ORIGINAL RESEARCH ARTICLE Open Access Extrapulmonary .
Ozalp et al. Multidisciplinary Respiratory Medicine 2012, 7:3http://www.mrmjournal.com/content/7/1/3ORIGINAL RESEARCH ARTICLEOpen AccessExtrapulmonary features of bronchiectasis: musclefunction, exercise capacity, fatigue, andhealth statusOzge Ozalp1, Deniz Inal-Ince1*, Ebru Calik1, Naciye Vardar-Yagli1, Melda Saglam1, Sema Savci2, Hulya Arikan1,Meral Bosnak-Guclu3 and Lutfi Coplu4AbstractBackground: There are limited number of studies investigating extrapulmonary manifestations of bronchiectasis.The purpose of this study was to compare peripheral muscle function, exercise capacity, fatigue, and health statusbetween patients with bronchiectasis and healthy subjects in order to provide documented differences in thesecharacteristics for individuals with and without bronchiectasis.Methods: Twenty patients with bronchiectasis (43.5 14.1 years) and 20 healthy subjects (43.0 10.9 years)participated in the study. Pulmonary function, respiratory muscle strength (maximal expiratory pressure – MIP - andmaximal expiratory pressure - MEP), and dyspnea perception using the Modified Medical Research Council DyspneaScale (MMRC) were determined. A six-minute walk test (6MWT) was performed. Quadriceps muscle, shoulderabductor, and hand grip strength (QMS, SAS, and HGS, respectively) using a hand held dynamometer andperipheral muscle endurance by a squat test were measured. Fatigue perception and health status weredetermined using the Fatigue Severity Scale (FSS) and the Leicester Cough Questionnaire (LCQ), respectively.Results: Number of squats, 6MWT distance, and LCQ scores as well as lung function testing values and respiratorymuscle strength were significantly lower and MMRC and FSS scores were significantly higher in patients withbronchiectasis than those of healthy subjects (p 0.05). In bronchiectasis patients, QMS was significantly associatedwith HGS, MIP and MEP (p 0.05). The 6MWT distance was significantly correlated to LCQ psychological score(p 0.05). The FSS score was significantly associated with LCQ physical and total and MMRC scores (p 0.05). TheLCQ psychological score was significantly associated with MEP and 6MWT distance (p 0.05).Conclusions: Peripheral muscle endurance, exercise capacity, fatigue and health status were adversely affected bythe presence of bronchiectasis. Fatigue was associated with dyspnea and health status. Respiratory muscle strengthwas related to peripheral muscle strength and health status, but not to fatigue, peripheral muscle endurance orexercise capacity. These findings may provide insight for outcome measures for pulmonary rehabilitation programsfor patients with bronchiectasis.Keywords: Bronchiectasis, Exercise, Muscle function, Health status* Correspondence: dinalince@yahoo.com1Faculty of Health Sciences, Department of Physiotherapy and Rehabilitation,Hacettepe University, 06100 Samanpazari, Ankara, TurkeyFull list of author information is available at the end of the article 2012 Ozalp et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly cited.
Ozalp et al. Multidisciplinary Respiratory Medicine 2012, ndBronchiectasis is a chronic pulmonary disease which iscaused by the destruction of elastic tissue and smoothmuscles on bronchial walls due to repeated severe infectionor inflammation and characterized by abnormal permanentdilatation [1]. Previous studies determined that skeletalmuscle (respiratory and limb) abnormalities in addition torespiratory tract involvement are present in chronic inflammatory pulmonary diseases [2]. In these diseases, muscledysfunction is caused by inflammation, gas exchange abnormalities, electrolyte imbalance, inactivity, malnutritionand drugs [2]. Peripheral muscle weakness and lack of endurance negatively affect the exercise capacity and perception of fatigue in chronic respiratory airway diseases [2-4].Bronchiectasis is a common health problem for adultpopulations in developing countries [5]; however there is alimited number of studies investigating exercise capacityin adult patients [6-9]. Peripheral muscle function has notbeen studied in adult patients with bronchiectais. No studywas found by the authors in the literature that providedfindings in comparison with the results of healthy individuals. In the limited number of studies found, physical dimension of quality of life and localization of the diseasewere reported to affect exercise capacity [8], depressionwas related to exercise performance [7], and perceptionof dyspnea was related to exercise capacity [6]. No studyassociating peripheral and respiratory muscle weaknessin bronchiectasis with exercise capacity, respiratoryfunction and health status was found in the literature.Therefore, the aim of the present study was to evaluateextrapulmonary manifestations of bronchiectasis namelyperipheral muscle function, exercise capacity, fatigueand health status of adult patients with bronchiectasis incomparison with healthy individuals to provide dataabout deviation from the normal values of these characteristics in individuals with bronchiectasis.MethodsThe study included 20 adult patients with bronchiectasisdiagnosed in the Department of Chest Medicine by highresolution computed tomography (10 F, 10 M) and 20healthy subjects (13 M, 7 F). Consecutive patients whowere referred to the Cardiopulmonary RehabilitationUnit participated in the study. The mean ( SD) numberof lobes showing changes of bronchiectasis was 2.9 1.0(median: 3, range 1–5 lobes). The mean ( SD) timefrom the diagnosis was 12.8 11.8 years (median: 8,range 1–33 years). Individuals who were using antibiotics, had neurologic or orthopedic disease, advancedheart failure, or an acute exacerbation within the lastthree weeks were not included in the study. The controlgroup was composed of individuals who had no knownsystemic, orthopedic or neurologic disease, aged between 18–64 years, could walk and cooperate, and werePage 2 of 6voluntary subjects among the relatives of researchers andacademic personnel. Participants were informed about theaim and scope of the study, and written consent wasobtained from each participant. This prospective study wasapproved by Ethical Committee of Hacettepe University.Physical, physiological and socio-demographic characteristics of the subjects were recorded. Body Mass Index(BMI) was calculated by the formula of weight/height2(kg/m2). Fat free mass (FFM) was determined using theskinfold method (Skinfold Caliper, Holtain Ltd, Crosswell,UK) from biceps, triceps, subscapular, and suprailiacregions. Measurements were repeated three times and themean of three measurements was used [10].The pulmonary function test was performed in sittingposition using a spirometer (Spirolab III Medical International Research, Rome, Italy). Forced vital capacity(FVC), forced expiratory volume in one second (FEV1),FEV1/FVC, peak expiratory flow (PEF) and forced expiratory flow 25–75% (FEF25–75%) values were recorded. Parameters of the respiratory function test were expressed aspercentages of the expected values in accordance with thesubject’s age, height, body weight and sex [11].Respiratory muscle strength was measured with aportable electronic mouth pressure device (Micro MedicalMicroMPM, UK). Maximal inspiratory and expiratorymouth pressures (MIP and MEP) were recorded. MIP wasmeasured at residual volume, while MEP was determinedat total lung capacity. Measurements were repeated threetimes to avoid any difference larger than 10% or 10 cmH2O and the best measurement analysis was chosen.Values were expressed as percentages of the expectedvalues in terms of age and sex [12].Perception of dyspnea was evaluated by the ModifiedMedical Research Council (MMRC) dyspnea scale. TheMMRC is a 0–4 point category scale which selects thebest expression to define the dyspnea levels among fiveexpressions related to dyspnea [13].Peripheral muscle strength of the participants (quadriceps, shoulder abductor and hand grip strength) wasevaluated by digital dynamometer (JTECH, MedicalCommander Powertrack II, USA). Measurements wererepeated three times for the dominant side [14]. Thehighest value of the measurements was expressed inNewton (N). Peripheral muscle endurance was assessedby a squat test. In the squat test, subjects were asked tomove from a standing position to a squatting position.The number of squats completed in thirty seconds wasrecorded for analysis [14].For the six-minute walk test (6MWT), subjects wereasked to walk along a flat corridor at their walking speed asquickly as possible for six minutes [15]. In pre- and posttest periods, values of oxygen saturation were measured bypulse oximeter (KPTS-01, Seoul, Korea). Heart rate, bloodpressure and respiratory rate were also recorded. Perception
Ozalp et al. Multidisciplinary Respiratory Medicine 2012, 7:3http://www.mrmjournal.com/content/7/1/3of fatigue and dyspnea in pre- and post-test periods wasassessed with the Modified Borg Scale, which is a 0–10point category scale [16]. Upon completion of the test, thedistance covered in the 6-minute walk was recorded inmeters. The 6MWT was applied twice with an interval ofhalf an hour on the same day. For each patient, the longerwalking distance of two tests was used for statistical analysis[16]. The 6MWT distances expressed as percentages ofexpected values from age and sex (6MWT% of distance)were calculated [17].The Fatigue Severity Scale (FSS) was used to estimatethe fatigue level of the subjects [18]. The FSS is a onedimensional scale developed to assess fatigue and composed of nine items. The subject is asked to score eachexpression between 1 (completely agree) and 7 (completelydisagree). In the FSS, 4 points implies the presence ofsevere fatigue [18].Health status was assessed using the Leicester CoughQuestionnaire (LCQ). The LCQ is composed of 19 itemsand includes physical (8 items), psychological (7 items)and social (4 items) sub-dimensions. Each item is scoredbetween 1 (always) and 7 (never). The score of each subdimension ranges between 1 and 7. Total score rangesbetween 3 and 21. Low scores on the LCQ indicate ahigher effect of coughing on the subject [19].SPSS 15.0 packet software was used for the statisticalanalysis [20]. Variables were expressed as mean standarddeviation, frequency and percentages. The Shapiro Wilktest was used to analyze the suitability of variables to normal distribution [21]. The Student’s t-test was used for thecomparison of variables suitable for normal distribution.Mann–Whitney u-test was used to compare nonparametric variables not suitable for normal distribution. Comparison of the variables determined by counting wasperformed by the Chi-Square test. Corrected correlations(for age, weight, height and sex) were used to investigateassociation among the variables. The level of significancewas set to p 0.05.ResultsPhysical and demographic characteristics of patients withbronchiectasis and healthy subjects were similar in thestudy (p 0.05, Table 1). FVC, FEV1, FEV1/FVC, PEF,FEF25-75%, MIP, and MEP were significantly lower inpatients with bronchiectasis compared to healthy subjects (p 0.05, Table 1). The MIP of four subjects (20%)and MEP value of 15 subjects (75%) were lower than80% of their predicted value. The perception of dyspneain subjects with bronchiectasis determined using theMMRC was significantly higher than that in healthy subjects (p 0.05, Table 1).Although no significant difference was found betweensubjects with bronchiectasis and healthy subjects regardingperipheral muscle strength measures (p 0.05, Table 2),Page 3 of 6Table 1 Characteristics of patients with bronchiectasisand healthy subjectsCharacteristicsBronchiectasis(n 20)Healthy(n 20)p43.5 14.143.0 10.90.89110/1013/70.52Height (cm)165.6 8.7164.7 7.60.72Body weight (kg)68.8 16.475.4 12.90.17Body mass index(kg/m2)24.8 4.627.96 5.20.06Age (years)Sex (male/female)FFM (kg)50.4 11.456.23 10.40.096FVC (%)70.4 15.9100.3 12.7 0.0001*FEV1 (%)62.5 20.097.3 10.7 0.0001*FEV1/FVC (%)73.4 14.880.9 5.40.045*PEF (%)63.9 23.3101.8 15.2 0.0001*FEF25–75% (%)45.4 24.080.2 17.2 0.0001*MIP (cmH2O)97.5 30.3115.8 19.90.030*%MIP99.0 28.1109.4 21.40.019*MEP (cmH2O)125.8 33.6170.0 47.00.003*%MEP68.0 13.885.7 23.20.006*MMRC (0–4)1.55 0.600.20 0.52 0.0001**p 0.05.Table 1 legend - FEF25-75%, forced expiratory flow 25–75%; FEV1, forcedexpiratory volume in one second; FFM, fat free mass; FVC, forced vital capacity;MIP, maximal inspiratory pressure; MEP, maximal expiratory pressure; MMRC,Modified Medical Research Council dyspnea scale, PEF, peak expiratory flowrate.quadriceps muscle strength tended to be lower in the groupwith bronchiectasis ( p 0.050, Table 2). Quadriceps musclestrength was significantly associated with hand gripstrength (r 0.52, p 0.037), MIP (r 0.58, p 0.020) andMEP (r 0.66, p 0.029) in patients with bronchiectasis.The SAS was significantly correlated with MEP (r 0.53,p 0.035), and HGS was significantly associated with MIP(r 0.52, p 0.040).The number of squats was significantly lower in subjects with bronchiectasis compared to healthy subjects(p 0.05, Table 2). It was not significantly related withany of the variables measured (p 0.05).The 6MWT distance and 6MWT% distance were significantly lower in subjects with bronchiectasis whencompared to the healthy group, while exercise dyspneaperception was significantly higher in subjects with bronchiectasis (p 0.05, Table 2). No significant differencewas noted between the two groups in maximal heart ratepercentage, oxygen saturation, blood pressure, general fatigue or quadriceps fatigue perceptions recorded duringthe test (p 0.05). The 6MWT distance was significantlyrelated to LCQ psychological score (r 0.52, p 0.042) inpatients with bronchiectasis.Thirteen patients (65%) with bronchiectasis reportedhaving severe fatigue. The FSS value was significantlyhigher in the bronchiectasis compared to the healthygroup (p 0.05, Table 2). It was significantly associated
Ozalp et al. Multidisciplinary Respiratory Medicine 2012, 7:3http://www.mrmjournal.com/content/7/1/3Page 4 of 6Table 2 Peripheral muscle function, exercise capacity,fatigue and health status in patients with bronchiectasisand healthy subjectsBronchiectasis(n 20)Healthy(n 20)pKnee extension (N)266.7 63.3310.4 73.00.050Shoulder abduction (N)158.6 56.7183.0 50.60.15Hand grip (N)176.9 62.0198.7 54.50.1815.80 3.2822.50 4.43 0.0001*4.66 1.673.37 1.530.007*6MWT distance (m)559.2 98.7636.0 74.30.008*6MWT%90.5 14.3105.6 12.50.001*Borg-dyspnea2.20 1.900.07 0.24 0.001*Peripheral muscle strengthPeripheral muscle enduranceSquats (n)FatigueFatigue Severity ScaleExercise capacityBorg-fatigue1.77 1.890.92 1.430.26Borg-quadriceps fatigue1.65 1.890.95 2.300.16LCQ total14.67 3.8819.43 1.33 0.0001*LCQ physical4.51 1.376.53 0.75 0.0001*LCQ psychological4.81 1.126.01 0.32 0.0001*LCQ social5.33 1.656.87 0.32 0.0001*Health status*p 0.05.Table 2 legend - 6MWT, six minute walk test; LCQ, Leicester CoughQuestionnaire.with LCQ physical score (r 0.56, p 0.024), LCQ totalscore (r 0.50, p 0.047) and MMRC score (r 0.53,p 0.043).The LCQ total score and the scores of physical, psychological and social sub-dimensions were significantlylower in the bronchiectasis group than in healthy subjects(p 0.0001, Table 2). The LCQ total score was significantly related to FSS (r 0.50, p 0.047), and physicalscore was significantly and inversely related to FSS(r 0.56, p 0.024). The LCQ psychological score wassignificantly associated with MEP (r 0.51, p 0.044) and6MWT distance (r 0.52, p 0.042).DiscussionThe present study demonstrated that bronchiectasisaffects peripheral muscle endurance, exercise capacity,fatigue, and health status in addition to its effects on pulmonary function, inspiratory and expiratory musclestrength, and dyspnea perception in adult subjects withbronchiectasis. Exercise capacity is related to health status.Fatigue is affected by dyspnea perception and healthstatus.Different levels of respiratory dysfunction could be seenin bronchiectasis [5,22]. Mucociliary clearance dysfunction,bronchial inflammation and infection, irreversible bronchialdilatation, and destruction in elastic and muscular components of bronchial walls decreased expiratory air flow inthe lungs [1,5,23]. Effects on pulmonary function could beseen as obstructive, restrictive or of a mixed type [5,22].According to the results of pulmonary function tests in thestudy, mild airflow obstruction was determined in large airways, while severe obstruction was present in medium orsmall airways. These findings indicate that pulmonary function in our patients with bronchiectasis showed a patternof airflow limitation probably due to chronic inflammationand destroyed bronchial wall [5,22-24].In the present study, MIP and MEP were decreased inbronchiectasis. The MIP was lower than 80% of theexpected value in four subjects, and MEP was lower in15 subjects. This finding is considered significant as itdemonstrates the presence of respiratory muscle weakness which is especially evident for expiratory muscles insubjects with bronchiectasis. Respiratory muscle strengthhas been measured for adult patients with bronchiectasisin a limited number of studies in literature [9,25,26]. Inthe present study, the obtained MIP and MEP valueswere higher than the measurements reported by Moranet al. (MIP: 74.20 cmH2O; MEP: 104.30 cmH2O), Newallet al. (MIP: 73.86 cmH2O; MEP: 86.83 cmH2O), andMurray et al. (MIP: 43.5 cmH2O; MEP: 68.5 cmH2O)[9,25,26] probably due to the inclusion of youngerpatients with bronchiectasis who had better respiratoryfunction.Dyspnea is seen in 60% of patients with bronchiectasis[5,24]. We used MMRC to evaluate dyspnea, which isconsidered one of the major factors defining bronchiectasis [27] and affects the survival along with airway obstruction, pulmonary hyperinflation and frequency ofdisease [1]. In the present study, dyspnea perception wasevidently higher in patients with bronchiectasis whencompared to the healthy group, which demonstrates thatMMRC could distinguish the dyspnea level between subjects with bronchiectasis and healthy groups.In a comprehensive evaluation of skeletal muscle function, peripheral muscle strength and peripheral muscleendurance must be considered together [3]. In this regard, the present study is the first in the literature to investigate peripheral muscle strength and endurance inadult patients with bronchiectasis. In our study, isotonicmuscle strength of quadriceps tended to be lower thanthe values of the healthy group, while the peripheralmuscle endurance was evidently reduced. Quadricepsmuscle strength was found to be related to inspiratoryand expiratory muscle strength and peripheral muscleendurance in patients with bronchiectasis. Peripheralmuscle endurance was associated with expiratory musclestrength, upper and lower extremity muscle strength, exercise capacity, and fatigue perception. However, MEPwas the only variable having an independent relationship
Ozalp et al. Multidisciplinary Respiratory Medicine 2012, 7:3http://www.mrmjournal.com/content/7/1/3with quadriceps muscle strength, and quadriceps strengthwas the only variable having an independent associationwith peripheral muscle endurance. Skeletal muscles play animportant role both in motor (ventilation, ambulation andpostural control) and non motor functions (thermoregulation and systemic metabolism) [28]. These neural networksand the vulnerability of skeletal muscles - respiratory orperipheral - to syste
position using a spirometer (Spirolab III Medical Inter-national Research, Rome, Italy). Forced vital capacity (FVC), forced expiratory volume in one second (FEV 1), FEV 1/FVC, peak expiratory flow (PEF) and forced expira-tory flow 25–75% (FEF 25–75%) values were recorded. Para-
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