http://informahealthcare.com/ptp ISSN: 0959-3985 (print), 1532-5040 (electronic) Physiother Theory Pract, 2014; 30(2): 79–84 ! 2014 Informa Healthcare USA, Inc. DOI: 10.3109/09593985.2013.820246

RESEARCH REPORT

Correlation between posture, balance control, and peripheral muscle function in adults with cystic fibrosis Tatiana Rafaela Lemos Lima, PT1, Fernando Silva Guimara˜es, PT, PhD1,2, Arthur Sa´ Ferreira, PT, PhD1, Jennifer Taborda Silva Penafortes, PT, MSc1, Vı´vian Pinto Almeida, PT, MSc1, and Agnaldo Jose´ Lopes, MD, PhD1,3 Rehabilitation Science Graduate Program, Augusto Motta University, Rio de Janeiro, Brazil, 2School of Physiotherapy, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil, and 3Laboratory of Respiratory Physiology, State University of Rio de Janeiro, Rio de Janeiro, Brazil

Abstract

Keywords

Background: In addition to pulmonary involvement, adults with cystic fibrosis (CF) are at higher risk of developing skeletal muscle dysfunction, nutritional depletion, and bone and joint disease. Objective: This study aimed to assess the correlation between posture, balance, and peripheral muscle function in adults with CF. Methods: A cross-sectional study of 14 clinically stable patients who were subjected to postural assessment (photogrammetry), stabilometry, and peripheral muscle function. Results: Comparing the right and left sides of the body, there were significant differences for the following variables: horizontal and vertical head alignments; heel angle; and vertical alignment of the trunk (p50.001 for all). Variables that represent the head-trunk position and the position of the lower limbs showed correlations with stabilometric parameters. The strongest correlation was observed between the vertical alignment of the body and the medial-lateral range ( ¼ 0.73; p ¼ 0.002). We also noted a significant correlation between the quadriceps muscle strength and the medial lateral range ( ¼ 0.69; p ¼ 0.003). Conclusions: In adults with CF, it is possible that the imbalance occurs by both distortion of the head–trunk relationship and lower extremity abnormalities as noted by the reduced quadriceps muscle strength.

Cystic fibrosis, posture, postural balance, psychomotor performance

Introduction Cystic fibrosis (CF) is the most common potentially lethal autosomal recessive disease of Caucasians. It is caused by mutations of the gene encoding for CF transmembrane conductance regulator (CFTR) (Rowe, Miller, and Sorscher, 2005). The median survival rate in CF patients in developed countries is currently over 30 years, with lung disease accounting for the majority of deaths (Bellis et al, 2007; Dodge, Lewis, Stanton, and Wilsher 2007; Salvatore et al, 2012). Based on data from the United Kingdom, CF individuals born after the year 2000 are projected to survive until the age of at least 50 (Quon and Aitken, 2012). Several factors have been attributed to the improved survival rate, including earlier diagnoses, the establishment of specialized care centers, new and better medications, better dietary management, physiotherapy and organ transplantation (Yankaskas et al, 2004). Physiotherapy has long been considered a cornerstone of condition management for people with CF. Airway clearance therapy, exercise, treatment to promote continence and good posture, and noninvasive ventilation are considered cornerstones of treatment (Daniels, 2010; Flume et al, 2009). Better chronic maintenance therapies to prevent loss of lung function, including inhaled antibiotic to treat infection, azithromycin to reduce inflammation, and aerosolized recombinant human DNase are

Address correspondence to Agnaldo Jose´ Lopes, MD, PhD, State University of Rio de Janeiro, Laboratory of Respiratory Physiology, Rua Araguaia, 1266, bloco 1, Freguesia, Jacarepagua´, Rio de Janeiro 22745-271, Brazil. E-mail: [email protected]

History Received 8 November 2012 Revised 10 April 2013 Accepted 11 May 2013 Published online 26 July 2013

also hypothesized reasons for improved survival (Heijerman et al, 2009; Quon and Aitken, 2012). However, as the life expectancy of CF patients continues to improve, the consequences of the condition that are not apparent at a young age may become clinically significant at an older age. The multisystemic components of CF cause important physical limitations in these patients. Following the chronicity of the disease, the hyperinflation of the chest can lead to a series of offsets in the thoracic spine, shoulder girdle and pelvic girdle. Hyperinflation shortens the operating length of the inspiratory muscles, which places them at a mechanical disadvantage and decreases their excursion (Reid et al, 2008). Adults with CF are also at higher risk of developing secondary impairments in their musculoskeletal system, including reduced peripheral muscle strength (Dunnink, Doeleman, Trappenburg, and de Vries, 2009; Elkin et al, 2000; Troosters et al, 2009). Low bone density, pathological fractures of the long bones, vertebrae and ribs, and high rates of kyphosis are complications that are related to CF (Elkin et al, 2001). Factors contributing to bone disease in CF patients include malnutrition, physical inactivity, malabsorption of vitamin D, and glucocorticoid therapy (Aris et al, 2005). CF patients have also been reported to have less peripheral muscle strength and function. However, it is still uncertain whether muscle damage is caused by metabolic, hormonal, or neuromuscular factors (Sahlberg, Svantesson, Thomas, and Strandvik, 2005). Posture is the regular and balanced arrangement of skeletal components to preserve the supportive structures of the body from injury and progressive deformation, as well as the rotational and translational positions of adjoining body segments and their

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orientation relative to gravity (Fabris de Souza et al, 2005). In an optimal alignment, it is expected that the muscles and joints are in dynamic balance, generating a minimal amount of effort and overhead, which leads to the optimum efficiency of the musculoskeletal system. In this sense, postural assessment is fundamentally important for diagnosing, planning, and monitoring the progress and results of physiotherapy (Zagyapan et al, 2012). Balance can be defined as the ability to maintain an appropriate relationship between body segments and the environment adjusting the body to control the center of gravity (CoG) amplitude and the task performed as well as properly positioning the center of mass (CoM) in relation to the support base (Pompeu, Romano, Pompeu, and Lima, 2012). CoM is the point on a body that moves in the same way that a particle subject to the same external forces would move (Rodgers and Cavanagh, 1984). CoM represents the displacement point for the center of pressure (CoP) because the CoP serves as the location point of the average distribution for all the pressure over the ground surface contact area. The CoP displacement represents the sum of the actions of the postural control system and the force of gravity (Gravante, Russo, Pomara, and Ridola, 2003). Spatial orientation in balance control is based on the interpretation of convergent information from the somatosensory, visual, and vestibular systems. Additionally, the proprioceptive muscle inputs originating from body parts, such as the foot–floor interface and the relationship of the head to the trunk, can contribute equally to balance (Johnson and Van Emmerik, 2012; Kavounoudias, Gilhodes, Roll, and Roll, 1999). When one of the inputs is disturbed, the central nervous system has to re-weigh the interaction from the remaining inputs to promote postural and balance control. In adults with CF, these systems are healthy, except for the musculoskeletal, which is the effector portion related to the motor responses of balance control (Troosters et al, 2009). The investigation of postural control, balance and peripheral muscle function in adults with CF is important because it can provide new information for the therapeutic approach in these patients. We hypothesize that sensorimotor inputs are impaired in adults with CF because of alterations in postural alignment and that balance control is ultimately compromised. Thus, the purpose of this study was to assess the correlation between posture, balance and peripheral muscle function in adults with CF.

Methods Patients We conducted a cross-sectional study with patients recruited at the Piquet Carneiro Polyclinic, State University of Rio de Janeiro, Brazil. Adult patients (aged 18 years or older) were included if they had clinical and laboratorial diagnoses of CF (sweat test and/or deoxyribonucleic acid (DNA) mutation analysis). The exclusion criteria included: using psychotropic medications; concomitant neurological, cardiovascular, metabolic, rheumatic or vestibular diseases; physical disabilities that impaired locomotion; orthopedic problems; or a history of musculoskeletal system operations. All patients continued their regular treatment for the duration of the study following the recommendations of the CF Foundation (Flume et al, 2007). The present investigation was approved by the Research Ethics Committee of the Augusto Motta University (# 012/2011), and all of the participants signed informed consent forms. Measurements In this study, pancreatic insufficiency was considered when fecal elastase level was 100 mg/g stool (Borowitz et al, 2012).

Physiother Theory Pract, 2014; 30(2): 79–84

CF related diabetes was diagnosed by a plasma glucose 11 mmol/L at a 2 h oral 75 g glucose tolerance test (Hillman et al, 2012). Spirometry was performed using the computerized Collins Plus Pulmonary Function Testing Systems (Warren E. Collins, Inc., Braintree, MA). Pereira, Sato, and Rodrigues (2007) equations were used to interpret the following pulmonary function parameters: forced vital capacity (FVC), forced expiratory volume in the first second (FEV1) and FEV1/FVC. Postural assessment was performed using photogrammetry with postural assessment software (PAS) (FAPESP Virtual Incubator, SP, Brazil; Ferreira et al, 2010) at the Human Movement Laboratory, Augusto Motta University. Coordinates of anatomical points (right and left tragus, right and left acromion, right and left greater trochanter of the femur, and spinous processes of the seventh cervical and third thoracic vertebrae) were labeled with passive markers (Styrofoam balls attached with double-sided adhesive tape), and photographs of the anterior, posterior, and right and left lateral views were taken for all the participants. The photographs were then transferred to a compatible microcomputer and analyzed. The following angles were used for the PAS protocol: (1) Anterior view: head – horizontal alignment (HHA) ¼ angle between the right-left tragus and a horizontal line; acromion – horizontal alignment (AHA) ¼ angle between the right–left acromion and a horizontal line; difference between lower limbs (DBLL) ¼ difference between right and left distances from anterior-superior iliac spine to medial malleoli; (2) Right and left view: head – horizontal alignment (HHA) ¼ angle between the spinal process of the seventh cervical (C7) vertebra, the ear lobe (tragus) and a horizontal line; (3) head – vertical alignment (HVA) ¼ angle between the tragus, the acromion, and a vertical line; lower limbs frontal angle (LLFA) ¼ angle between the greater trochanter, the lateral projection of the knee joint line and the lateral malleoli; (4) leg – heel angle (LHA) ¼ angle between the midpoint of the leg, the intermalleolar line and the bilateral calcaneal tendon; hip angle (HA) ¼ angle between the anterior-superior iliac spine, the large trochanter of the femur, and the articular line of the knee; (5) trunk – vertical alignment (TVA) ¼ angle between the acromion, the greater trochanter, and a vertical line; (6) body – vertical alignment (BVA) ¼ angle between the acromion, the lateral malleolus, and a vertical line; (7) pelvis – horizontal alignment (PHA) ¼ angle between the anterior-superior iliac spine, the posterior-superior spine iliac, and a horizontal line; (8) knee angle (KA) ¼ angle between the greater trochanter, the projection of the knee joint line, and the lateral malleolus; and (9) ankle angle (AA) ¼ angle between the projection of the knee joint line, the lateral malleolus, and a horizontal line (Ferreira et al, 2011). The subjects performed force plate stabilometry (AccuSway Plus, AMTI, Watertown, MA), and the data collected were analyzed using Suite EBG software version 1.0 at the Human Movement Laboratory, Augusto Motta University. All of the participants were tested in two positions: (1) feet apart, eyes open (FAEO) with heels 30 cm apart; and (2) feet together, eyes closed (FTEC) (feet parallel and 51 cm apart). The patients were asked to maintain a static position with their eyes focused on a target on the wall for 30 s. The following stabilometric variables were calculated: medial–lateral range; anterior–posterior range; effective area; length; and average velocity (Era, Sainio, and Koshinen, 2006; Mainenti et al, 2011). The peripheral muscle function was assessed using isometric dynamometry (model DIN-TRO, EMG System do Brasil LTDA, Brazil) and an endurance test with surface electromyography (model EMG 810 C, EMG System do Brasil LTDA, Brazil). Subjects were instructed to fold their arms across their chest and the seat was adjusted to allow 90 degrees of flexion of the hip joint. EMG surface electrodes were placed on the quadriceps

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(vastus medialis), according to the SENIAM recommendations (Hermens, Freriks, Disselhorst-Klug, and Rau, 2000). Maximal voluntary isometric contractions (MVIC) were performed at 90 degrees of knee flexion for the quadriceps muscles, with the leg contracting to move toward extension; each test was performed three times with a 2-min rest period between trials and the highest value was chosen. The muscle endurance test consisted of a sustained 60-s contraction using 30% of the MVIC obtained in the strength test. The median frequency and root mean square slopes (MDF and RMS, respectively) corresponding to the EMG signal during isometric contraction over time were used to analyses the quadriceps fatigability (Mathur, Eng, and MacIntyre, 2005). A control group (CG) of 14 healthy volunteers (8 male) also performed the MVIC and quadriceps fatigability test and spirometry examination using the same protocols described above. This group had the following anthropometric characteristics: age ¼ 26.1 (21–32.5) years; height ¼ 171 (163–171) cm; weight ¼ 71.6 (58.2–80.5) kg; and body mass index (BMI) ¼ 25.3 (20.7–27.8) kg/m2. Only weight and BMI were statistically different between healthy volunteers and CF patients (p ¼ 0.002 and p ¼ 0.004, respectively). However, the CG was not examined for postural assessment or stabilometry. All tests were performed within 1 week and in the following order: anthropometric and clinical evaluation; spirometry; postural assessment; stabilometry; and muscular strength/endurance. Postural assessment and stabilometry were done barefoot. Data analysis To check the homogeneity of the sample, KolmogorovSmirnov’s test was used for all variables except for those related to the two groups assessed for peripheral muscle function. In the latter set of variables, two multivariate analyses of variance (MANOVA) were conducted for one fixed factor with two levels (groups: CF and control) separately for the variables related to muscle and pulmonary function. The multivariate general linear model was used to test the null hypothesis of no main effects related to peripheral muscle function (RMS slope, MDF slope and quadriceps strength) and pulmonary function (FVC% predicted, FEV1% predicted, and FEV1/FVC% predicted) on groups. Due to the small sample size, the Box’s M test was performed to test the assumptions that dependent variables follow a multivariate normal distribution, and the variancecovariance matrices are equal across the cells formed by the between-subjects effects. Likewise, Levene’s test was used to test the assumption of equality of the error variances across the cells defined by the combination of factor levels. The nonparametric tests were used to analyze data with a statistically non-normal distribution; conversely, a parametric analysis was applied to normally distributed data. The results were expressed as median and interquartile range values, or mean and standard deviations values. The MannWhitney test was used to compare groups’ anthropometric characteristics; to compare right and left sides in PAS analysis; and to compare stabilometric parameters between the two positions (FAEO versus FTEC). Spearman’s rank correlation coefficient was calculated to investigate associations. Correlation coefficients 50.25 (or 0.25) represents a weak correlation; those between 0.25 and 0.50 (or 0.25 and 0.50) represents a reasonable correlation; those between 0.50 and 0.75 (or 0.50 and 0.75) represents a moderate to good correlation; those40.75 (or 0.75) represents a good to excellent correlation (Dawson and Trapp, 2004). Data analysis was performed using SAS 6.11 software (SAS Institute, Inc., Cary, NC). The statistical significance level was set at p50.05.

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Results Among the 27 subjects who were initially eligible for assessment, 15 were excluded. Of the excluded patients, eight were excluded because they declined to participate and six for limited mobility. One patient was excluded for vestibular disease. Thus, 14 patients completed the study. The anthropometric and clinical data of the studied subjects are summarized in Table 1. Overall, 8 patients (57%) were male and the median age was 24.5 years (20–34 years). No patient had a history of fractures of the long bones, vertebrae and ribs, or physical examination with relevant kyphosis. The postural assessment data are described in Table 2, and the stabilometric data are shown in Table 3. Comparing the right and left sides of the body, there were significant differences for the following variables: head – horizontal alignment (HHA); head – vertical alignment (HVA); leg – heel angle (LHA); and trunk – vertical alignment (TVA) (p50.001 for all). All of the stabilometric parameters were significantly different between the two positions that were evaluated (FAEO versus FTEC) (p50.001 for all). MANOVA of muscle function variables revealed a significant multivariate main effect for group [Wilks’ Lambda ¼ 0.568, Table 1. Anthropometric and clinical data (N ¼ 14 patients). Demographic characteristics

Values N¼8 24.5 170 54 20.5

Sex (male) Age (years) Height (cm) Weight (kg) BMI (kg/m2) Clinical data Pancreatic insufficiency (%) Cystic fibrosis related diabetes (%) Use of aerosolized recombinant human DNase (%) Use of inhaled antibiotic (%)

(57%) (20–34) (160–170) (47.5–68.9) (18.2–25.1)

13 (93) 6 (43) 11 (79) 10 (71)

Results are medians (interquartile ranges) or number (%). BMI, body mass index. Table 2. Values of postural assessment software in adults with cystic fibrosis. Variables

Values 

HHA (AV) ( ) AHA (AV) ( ) DBLL ( )

2.80 (0 to 7.90) 1.35 (0 to 7.40) 1.15 (1.70 to 2.50) Right



HHA (SV) ( ) HVA ( ) LLFA ( ) LHA ( ) HA ( ) TVA ( ) BVA ( ) PHA ( ) KA ( ) AA ( )

8.55 12.3 1.80 0.70 42.9 2.15 14.9 1.95 5.20 2.75

(26.7 (0.80 (6.30 (8.10 (1.50 (9.10 (11.9 (5.20 (15.4 (0.50

Left to to to to to to to to to to

37.1) 31.0) 4.20) 13.9) 52.9) 17.6) 33.7) 4.60) 7.10) 80.8)

5.60 3.80 2.35 85.6 41.2 82.5 13.6 2.50 5.85 1.60

(14.0 to 37.1) (12.0 to 11.0) (5.70 to 3.00) (6.60 to 90.6) (11.6 to 55.8) (0.60 to 90.7) (0 to 31.0) (9.60 to 0.40) (13.5 to 11.2) (0.50 to 81.1)

Results are medians (interquartile ranges). HHA (AV), head – horizontal alignment (anterior view); AHA (AV), acromion – horizontal alignment (anterior view); DBLL, difference between lower limbs; HHA (SV), head – horizontal alignment (side view); HVA, head – vertical alignment; LLFA, lower limbs frontal angle; LHA, leg – heel angle; HA, hip angle; TVA, trunk – vertical alignment; BVA, body – vertical alignment; PHA, pelvis – horizontal alignment; KA, knee angle; AA, ankle angle.

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Table 3. Stabilometry values in adults with cystic fibrosis. Variables

Trials

Medial-lateral range (cm)

FAEO FTEC FAEO FTEC FAEO FTEC FAEO FTEC FAEO FTEC

Antero-posterior range (cm) Effective area (cm2) Length (cm) Average velocity (cm/s)

Values 0.13 0.43 0.24 0.34 0.23 0.97 11.6 26.5 0.39 0.92

(0.11–0.14) (0.35–0.68) (0.21–0.37) (0.31–0.56) (0.17–1.28) (0.70–2.01) (9.66–12.2) (24.1–32.4) (0.32–0.51) (0.80–1.44)

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Results are medians (interquartile ranges). FAEO, feet apart, eyes open; FTEC, feet together, eyes closed.

F(3,24) ¼ 6.095, p ¼ 0.003, 2 ¼ 0.432]. In comparison to the CG, adults with CF showed higher mean values of RMS slope (CF: 0.624  0.465; CG: 0.308  0.257, p ¼ 0.03), which suggests low localized muscle resistance to fatigue. Also, adults with CF presented lower mean values of quadriceps strength (CF: 33.1  15.7 kg; CG: 52.2  13.3 kg, p ¼ 0.002), indicating lower localized muscle strength. No significant difference was observed in CF adults concerning mean values of MDF slope (CF:  0.261  0.219; CG: 0.266  0.261, p ¼ 0.95). Box’s M text showed that the assumptions of multivariate normal distribution and equality of covariances were met since F(6,4897.811) ¼ 1.183 (p ¼ 0.31) and thus the results of the model are trustworthy. Levene’s test showed no violation of the equality of error variances for all muscle function variables (RMS: p ¼ 0.06; MDF: p ¼ 0.60; quadriceps strength: p ¼ 0.68). MANOVA of pulmonary function variables revealed a significant multivariate main effect for group [Wilks’ Lambda ¼ 0.406, F(3,24) ¼ 11.713, p50.001, 2 ¼ 0.594]. In comparison to the CG, adults with CF showed lower mean values of FVC (CF: 75.3  27.2% predicted; CG: 102.2  13.8% predicted, p ¼ 0.003); lower mean values of FEV1 (CF: 57.5  28.4% predicted; CG: 101.4  11.8% predicted, p50.001); and lower mean values of FEV1/FVC (CF: 63.1  15.4% predicted; CG: 84.8  3.0% predicted, p50.001). Although the Box’s M text showed that the assumptions of multivariate normal distribution and equality of covariances were not met (F(6,4897.811) ¼ 8.588; p50.001), the impact is minimal since the number of subjects is the same in both groups. Levene’s test also showed violation of the equality of error variances for all pulmonary function variables (FVC: p ¼ 0.016; FEV1: p ¼ 0.004; FEV1/FVC: p50.001). Table 4 shows the correlations between the postural assessment measurements and stabilometric values; only the statistically significant data are shown. Regarding peripheral muscle function and balance, we observed significant correlations of RMS with: medial-lateral range in FTEC ( ¼ 0.53; p ¼ 0.024); and average velocity in FAEO ( ¼ 0.50; p ¼ 0.038), and significant correlations of quadriceps muscle strength with: medial-lateral range in FTEC ( ¼ 0.69; p ¼ 0.003); average velocity in FTEC ( ¼ 0.61; p ¼ 0.005); average velocity in FAEO ( ¼ 0.52; p ¼ 0.027); and effective area in FTEC ( ¼ 0.48; p ¼ 0.041). Regarding peripheral muscle function and posture, we observed significant correlations of RMS with: KA (right view) ( ¼ 0.46; p ¼ 0.043); and LLFA (left view) ( ¼ 0.44; p ¼ 0.047), and significant correlations of quadriceps muscle strength with: KA (right view) ( ¼ 0.48; p ¼ 0.042); and DBLL ( ¼ 0.42; p ¼ 0.048).

Table 4. Correlation between postural assessment measurements and stabilometric values in patients with cystic fibrosis (Spearman’s correlation test showing only statistically significant correlations). 

p Value

 0.53 0.62 Right

0.027 0.009 Left

Variables DBLL  Effective area FTEC DBLL  Length FAEO HHA  Anterior-posterior range FAEO HVA  Effective area FTEC LLFA  Medial–lateral range FTEC LLFA  Anterior–posterior range FAEO LLFA  Anterior–posterior range FTEC LLFA  Effective area FAEO LLFA  Average velocity FAEO LHA  Average velocity FAEO BVA  Medial-lateral range FTEC PHA  Effective area FTEC KA  Effective area FAEO KA  Average velocity FAEO KA  Average velocity FTEC KA  Anterior–posterior range FAEO

0.58

0.016 –

– 0.52

0.029

0.52

0.028

–

0.64

0.007

–

0.59

0.013

– 0.60 0.65

– – 0.48 0.73 0.65 0.50 0.48 0.64

0.041 0.002 0.006 0.034 0.042 0.007 –

0.011 0.006 – – – – – –

0.56

0.019

DBLL, difference between lower limbs; FTEC, feet together, eyes closed; FAEO, feet apart, eyes open; HHA, head – horizontal alignment; HVA, head – vertical alignment; LLFA, lower limbs frontal angle; LHA, leg – heel angle; BVA, body – vertical alignment; PHA, pelvis – horizontal alignment; KA, knee angle.

Discussion The following main findings were observed in the present investigation: in adults with CF, there was a strict association between the vertical alignment of the body and the medial-lateral range; both the head–trunk relationship and the lower extremity contributed to the imbalance; and the reduction of peripheral muscle strength showed a more negative impact on balance control than posture. To date, there do not appear to be any studies that have focused on this issue. The increased life expectancy in CF patients involves the development of secondary complications related to the musculoskeletal system, which may lead to changes in body posture (Aris et al, 2005; Sahlberg, Svantesson, Thomas, and Strandvik, 2005). Okuro et al (2012) assessed posture in children and adolescents with CF through the New York test (NYT), which is a scoring system where each body segment is scored according to the suitability of its alignment; these authors observed postural changes in 81% of cases. In our study, when the two sides of the body were compared on PAS, the main postural deviations occurred in the alignment of the head/trunk and in the angle of heel. Factors that may contribute to postural changes in patients with CF include: pulmonary hyperinflation; reduced muscle mass; bone demineralization; osteopenia; and chronic pain (Botton et al, 2003; Conway, 2001; Henderson and Specter, 1994). Although postural deviations alter the body mechanics, compensating adjustments prevent falling when the projection of the center of gravity moves beyond the sustaining base. Thus, the primary objective of such compensation is to maintain the functionality and adaptation of daily activities (Spoorenberg et al, 1999). The task of the postural control system is to keep the horizontal projection of the CoG of an individual within the base of support that is defined by the base area of the feet during a static stance. The stability is achieved by generating moments of force on the body joints to counteract the effects of gravity or

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other disturbances in a continuous and dynamic process during an individual’s stay in a particular posture. Thus, by eliminating visual input and narrowing the base of support (feet together, eyes closed), our adult CF patients showed worse imbalance in all of the measured stabilometric parameters (p50.05). Changing from standing with feet apart to feet together decreased whole-body movement patterns to control standing stability. Thus, stability decreased when the eyes were closed; this is a situation in which visual feedback is eliminated and better integration of somatosensory and vestibular inputs is required to ensure adequate postural control (Mainenti et al, 2011). A possible association between posture and balance has been poorly investigated in the literature. Danis, Krebs, Gill-Body, and Sahrmann (1998) showed that in both subjects with vestibular hypofunction and subjects without impairment, there is a low correlation between posture and standing stability (r50.3). Horak and Shupert (1994) have reported that subjects with vestibular hypofunction had a more forward head position than did subjects without impairment. In the present study, we investigated the posture in adult CF patients and its relationship to CoG stability. The variables measured on a force platform showed significant correlations, mainly with lower limbs frontal angle (LLFA) and knee angle (KA). Since the subjects with history of orthopedic problems or musculoskeletal surgery were excluded from the study, we believe that the peripheral muscle weakness may partially explain our results. As there is some evidence on the reduced joint range of motion in CF patients (Mandrusiak et al, 2010), we also hypothesize that the joint mobility of our sample might have influenced the imbalance results observed in our study. The multiple proprioceptive inputs originating from various parts of the body may be co-processed in terms of vector-addition laws; in humans, this vector may play an important role in the vertical alignment of body (Kavounoudias, Gilhodes, Roll, and Roll, 1999). In our study, the strongest correlation was observed between the vertical alignment of the body and the medial-lateral range, with the patient in the FTEC position ( ¼ 0.73; p ¼ 0.002). The anterior–posterior balance is maintained by torque at the ankle, but the medial-lateral balance is maintained by torques at the hips and trunk. Thus, as a result of hyperinflation, the increased activity of the trunk muscles enhances trunk stiffness and likely reduces the contribution of trunk movement and balance control (De Troyer, Leeper, McKenzie, and Gandevia, 1997). Our results showed that measurements that assess the positioning of the head and trunk [HHA and HVA] and those that assess the lower limbs [DBLL, LLFA, LHA, pelvis – horizontal alignment (PHA), and KA] correlated with abnormalities in stabilometric parameters. Because the muscle-spindle inputs form a proprioceptive chain that functionally links the head–trunk muscles to the lower extremity muscles (Kavounoudias, Gilhodes, Roll, and Roll, 1999), we think that the imbalance in adults with CF may result from several different mechanisms. In CF patients, pulmonary hyperinflation causes significant changes in the head–trunk relationship. An increased thoracic diameter can lead to a deficit in inspiratory muscle contraction and impair its ability to generate pressure. These muscles have insertions out of the trunk, which maintains the position of the head and shoulders. Thus, the altered position of the shoulders, which are now projected forward over the trunk, can cause head protrusion (Laghi and Tobin, 2003). Regarding the lower limbs, several studies have shown peripheral muscle atrophy and strength in CF patients, most likely because of malnutrition, physical inactivity, intrinsic muscle defect or a combination of these factors (Dunnink, Doeleman, Trappenburg, and de Vries, 2009; Lands, Heigenhauser, and Jones, 1993).

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Ultimately, these changes could contribute to increased amplitude of medial-lateral CoP displacement (Smith et al, 2010). It is worth noting that no postural variable showed association with balance for right and left sides. Since patients with localized and unrelated to CF sequelae were excluded from the study, we think that the multi-systemic components of CF are co-processed in terms of unilateral multiple vectors. In the present study, peripheral muscle strength was 55% lower in adults with CF compared with controls. This reduction in quadriceps strength was slightly greater to that reported in a study by Troosters et al (2009), which was 69%. It is of note that significant correlations were observed between the quadriceps fatigability/strength and stabilometric values. Several factors may contribute to skeletal muscle weakness in adults with CF, including systemic inflammation, oxidative stress, nutritional imbalance, electrolyte disturbances, and physical inactivity (Elkin et al, 2000; Gupta, Eastham, Wrightson, and Spencer, 2007). A critical analysis of the results and limitations is appropriate. One limitation of this study was the small sample size and the absence of a control group for all assessed outcome measures (postural assessment and stabilometry not tested and compared). However, because there are few published studies regarding posture and balance control of this group of patients, we believe that our results make an important contribution to the field. Future studies may provide comprehensive results by using more detailed statistical analyses by increasing the number of adult with CF, adding a control group and providing longitudinal follow-ups. We believe that the data in the present study may be important as end points for interventions in future investigations.

Conclusion The present results suggest that there is a relationship between posture, balance and peripheral muscle function in adults with CF, particularly between the vertical alignment of body and the medial-lateral range. It is possible that the imbalance occurs by both distortion of the head–trunk relationship and lower extremity abnormalities as noted by the reduced quadriceps muscle strength. The reduced quadriceps muscle strength shows a more negative impact on balance control than posture. The impact of these findings in subjects with CF is useful for evaluating the effect of intervention programs.

Declaration of interest The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the article.

References Aris RM, Merkel PA, Bachrach LK, Borowitz DS, Boyle MP, Elkin SL, Guise TA, Hardin DS, Haworth CS, Holick MF, Joseph PM, O’Brien K, Tullis E, Watts NB, White TB 2005 Consensus statement: Guide to bone health and disease in cystic fibrosis. Journal of Clinical Endocrinology and Metabolism 90: 1888–1896. Bellis G, Cazes MH, Parant A, Gaimard M, Travers C, Le Roux E, Ravilly S 2007 Cystic fibrosis mortality trends in France. Journal of Cystic Fibrosis 6: 179–186. Borowitz D, Stevens C, Brettman LR, Campion M, Wilschanski M, Thompson H; Liprotamase 767 Study Group 2012 Liprotamase longterm safety and support of nutritional status in pancreatic-insufficient cystic fibrosis. Journal of Pediatric Gastroenterology and Nutrition 54: 248–257. Botton E, Saraux A, Laselve H, Jousse S, Le Goff P 2003 Musculoskeletal manifestations in cystic fibrosis. Joint, Bone, Spine 70: 327–335. Conway SP 2001 Impact of lung inflammation on bone metabolism in adolescents with cystic fibrosis. Paediatric Respiratory Reviews 2: 324–331.

Physiother Theory Pract Downloaded from informahealthcare.com by University of Auckland on 10/16/14 For personal use only.

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T. R. L. Lima et al.

Daniels T 2010 Physiotherapeutic management strategies for the treatment of cystic fibrosis in adults. Journal of Multidisciplinary Healthcare 19: 201–212. Danis CG, Krebs DE, Gill-Body KM, Sahrmann S 1998 Relationship between standing posture and stability. Physical Therapy 78: 502–517. Dawson B, Trapp RG 2004 Basic and clinical biostatistics, 4th edn. New York, Lange Medical Books/McGraw-Hill. De Troyer A, Leeper JB, McKenzie DK, Gandevia SC 1997 Neural drive to the diaphragm in patients with severe COPD. American Journal of Respiratory and Critical Care Medicine 155: 1335–1340. Dodge JA, Lewis PA, Stanton M, Wilsher J 2007 Cystic fibrosis mortality and survival in the UK: 1947–2003. European Respiratory Journal 29: 522–526. Dunnink MA, Doeleman WR, Trappenburg JC, de Vries WR 2009 Respiratory muscle strength in stable adolescent and adult patients with cystic fibrosis. Journal of Cystic Fibrosis 8: 31–36. Elkin SL, Fairney A, Burnett S, Kemp M, Kyd P, Burgess J, Compston JE, Hodson ME 2001 Vertebral deformities and low bone mineral density in adults with cystic fibrosis: A cross-sectional study. Osteoporosis International 12: 366–372. Elkin SL, Williams L, Moore M, Hodson ME, Rutherford OM 2000 Relationship of skeletal muscle mass, muscle strength and bone mineral density in adults with cystic fibrosis. Clinical Science 99: 309–314. Era P, Sainio P, Koshinen S 2006 Postural balance in a random sample of 7,979 subjects aged 30 years and over. Gerontology 52: 204–213. Fabris de Souza SA, Faintuch J, Valezi AC, Sant’Anna AF, Gma-Rodrigues JJ, de Batista Fonseca IC, de Melo RD 2005 Postural changes in morbidly obese patients. Obesity Surgery 15: 1013–1016. Ferreira EA, Duarte M, Maldonado EP, Bersanetti AA, Marques AP 2011 Quantitative assessment of postural alignment in young adults based on photographs of anterior, posterior, and lateral views. Journal of Manipulative and Physiological Therapeutics 34: 371–380. Ferreira EA, Duarte M, Maldonado EP, Burke TN, Marques AP 2010 Postural assessment software (PAS/SAPO): Validation and reliability. Clinics 65: 675–681. Flume PA, O’Sullivan BP, Robinson KA, Goss CH, Mogayzel Jr PJ, Willey-Courand DB, Bujan J, Finder J, Lester M, Quittell L, Rosenblatt R, Vender RL, Hazle L, Sabadosa K, Marshall B 2007 Cystic fibrosis pulmonary guidelines: Chronic medications for maintenance of lung health. American Journal of Respiratory and Critical Care Medicine 176: 957–969. Flume PA, Robinson KA, O’Sullivan BP, Finder JD, Vender RL, Willey-Courand DB, White TB, Marshall BC; Clinical Practice Guidelines for Pulmonary Therapies Committee 2009 Cystic fibrosis pulmonary guidelines: Airway clearance therapies. Respiratory Care 54: 522–537. Gravante G, Russo G, Pomara F, Ridola C 2003 Comparison of ground reaction forces between obese and control Young adults during quiet standing on a baropodometric platform. Clinical Biomechanics 18: 780–782. Gupta A, Eastham KM, Wrightson N, Spencer DA 2007 Hypomagnesaemia in cystic fibrosis patients referred for lung transplant assessment. Journal of Cystic Fibrosis 6: 360–362. Heijerman H, Westerman E, Conway S, Touw D, Do¨ring G; Consensus Working Group 2009 Inhaled medication and inhalation devices for lung disease in patients with cystic fibrosis: A European consensus. Journal of Cystic Fibrosis 8: 295–315. Henderson RC, Specter BB 1994 Kyphosis and fractures in children and young adults with cystic fibrosis. Journal of Pediatrics 125: 208–213. Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G 2000 Development of recommendations for SEMG sensors and sensor placement procedures. Journal of Electromyography and Kinesiology 10: 361–374. Hillman M, Eriksson L, Mared L, Helgesson K, Landin-Olsson M 2012 Reduced levels of active GLP-1 in patients with cystic fibrosis with and without diabetes mellitus. Journal of Cystic Fibrosis 11: 144–149.

Physiother Theory Pract, 2014; 30(2): 79–84

Horak FB, Shupert C 1994 Role of the vestibular system in postural control. In: Herdman S (ed) Vestibular rehabilitation, pp 22–46. Philadelphia: FA Davis. Johnson MB, Van Emmerik REA 2012 Effect of head orientation on postural control during upright stance and forward lean. Motor Control 16: 81–93. Kavounoudias A, Gilhodes JC, Roll R, Roll JP 1999 From balance regulation to body orientation: Two goals for muscle proprioceptive information processing? Experimental Brain Research 124: 80–88. Laghi F, Tobin MJ 2003 Disorders of the respiratory muscles. American Journal of Respiratory and Critical Care Medicine 168: 10–48. Lands LC, Heigenhauser GJF, Jones NL 1993 Respiratory and peripheral muscle function in cystic fibrosis. American Review of Respiratory Disease 147: 865–869. Mainenti MRM, Rodrigues EC, Oliveira JF, Ferreira AS, Dias CM, Silva ALS 2011 Adiposity and postural balance control: Correlations between bioelectrical impedance and stabilometric signals in elderly Brazilian women. Clinics 66: 1513–1518. Mandrusiak A, Giraud D, MacDonald J, Wilson C, Watter P 2010 Muscle length and joint range of motion in children with cystic fibrosis compared to children developing typically. Physiotherapy Canada 62: 141–146. Mathur S, Eng JJ, MacIntyre DL 2005 Reliability of surface EMG during sustained contractions of the quadriceps. Journal of Electromyography and Kinesiology 15: 102–110. Okuro RT, Coˆrrea EP, Conti PBM, Ribeiro JD, Ribeiro MAGO, Schivinski CIS 2012 Influence of thoracic spine postural disorders on cardiorespiratory parameters in children and adolescents with cystic fibrosis. Jornal de Pediatria (Rio de Janeiro) 88: 310–316. Pereira CAC, Sato T, Rodrigues SC 2007 New reference values for forced spirometry in white adults in Brazil. Jornal Brasileiro de Pneumologia 33: 397–406. Pompeu JE, Romano RSL, Pompeu SMAA, Lima SMAL 2012 Static and dynamic balance in subjects with ankylosing spondylitis: Literature review. Revista Brasileira de Reumatologia 52: 409–416. Quon BS, Aitken ML 2012 Cystic fibrosis: What to expect now in the early adult years. Paediatric Respı´ratory Reviews 13: 206–214. Reid WD, Geddes EL, O’Brien K, Brooks D, Crowe J 2008 Effects of inspiratory muscle training in cystic fibrosis: A systematic review. Clinical Rehabilitation 22: 1003–1013. Rodgers MM, Cavanagh PR 1984 Glossary of biomechanical terms, concepts, and units. Physical Therapy 64: 1886–1902. Rowe SM, Miller S, Sorscher EJ 2005 Cystic fibrosis. New England Journal of Medicine 352: 1992–2001. Sahlberg ME, Svantesson U, Thomas EM, Strandvik B 2005 Muscular strength and function in patients with cystic fibrosis. Chest 127: 1587–1592. Salvatore D, Buzzetti R, Baldo E, Furnari ML, Lucidi V, Manunza D, Marinelli I, Messore B, Neri AS, Raia V, Mastella G 2012 An overview of international literature from cystic fibrosis registries. Part 4: update 2011. Journal of Cystic Fibrosis 11: 480–493. Smith MD, Chang AT, Seale HE, Walsh JR, Hodges PW 2010 Balance is impaired in people with chronic obstructive pulmonary disease. Gait and Posture 31: 456–460. Spoorenberg A, van der Heijde D, de Klerk E, Dougados M, de Vlam K, Mielants H, van der Tempel H, van der Linden S 1999 A comparative study of the usefulness of the Bath ankylosing spondylitis functional index and the Dougados functional index in the assessment of ankylosing spondylitis. Journal of Rheumatology 26: 961–965. Troosters T, Langer D, Vrijsen B, Seders J, Wouters K, Janssens W, Gosselink R, Decramer M, Dupont L 2009 Skeletal muscle weakness, exercise tolerance and physical activity in adults with cystic fibrosis. European Respiratory Journal 33: 99–106. Yankaskas JR, Marshall BC, Sufian B, Simon RH, Rodman D 2004 Cystic fibrosis adult care: Consensus conference report. Chest 125(Supplement 1): 1S–39S. Zagyapan R, Iyem C, Kurkcuoglu A, Pelin C, Tekindal MA 2012 The relationship between balance, muscles, and anthropomorphic features in young adults. Anatomy Research International 2012: 146063.