeida a , F.S. Guimarães a , V.J.R. Moc ¸o a,, S.L.S. Menezes a , T.T. Mafort b , A.J. Lopes a,c,a Programa de Pós-graduac ¸ão em Ciências da Reabilitac ¸ão, Universidade Augusto Motta, Rio de Janeiro, Brazil b Departamento de Pneumologia, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil c Laboratório de Fisiologia Respiratória, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil Received 16 October 2012; accepted 11 March 2013 KEYWORDS Asthma; Respiratory function tests; Respiratory mechanics; Respiratory muscles; Posture; Pulmonary diffusing capacity; Body composition Abstract Aim: Asthma may result in postural disorders due to increased activity of accessory respiratory muscles and hyperinflation. Our primary objective was to assess the correlation between pul- monary function and posture in adult patients with asthma. Secondarily, we aimed to study the correlation between body composition and body posture in this group of patients. Method: This was a cross-sectional study including 34 patients with asthma who were subjected to postural assessment (photogrammetry), pulmonary function testing (spirometry, whole-body plethysmography, diffusing capacity for carbon monoxide, and respiratory muscle strength), and body composition estimation by means of bioelectrical impedance. Results: Most patients were female (70.6%) with a median age of 32.5 years (range: 23---42 years old). We found a significant correlation between horizontal alignment of head (ante- rior view) and the ratio of forced expiratory volume in 1 s to forced vital capacity (FEV 1 /FVC; = 0.37; P = 0.03), total lung capacity (TLC; = 0.42; P = 0.01), and residual volume (RV; = 0.45; P < 0.001). Bronchial obstruction and respiratory muscle strength variables also corre- lated with postural assessment measures on the right and left lateral views. Both body mass index and the percentage of fat mass were correlated with horizontal alignment of head, horizontal alignment of the pelvis, and the frontal angle of the lower limbs. Conclusion: Adult patients with asthma exhibit specific postural disorders that correlate with pulmonary function and body composition. The assessment of postural variables may provide a better pulmonary rehabilitation approach for these patients. © 2012 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L. All rights reserved. Please cite this article as: Almeida VP, Guimarãesa FS, Moc ¸oa1 VJR, Menezesa SLS, Mafortb TT, Lopes AJ. Correlac ¸ão entre func ¸ão pulmonar, postura e composic ¸ão corporal em pacientes com asma. Rev Port Pneumol. 2013;19:204---210. Corresponding author. E-mail address: [email protected] (A.J. Lopes). Role in the study: Analysis and interpretation of data, revising the article, and final approval of the version of manuscript. 2173-5115/$ – see front matter © 2012 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L. All rights reserved.

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ev Port Pneumol. 2013;19(5):204---210

www.revportpneumol.org

RIGINAL ARTICLE

orrelation between pulmonary function, posture, and bodyomposition in patients with asthma�

.P. Almeidaa, F.S. Guimarãesa, V.J.R. Mocoa,♦, S.L.S. Menezesa, T.T. Mafortb,.J. Lopesa,c,∗

Programa de Pós-graduacão em Ciências da Reabilitacão, Universidade Augusto Motta, Rio de Janeiro, BrazilDepartamento de Pneumologia, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, BrazilLaboratório de Fisiologia Respiratória, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil

eceived 16 October 2012; accepted 11 March 2013

KEYWORDSAsthma;Respiratory functiontests;Respiratorymechanics;Respiratory muscles;Posture;Pulmonary diffusingcapacity;Body composition

AbstractAim: Asthma may result in postural disorders due to increased activity of accessory respiratorymuscles and hyperinflation. Our primary objective was to assess the correlation between pul-monary function and posture in adult patients with asthma. Secondarily, we aimed to study thecorrelation between body composition and body posture in this group of patients.Method: This was a cross-sectional study including 34 patients with asthma who were subjectedto postural assessment (photogrammetry), pulmonary function testing (spirometry, whole-bodyplethysmography, diffusing capacity for carbon monoxide, and respiratory muscle strength),and body composition estimation by means of bioelectrical impedance.Results: Most patients were female (70.6%) with a median age of 32.5 years (range: 23---42years old). We found a significant correlation between horizontal alignment of head (ante-rior view) and the ratio of forced expiratory volume in 1 s to forced vital capacity (FEV1/FVC;� = −0.37; P = 0.03), total lung capacity (TLC; � = 0.42; P = 0.01), and residual volume (RV;� = 0.45; P < 0.001). Bronchial obstruction and respiratory muscle strength variables also corre-lated with postural assessment measures on the right and left lateral views. Both body massindex and the percentage of fat mass were correlated with horizontal alignment of head,horizontal alignment of the pelvis, and the frontal angle of the lower limbs.Conclusion: Adult patients with asthma exhibit specific postural disorders that correlate with

pulmonary function and body composition. The assessment of postural variables may provide a better pulmonary rehabilitation approach for these patients. © 2012 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L. All rightsreserved.

� Please cite this article as: Almeida VP, Guimarãesa FS, Mocoa1 VJR, Menezesa SLS, Mafortb TT, Lopes AJ. Correlacão entre funcãoulmonar, postura e composicão corporal em pacientes com asma. Rev Port Pneumol. 2013;19:204---210.∗ Corresponding author.

E-mail address: [email protected] (A.J. Lopes).♦ Role in the study: Analysis and interpretation of data, revising the article, and final approval of the version of manuscript.

173-5115/$ – see front matter © 2012 Sociedade Portuguesa de Pneumologia. Published by Elsevier España, S.L. All rights reserved.

Correlation between pulmonary function, posture, and body composition in patients with asthma 205

PALAVRAS-CHAVEAsma;Testes de funcãorespiratória;Mecânicarespiratória;Músculosrespiratórios;Postura;Capacidade dedifusão pulmonar;Composicão corporal

Correlacão entre funcão pulmonar, postura e composicão corporal em pacientes comasma

ResumoObjetivos: A asma pode resultar em alteracões posturais causadas pelo aumento da atividadeda musculatura acessória, respiratória e insuflacão pulmonar. Nosso objetivo primário foi avaliara correlacão entre funcão pulmonar e postura em pacientes adultos com asma. Como segundoobjetivo buscou-se estudar a correlacão entre composicão corporal e postura neste grupo depacientes.Métodos: Foi realizado um estudo transversal onde 34 pacientes com asma se submeteram àavaliacão da análise postural (fotogrametria), funcão pulmonar (espirometria, pletismografiade corpo inteiro, medicão da capacidade de difusão do CO e forca muscular respiratória) ecomposicão corporal através da bioimpedância elétrica.Resultados: A maioria dos pacientes era do sexo feminino (70,6%), com mediana da idade de32,5 anos (variacão: 23-42 anos). O alinhamento horizontal da cabeca (vista anterior) correla-cionou de forma significante com as seguintes variáveis: relacão entre o volume expiratóriomáximo no primeiro segundo e a capacidade vital forcada (VEMS/CVF) (� = −0,37; P = 0,03);capacidade pulmonar total (CPT) (� = 0,42; P = 0,01); e volume residual (VR) (� = 0,45; P <0,001). Os indicadores de obstrucão brônquica e forca muscular respiratória correlacionaram-se também com as medidas de avaliacão postural obtidas em vista lateral direita e esquerda.Tanto o índice de massa corporal quanto o percentual de massa gorda correlacionaram-se comalinhamento horizontal da cabeca, alinhamento horizontal da pélvis e ângulo frontal do membroinferior.Conclusões: Pacientes asmáticos adultos apresentam alteracões posturais específicas que cor-relacionam com a funcão pulmonar e com a composicão corporal. A avaliacão das medidasposturais pode fornecer uma melhor abordagem para a reabilitacão pulmonar nestes pacientes.© 2012 Sociedade Portuguesa de Pneumologia. Publicado por Elsevier España, S.L. Todos osdireitos reservados.

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Introduction

Asthma is a chronic respiratory disease characterizedby increased bronchial responsiveness, reversible airflowobstruction, and bronchial inflammation, which is consid-ered the main physiopathogenic aspect of the disease.1,2

The World Health Organization estimates that 235 millionpeople suffer from asthma worldwide.3

Posture is defined as a balanced arrangement of the bodystructures determined by the position of all the body seg-ments at a given moment.4 In normal postural alignment,the muscles and joints are expected to be in a state of equi-librium while exhibiting minimal effort and overload.5 Thepostural stance associated with thorax hyperinflation mightinduce a series of compensations involving the vertebral col-umn and the scapular belt and pelvic girdle. Thus, patientswith chronic respiratory diseases may develop changes inposture and balance.6---9

Patients with asthma exhibit excessive respiratory mus-cle recruitment in response to airflow obstruction, whichresults in adaptive hypertrophy.6,7 Because these musclesare repeatedly under tension, they become shorter andlose flexibility.10 However, since there is a biomechanicalinterdependence in the human locomotor system, anymechanical abnormality in the thoracic cage influences the

overall body mechanics.11 In this sense, postural assessmentis of fundamental importance for the diagnosis, planning,and monitoring of the progress and results of physicaltherapy.

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Obesity is a common condition among adults with asthmand is usually associated with symptom exacerbation andse of oral corticosteroids.12,13 Obese asthmatic individualsxhibit reduced pulmonary function and poorer quality ofife than eutrophic patients.14 Population-based studies sug-est that high values of body fat and low values of fat-freeass (FFM) are predictors of mortality that are independent

f the underlying disease.15 In addition, the percentages ofat mass (FM) and FFM directly correlate with pulmonaryunction. It has been demonstrated that weight loss andody mass index (BMI) reduction is associated with improve-ent in pulmonary function.16

Asthma might cause systemic repercussions due to itseverity and the effects of treatment.12,13 Our hypothesiss that, in adults with asthma, the changes in respiratoryechanics and obesity interfere with body posture. Weelieve that knowledge about the impact of pulmonary func-ion abnormalities and obesity on body posture can helprevent postural impairments in these patients. Thus, ourrimary objective was to assess the correlation betweenulmonary function and posture. Secondarily, we aimed tonvestigate the correlation between body composition andody posture in this group of patients.

ethods

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e conducted a cross-sectional study with adult patientsecruited at the Newton Bethlem Community Health Clinic

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Table 1 Anthropometry, body composition, and data onthe pulmonary function of the investigated sample (n = 34).

Variables Values

Sex (female/male) 24/10Age (years) 32.5 (23---42)BMI (kg/m2) 25.3 (22.2---31.2)FFM (kg) 45.4 (39---51.8)FM (%) 33.2 (28.6---33.7)FVC (%) 94 (79---104)FEV1 (%) 73.5 (52---84)FEV1/FVC (%) 70.5 (30---82)PEF (%) 61.5 (42---77)MIP (%) 53.3 (34.1---66.8)MEP (%) 54.2 (43.7---76.9)TLC (%) 120 (103---125)RV (%) 138 (113---216)RV/TLC (%) 131 (105---165)Raw (cm H2O/L/s) 1.58 (1---2.80)DLco (%) 99.5 (89---114)

Results expressed as median (interquartile range) or number (%).BMI: body mass index; FFM: fat-free mass; FM: fat mass; FVC:forced vital capacity; FEV1: forced expiratory volume in 1 s; MIP:maximal inspiratory pressure; MEP: maximal expiratory pres-sure; PEF: peak expiratory flow; TLC: total lung capacity; RV:residual volume; Raw: airway resistance; DLco: diffusing capacityfor carbon monoxide.

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fmdiscrepancy between the mean values of the right and leftsides, the differences investigated with PAS were not statis-tically significant (P > 0.05).

Table 2 Values of postural assessment software of patientswith asthma (n = 34).

Variables Values

HHA (AV) 1.65 (2.20---3.70)

Right Left

HHA 39.3 (35.8---45) 39.5 (36.5---45)LLFA 4.90 (1.40---7.30) 4.40 (0.50---7)HA 18.3 (9.40---24.8) 23.4 (14.5---33.6)TVA 4.80 (3.50---7.70) 4 (2.50---8.30)PHA 13.7 (8.70---19.7) 13.8 (10.5---19.9)KA 4.90 (4.50---5.40) 4.90 (1.70---8.10)AA 83.8 (81.2---86.4) 87.4 (82.9---90)

Results expressed as median (interquartile range) or number (%).HHA (AV), head --- horizontal alignment (anterior view); LLFA,

06

n the city of Rio de Janeiro, Brazil. Patients aged 18---50ears old who were diagnosed with asthma were included.atients who were ex-smokers, used psychotropic drugs orad a history of respiratory comorbidities were excluded.he present study was approved (n◦ 012/2011) by the Ethicsommittee of the institution, and all participants signed

nformed consent forms.

easurements

ostural assessment was performed by means of photogram-etry using the postural assessment software (PAS) (FAPESPirtual Incubator, SP, Brazil).17 Coordinates of anatomicaloints (right and left tragus, right and left acromion, rightnd left greater trochanter of the femur, and spinous pro-esses of the seventh cervical and third thoracic vertebrae)ere labeled with passive markers (styrofoam balls attachedith double-sided adhesive tape), and photographs of thenterior, posterior, and right and left lateral views wereaken for all participants. Then, the photographs were trans-erred to a compatible microcomputer and analyzed.

The following tests were performed using the comput-rized Collins Plus Pulmonary Function Testing SystemsWarren E. Collins, Inc., Braintree, MA, USA): spirome-ry, whole-body plethysmography, measurement of diffusingapacity for carbon monoxide (DLco), and assessment ofespiratory muscle strength. All spirometric tests followedhe standards and interpretation of the American Thoracicociety (ATS).18 Pereira’s (spirometry) and Neder’s (lung vol-mes, DLCOsb, and muscle strength) equations were used fornterpreting functional parameters.19---22

Body composition was analyzed using a bioelectri-al impedance device (BIA 310e, Biodynamics, Seattle,A, USA). The participants were instructed to rest formin before the exam. During the test they were bare-

oot, away from metallic objects, and stood with theireet 15---30 cm apart.23 Two electrodes were placed onhe dorsum of the right hand, and two were placed onhe dorsum of the right foot. Resistance and reactanceere calculated and used to estimate FFM. The selectedquation has been previously validated for Brazilian individ-als: FFM = −4.104 + (0.518 × height2/resistance) + (0.231weight) + (0.130 × reactance) + (4.229 × gender: male = 1,

emale = 0).23

ata analysis

ata are given as median and interquartile ranges (25% and5% percentiles) or as frequencies (percentages). Becausehe Shapiro---Wilk test determined that the variables wereot distributed normally, correlations were assessed withpearman’s test. Analysis was performed using SigmaStator Windows, version 3.5 (Systat Software, Inc., Chicago,L, USA). Statistical significance was established as P < 0.05.

esults

f the forty-six patients with asthma who were initiallycreened, 12 were excluded for the following reasons:eclining to participate (3), associated restrictive disease

4), inability to perform the pulmonary function testing (4),nd death (1).

The anthropometric, body composition, and pulmonaryunction data are described in Table 1, and postural assess-ent data are shown in Table 2. Although there was a slight

lower limbs frontal angle; HA, hip angle; TVA, trunk --- verticalalignment; PHA, pelvis --- horizontal alignment; KA, knee angle;AA, ankle angle.

Correlation between pulmonary function, posture, and body composition in patients with asthma 207

Table 3 Correlation between body composition and postural assessment measurements (Spearman’s correlation test, showingonly statistically significant correlations) (n = 34).

Variables Right Left

� P-value � P-value

BMI × HHA 0.40 0.02 --- ---BMI × LLFA 0.40 0.02 --- ---BMI × PHA 0.54 <0.001 0.46 <0.01FFM × HA −0.55 <0.001 --- ---FFM × KA 0.46 0.01 --- ---FM (%) × HHA −0.38 0.02 −0.60 <0.001FM (%) × LLFA −0.50 0.002 −0.40 0.01FM (%) × PHA 0.66 <0.001 0.60 <0.001FM (%) × AA 0.35 0.04 --- ---

BMI: body mass index; HHA: head --- horizontal alignment; LLFA: lower limbs frontal angle; PHA: pelvis --- horizontal alignment; FFM:fat-free mass; HA: hip angle; KA: knee angle; FM: fat mass; AA: ankle angle.

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Discussion

Table 3 describes the correlation between body compo-sition and postural assessment, whereas Table 4 showsthe correlation between pulmonary function and posturalassessment; only the statistically significant data are shownin both tables. A significant correlation was found betweenpostural deviations and indicators of bronchial obstruc-

tion, including reduction of the ratio of forced expiratoryvolume in 1 s to forced vital capacity (FEV1/FVC), reduc-tion of the peak expiratory flow (PEF), increased total lung

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Table 4 Correlation between pulmonary function values and postshowing only statistically significant correlations) (n = 34).

Variables

FEV1/FVC (%) × HHA (AV)TLC (%) × HHA (AV)RV (%) × HHA (AV)

Right

FEV1 (%) × TVA 0.35FEV1 (%) × KA ---FEV1/FVC (%) × KA ---PEF (%) × PHA −0.48PEF (%) × KA ---PEF (%) × AA ---MIP (%) × TVA −0.46MIP (%) × HA −0.51MIP (%) × PHA −0.43MEP (%) × PHA −0.43MEP (%) × TVA −0.47MEP (%) × HA −0.43TLC (%) × TVA 0.45RV (%) × TVA 0.49RV (%) × HA ---Raw (cm H2O/L/s) × HA 0.46

FEV1: forced expiratory volume in 1 s; FVC: forced vital capacity; HHA (capacity; RV: residual volume; TVA: trunk --- vertical alignment; KA: kneflow; AA: ankle angle; MIP: maximal inspiratory pressure; HA: hip angle

apacity (TLC) and residual volume (RV), and increased air-ay resistance (Raw). Postural assessment parameters alsoxhibited significant correlation with respiratory muscletrength measurements.

he main findings of the present investigation were that,n adult patients with asthma, there is a close association

ural assessment measurements (Spearman’s correlation test,

� P-value

−0.37 0.030.42 0.010.45 <0.001

Left

0.04 --- ------ −0.38 0.03--- −0.38 0.02

<0.01 −0.41 0.02--- −0.50 <0.01--- −0.37 0.03

<0.01 −0.40 0.02<0.001 −0.43 0.010.01 −0.45 <0.010.01 −0.37 0.03

<0.01 --- ---0.01 --- ---

<0.01 --- ---<0.01 --- ------ 0.37 0.03

<0.01 --- ---

AV): head --- horizontal alignment (anterior view); TLC: total lunge angle; PHA: pelvis --- horizontal alignment; PEF: peak expiratory; MEP: maximal expiratory pressure; Raw: airway resistance.

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etween postural deviations and airways obstruction varia-les, including ‘air trapping’ and hyperinflation. Also, bothespiratory muscle strength and body composition con-ribute to the abnormalities in body posture. To the bestf our knowledge, this study is the first to assess the rela-ionship between pulmonary function, posture, and bodyomposition in this group of patients.

Posture assessment in a standing position has beenncreasingly used in clinical practice, as the body alignmentbservation can be used to plan and monitor physical ther-py treatments. Photogrammetry by means of the PAS haseen used to assess the correlations between posture, pul-onary function, and body composition.24---26

Compared to normal values,5 we found forward headosture and increased lumbar lordosis among asthmatic indi-iduals, as well as bilateral hip and knee flexion. Although

slight discrepancy was found between the right- andeft-side values, the variables investigated by PAS did notxhibit significant differences (P > 0.05). This relative sym-etry can be justified because asthma affects the lungsiffusely and patients with comorbidities which might causeateral posture deviations were excluded from the presenttudy.

With regard to body composition, some postural changesuch as the horizontal alignment of head and lower limbrontal angle correlated positively with BMI and negativelyith FM (%), whereas the angle of the knee exhibitedsignificant positive correlation with FFM. The associa-

ions between body composition and postural deviationsn the lower half of the body were probably because ofhe greater distribution of body fat in the hips. This dis-ribution pattern of body fat (gynoid pattern obesity) is aommon finding among females, who represent the major-ty of our sample because of the higher prevalence of asthmamong female adults.27,28 Interestingly, Beckett et al.27

howed that the asthma is associated with weight gain inomen but not in men, independent of physical activity;

hus, we think that this finding may have influenced ouresults.

Robles-Ribeiro et al.29 observed that adult patients withild to severe asthma exhibit several postural changes.hey also noted that shoulder protraction in these patients

ncreased as PEF decreased. However, the present study didot find a correlation between these postural changes andulmonary function.

When assessing the correlation between postural varia-les and respiratory maximum pressures, we found arevalence of chest and pelvic changes (trunk vertical align-ent --- right/trunk vertical alignment --- left; horizontal

lignment of the pelvis --- right/horizontal alignment of theelvis --- left; right hip angle/left hip angle), which were neg-tively correlated with MIP and MEP. Abdominal weaknesss known to exacerbate lumbar lordosis in children, mainlyue to alterations of the oblique and transverse abdominaluscles.30 This group of muscles plays an important role in

ertebral stabilization and forced expiration; therefore, itnterferes with MEP measurements. In the present study webserved the same phenomenon in adults.

Boulay et al.31 observed that the postural behavior of theyperinflated thorax induces a series of compensations inhe thoracic spine, pelvic girdle, and scapular belt becausehe diaphragm becomes rectified and shortened. Because

pfva

V.P. Almeida et al.

he diaphragm is directly connected to the endothoracic fas-ia, thoracic hyperinflation might results in the increase ofhoracic kyphosis. We cannot claim that thoracic kyphosisas increased in our sample because the postural assess-ent software does not analyze this variable. However, we

an confirm that, due to the connection of the diaphragmo other thoracic muscles such as the iliopsoas, transversebdominals, and quadratus lumborum, asthma may leado pelvic anteversion and lumbar hyperlordosis, which wasbserved in our sample of patients with asthma and also cor-elated with lung volumes.11 When evaluating the static lungolumes and Raw in patients with asthma, the most strikinghenomenon is the ‘air trapping’ that is the consequence ofdelayed alveolar emptying. The TLC can also be increasedue to the loss of elastic recoil. Another mechanism involvedn TLC increase is the shortening of the expiratory time inatients with asthma, so that inspiration begins before airs entirely expelled from the lungs. These findings mightxplain the correlations of TLC and Raw with the modifi-ations of vertical alignment of the trunk observed in theresent study.

Unlike Boulay et al.31, we did not find a correlationetween pelvic misalignment and lung volume. However,e did observe a negative correlation of pelvic misalign-ent with muscle strength and peak flow, and we observed

igher values on the right side for all variables. Ourypothesis is that there is a difference in the extent ofulmonary parenchyma damage. Greater alveolar destruc-ion in one lung results in increased ‘air trapping’ andonsequent rectification and shortening of the ipsilateraliaphragm, intercostal, and abdominal muscles. These one-ided changes might favor muscle imbalance and result inelvic unleveling.

Increased DLco has been described in patients withsthma, including those with stable disease.32,33 Severalechanisms have been proposed as possible explanations

or this abnormality, including increased perfusion of lungpices due to increased pulmonary arterial pressure or moreegative pleural pressure as a consequence of bronchialarrowing.32 In the present study, we did not find anyorrelations among DLco, body composition, or postural dis-rders.

A critical analysis of the results and their limitations isppropriate. Respiratory and peripheral muscle strength andody composition are affected by oral steroid use, which isommonly prescribed to patients with asthma. Therefore,uch medications might be a confounding factor. Due to theack of a control group, we could not establish the influencef corticosteroids in the investigated sample. In addition,he present study is a cross-sectional analysis. It only indi-ates associations, it does not establish of cause-effectelationships. However, because there are few publishedtudies regarding body posture of this group of patients, weelieve that our results are an important contribution to theeld.

In conclusion, our study demonstrates that adult patientsith asthma exhibit specific postural disorders such as

horacic hyperkyphosis and lumbar hyperlordosis. Theseostural abnormalities correlate with patients’ pulmonaryunction and body composition. The assessment of postural

ariables may provide a better pulmonary rehabilitationpproach for these patients.

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Correlation between pulmonary function, posture, and body

Ethical disclosures

Protection of human and animal subjects. The authorsdeclare that the procedures followed were in accordancewith the regulations of the relevant clinical research ethicscommittee and with those of the Code of Ethics of the WorldMedical Association (Declaration of Helsinki).

Confidentiality of data. The authors declare that they havefollowed the protocols of their work center on the publica-tion of patient data and that all the patients included in thestudy received sufficient information and gave their writteninformed consent to participate in the study.

Right to privacy and informed consent. The authors haveobtained the written informed consent of the patients orsubjects mentioned in the article. The corresponding authoris in possession of this document.

Authorship/collaborators

Vívian Pinto de Almeida, Fernando Silva Guimarães, SaraLucia Silveira de Menezes, Thiago Thomaz Mafort andAgnaldo José Lopes contributed to the conception andproject, article review and approval of the final version ofthe manuscript. Vanessa Joaquim Ribeiro Moco carried outthe analysis and interpretation of data, article review andapproval of the final version of the manuscript.

Conflicts of interest

The authors have no conflicts of interest to declare.

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