ORIGINAL ARTICLE
Influence of general clinical parameters on the quality of life of chronic obstructive
pulmonary disease patients*
VICTOR ZUNIGA DOURADO, LETÍCIA CLÁUDIA DE OLIVEIRA ANTUNES, LÍDIA RAQUEL DE CARVALHO, IRMA GODOY(TE SBPT)
Background: There is currently no consensus regarding which factors influence the quality of life of patients suffering from chronic obstructive pulmonary disease (COPD). However, identifying such factors could orient approaches to improving the quality of the lives of these patients.
Objective: To evaluate factors that can interfere with quality of life in COPD patients selected for pulmonary rehabilitation.
Methods: Twenty-one patients with moderate to severe COPD were evaluated. Maximal inspiratory pressure (MIP), 6-minute walk test (6MWT), body mass index (BMI), pulmonary function, blood gases, grip strength (measured with a dynamometer), quadriceps strength and St. George’s Respiratory Questionnaire (SGRQ) scores were assessed.
Results: Statistically significant negative correlations with quality of life were found for the following factors: “impact” scores of: forced expiratory volume in one second (FEV1) (r = -0.68; p = 0.004), FEV1 to forced vital capacity ratio (FEV1/FVC) (r = -0.61; p = 0.014), peak expiratory flow (PEF) (r = -0.53 (p = 0.015), 6MWT (r = -0.63; p = 0.001) and BMI (r = -0.64; p = 0.002); “activity” scores for: MIP (r = -0.57; p = 0.007), baseline arterial oxygen saturation by pulse oximetry (SpO2) (r = -0.52; p = 0.018) and 6MWT (r = -0.58; p = 0.007); “symptom” score for: BMI (r = -0.60; p = 0.005); and “total” scores for: FEV1 (r = -0.64; p = 0.01), PEF (r = -0.47; p = 0.033) and BMI (r = -0.57; p = 0.009). Multiple linear regression revealed the primary factors influencing quality of life to be: BMI, which presented a significant influence on “symptom”, “impact” and “total” scores (p = 0.002, p = 0.009 and p = 0.024, respectively); and 6MWT, which had a significant influence on “activity” and “impact” scores (p = 0.048 and p = 0.010, respectively).
Conclusions: The BMI and 6MWT were shown to have an influence on quality of life in the COPD patients studied. Therefore, therapeutic approaches to improving the quality of life of COPD patients should take these indices into consideration.
Key words: Lung diseases, obstructive/rehabilitation. Quality of life
* S t u d y c a r r i e d o u t a t t h e H o s p i t a l d a s C l í n i c a s o f t h e F a c u l d a d e d e M e d i c i n a d e B o t u c a t u , S ão P a u l o ( U N E S P ) i n t h e p u l m o n a r y r e h a b i l i t a t i o n p r o g r a m o f t h e P u l m o n o l o g y D e p a r t m e n t .
C o r r e s p o n d e n c e t o — V i c t o r Z u n i g a D o u r a d o . R u a A n t ô n i o A m a r a l C é s a r , 4 4 1 . V i l a M a r i a — B o t u c a t u - S P . C E P : 1 8 6 1 1 - 2 1 0 . P h o n e : 5 5 - 1 4 - 3 8 1 5 9 7 4 4 / 9 1 4 1 0 5 5 3 . e - m a i l : v z u n i g a @ u n i v e r s i a b r a s i l . n e t
There has been a recent upsurge in the number of studies assessing quality of life (QOL). Since it is often impossible to extend the life of patients suffering from incurable diseases, improving the
QOL of such patients should be made a priority( 1 , 2 ).
According to the American Thoracic Society
(ATS)( 3 ), QOL can be defined as satisfaction or
happiness with life in relation to what the individual considers important. In addition, it can be defined as the relationship between what is desired and what is achieved or achievable. The definition of QOL is broad and complex, made more so by the highly subjective nature of the concept.
In the elderly, chronic obstructive pulmonary disease (COPD) affects QOL and is the leading
cause of death( 1 ). Various aspects such as anxiety,
depression, a sensation of dyspnea, exercise intolerance, compromised nutritional state, chronic cough and disease severity may interfere
with QOL( 1 ). However, there is no consensus
regarding the influence of each factor on the QOL
of patients suffering from COPD( 4 ).
Pulmonary function data and QOL indices must be taken into consideration when determining the
severity of diseases such as COPD and asthma( 5 ).
However, the correlation between spirometry findings and QOL is weak or virtually
nonexistent( 6 - 1 0 ). In fact, the correlation between
the development of the pulmonary obstruction and lower QOL has not been demonstrated with consistency. Therefore, patient QOL cannot be
quantified based on spirometry data alone( 6 - 1 0 ).
Body mass index (BMI) is another important indicator of the health status of patients suffering
from COPD( 1 1 ). Those COPD patients presenting
low BMIs also score poorly on the St. George’s
Respiratory Questionnaire (SGRQ)( 7 ). Other factors
that have been related to QOL are age( 6 ), exercise
tolerance and muscle strength( 1 2 ), as well as
psychological aspects such as anxiety and
depression( 6 ).
Pulmonary rehabilitation programs that
resulted in improved peripheral( 1 2 ) and
respiratory( 1 3 ) muscle strength, as well as greater
exercise tolerance( 1 4 ) and higher BMI( 1 1 ), also
improved the QOL of COPD patients, suggesting that specific aspects influence QOL.
Taking into consideration the influence of various factors, such as those mentioned above, the objective of this study was to evaluate the main factors that may interfere with the QOL of patients suffering from COPD. The patients studied were selected for pulmonary
6 M W T — 6 - m i n u t e w a l k t e s t A T S — A m e r i c a n T h o r a c i c S o c i e t y B D I — B a sel i ne D y sp nea I nd e x B M I — B o d y m a s s i n d e x
C O P D — C h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e C R Q — C h r o n i c R e s p i r a t o r y Q u e s t i o n n a i r e F E V1 — F o r c e d e x p i r a t o r y v o l u m e i n o n e s e c o n d F V C — F o r c e d v i t a l c a p a c i t y
M E P — M a x i ma l e x p i r a to r y p r e s s ur e M I P — M a x i m a l i n s p i r a t o r y p r e s s u r e
M O S — M e d i c a l O u t c o m e s S t u d y S h o r t F o r m S u r v e y P a O2 — A r t e r i a l o x y g e n t e n s i o n
P E F — P e a k e x p i r a to r y fl o w Q O L — Q u a l i t y o f l i f e
R Q L Q — R e s p i r a t o r y Q u a l i t y o f L i f e Q u e s t i o n n a i r e
S F - 2 0 — M e d i c a l O u t c o m e s S t u d y S h o r t F o r m 2 0 - i t e m Q u e s t i o n n a i r e
S F - 3 6 — M e d i c a l O u t c o m e s S t u d y S h o r t F o r m 3 6 - i t e m Q u e s t i o n n a i r e
S G R Q — S t . G e o r g e ’ s R e s p i r a t o r y Q u e s t i o n n a i r e
S p O2 — A r teria l ox ygen sa tura tion
rehabilitation at the Hospital das Clínicas of the Faculdade de Medicina de Botucatu (SP).
METHOD
The study involved 21 patients of both genders diagnosed with COPD and selected for pulmonary
rehabilitation, independent of disease severity( 1 5 ).
The patients were clinically stable, without recent worsening of symptoms. None presented cardiovascular or osteoarticular involvement. Diagnosis was made through the analysis of clinical history of exposure to COPD risk factors and confirmed by spirometry. In accordance with the Global Initiative for Chronic Obstructive Pulmonary Disease, partially reversible airflow limitation is defined as post-bronchodilator administration forced expiratory volume in one
second (FEV1) lower than 80% of predicted value
and FEV1 as a percentage of forced vital capacity
(FEV1/FVC) lower than 70%( 1 5 ).
Patients were informed of the procedures proposed in the study and gave written informed consent. The Ethics Research Committee of the Faculdade de Medicina de Botucatu approved the study. All patients were submitted to a variety of tests and evaluations.
Nutritional evaluation
Using anthropometry, height and weight were measured and BMI was calculated
(weight/height2). For body composition analyses,
bioimpedance analyzer (BIA 101A /RJL systems, Detroit, MI, USA). Lean body mass was estimated in accordance with a model developed by Kyle et al.( 1 6 ): lean body mass = -6.06 + (height x 0.283) +
(weight x 0.207) — (resistance x 0.024) + [gender (male = 1, female = 0)] x 4.036.
Assessment of respiratory muscle strength
Maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) were measured in accordance with the method proposed by Black
& Hyatt( 1 7 ). Both MIP and MEP were measured
three times with a vacuum manometer and only the highest measurement was recorded for analysis. Values of MIP were obtained from residual volume, whereas MEP values were obtained from total lung capacity. Patients received verbal encouragement and second measurements were taken when there was a greater than 10% difference between one measurement and the next.
6-minute walk test
Patients were asked to walk at their fastest pace over a 30-meter course clearly marked in a corridor. Patients received verbal encouragement. Arterial oxygen saturation by pulse oximetry
(SpO2) was monitored throughout the test with a
Biox 3700 Ohmeda oximeter (Ohmeda, Boulder, CO, USA). The distance covered was measured in
meters. Heart rate and SpO2 were recorded prior to
and after the test, as were respiratory rate, arterial blood pressure (by sphygmomanometer) and Borg scale dyspnea index, which consists of a scale from 0 (insignificant effort) to 10 (exhaustive effort).
Quality of life
A validated version of the SGRQ was used( 1 8 ). It
comprises three domains: “symptom” score assesses discomfort caused by respiratory symptoms; “impact” score assesses the global impact on daily life and perceived well-being of patients; and “activity” score assesses changes in physical activities. “Total” scores were also quantified. Results were expressed as percentages. High scores indicate worse performance in each domain.
Hand-grip dynamometer measurements
Muscle strength in the arms was estimated by quantifying grip strength exerted by the
dominant hand, measured with a hand-grip dynamometer (TEC-60; Technical Products,
Clifton, NJ, USA). While sitting, patients extended
their dominant arm (shoulder flexion at 90° , forearm in neutral position) and gripped the dynamometer. The best of three trials was chosen for later analysis.
Quadriceps strength
A maximal repetition test was conducted. Patients were encouraged to attain maximal repetition in bench press. Three trials were allowed until a maximal repetition (in kg) was obtained for the muscle group in question. If this was not achieved after 3 trials, patients were allowed to repeat the test after resting for at least one day.
Pulmonary function and gas exchange
Pulmonary function tests included
determination of FEV1, FVC, and FEV1/FVC. A
computer-assisted system (model 1070; Medical Graphics, St. Paul, MN, USA) was used in
accordance with ATS guidelines( 1 9 ). Values of FEV
1
were expressed in liters, as percentage of FVC and as percentage of reference values. The objective of the tests was to categorize the patients as having the mild, moderate or severe form of the disease. Subjects were classified in accordance with the criteria recommended by the Global Initiative for
Chronic Obstructive Pulmonary Disease( 1 5 ). Blood
was collected in room air and blood gas exchange was determined with a blood gas analyzer (Stat Profile 5 Plus; Nova Biomedical, Waltham, MA, USA).
Peak expiratory flow
Peak expiratory flow (PEF) was determined in three tests performed with an Assess peak flow meter (Assess, HealthScan Products, Cedar Grove, NJ, USA). The highest value was chosen as quantifiably representative of the degree of airway obstruction.
Statistical analysis
RESULTS
Twenty-one patients diagnosed with moderate to severe COPD were studied. Basal patient characteristics are shown in Table 1. Results are summarized in Table 2.
The “Impact” domain was found to correlate
negatively and significantly with FEV1 (r = -0.68;
p = 0.004), FEV1/FVC (r = -0.61; p = 0.014) and
PEF (r = -0.53; p = 0.015). In addition, PEF and
FEV1 both correlated negatively with SGRQ “total”
score (r = -0.53; p = 0.015). Similarly, MIP and
SpO2 correlated negatively with the “Activity”
domain (r = -0.57; p = 0.007 and r = -0.52; p = 0.018, respectively). There were no significant correlations between any SGRQ domain and MEP
or arterial oxygen tension (PaO2).
Patient BMI correlated negatively and significantly with “Impact” domain (r = -0.64; p =
0.002), “Symptom” domain (r = -0.60; p = 0.005)
and “Total” score (r = -0.57; p = 0.009). There
was no correlation between the percentage of lean body mass and QOL indices.
The 6MWT results correlated negatively and significantly with the “Activity” domain (r =
-0.58; p = 0.007) and the “Impact” domain (r =
-0.63; p = 0.001). Neither hand-grip dynamometer
measurements nor quadriceps strength correlated with any SGRQ domain.
We used SGRQ domains as dependent variables in the analysis of multiple linear regression. We found the SGRQ “Total” score to be significantly
influenced by BMI (p = 0.024). In addition, the
“Impact” domain was significantly influenced by BMI and 6MWT (p = 0.009 and p = 0.010, respectively). Furthermore, the “Activity” domain was significantly influenced by 6MWT (p = .048), nd the “Symptom” domain was significantly
influenced by BMI (p = 0.002).
DISCUSSION
The SGRQ “Impact” domain correlated significantly with pulmonary function parameters
(FEV1; FEV1/FVC; PEF) and with BMI. The
“Activity” domain was influenced by MIP, 6MWT,
and SpO2. The “Symptom” domain correlated
significantly only with BMI. The “Total” score was
influenced by FEV1, PEF, and BMI. When SGRQ
domains were used as dependent variables in the analysis of multiple linear regression, only BMI significantly influenced “Symptom”, “Impact”, and “Total” score, whereas 6MWT significantly influenced “Activity” and “Impact”. Both BMI and 6MWT proved to be significant independent variables.
It is important to exercise caution when attempting to use spirometry data to predict QOL for COPD patients. It has been suggested in the
literature that FEV1 and FEV1/FVC correlate only
weakly with QOL indices( 6 ).
In the present study, FEV1, FEV1/FVC and PEF
were found to correlate negatively and significantly with the “Impact” domain and “Total” score. However, when the spirometry indices were submitted to multiple regression, none influenced any SGRQ components, confirming the supposition that disease severity
has little effect on QOL( 7 , 8 , 9 , 1 0 ).
Mahler et al.( 7 ) compared the impact of dyspnea
and pulmonary function on the QOL of 110
TABLE 1
Demographics, pulmonary function data and SGRQ domain values for the 21 patients studied
Mean Standard deviation
Age (years) 65 8
Gender M/F 17/4 –-
BMI (kg/m2) 25 5
SpO2 (%) 93 2
Symptoms (%) 52 17
Activity (%) 54 24
Impacts (%) 43 17
Total (%) 48 16
PaO2 (mmHg) 73 8
FEV1 (%) 46 15
FEV1/FVC (%) 46 11
S G R Q : S t . G e o r g e ’ s R e s p i r a t o r y Q u e s t i o n n a i r e ; B M I : b o d y m a s s i n d e x ; S p O2: a r t e r i a l o x y g e n s a t u r a t i o n b y p u l s e o x i m e t r y ; P a O2: a r t e r i a l
o x y g e n t e n s i o n ; F E V1: f o r c e d e x p i r a t o r y v o l u m e i n o n e s e c o n d ; F V C :
TABLE 2
Pearson’s linear correlations of SGRQ domains and “Total” score in relation to the independent variables evaluated in the 21 patients analyzed
SGRQ FEV1 FEV1/FVC PEF MIP BMI 6MWT SpO2
Impacts r = -0.68 r = -0.61 r = -0.53 –- r = -0.64 r = -0.63 –-
p = 0.00486 p = 0.0149 p = 0.0151 p = 0.00293 p = 0.00197
Activity –- –- –- r = -0.57 –- r = 0.58 r = -0.52
p = 0.00762 p = 0.0074 p = 0.0181
Symptoms –- –- –- –- r = -0.60 –- –-
p = 0.00587
Total r = -0.64 –- r = -0.477 –- r = -0.57 –- –-
p = 0.01 p = 0.0334 p = 0.00959
— No significant correlation
SGRQ: St. George’s Respiratory Questionnaire; FEV1: forced expiratory volume in one second; FVC: forced vital capacity; PEF: peak expiratory flow; MIP: maximal
inspiratory pressure; BMI: body mass index; 6MWT: six-minute walk test; SpO2: arterial oxygen saturation by pulse oximetry
patients with COPD. A generic instrument for assessing QOL, the Medical Outcomes Study 20-item short-form health survey (SF-20), and Mahler’s Baseline Dyspnea Index (BDI) were used. Using multiple regression, only BDI significantly
influenced QOL. Renwick & Connoly( 8 ) evaluated
the influence of FEV1 on QOL (as assessed by
SGRQ score) of 190 patients and reported
significant correlations between FEV1 and all
SGRQ components. However, when submitted to
multiple regression, the correlation between FEV1
and SGRQ was weak. Hajiro et al.( 9 ) categorized
dyspnea in 194 patients as mild, moderate or severe and compared the impact of dyspnea with that of disease severity (as defined by the ATS) on QOL as assessed by the Medical Outcomes Study 36-item short-form health survey (SF-36). They concluded that the degree of dyspnea is a more relevant determinant of QOL than is disease
severity. Hajiro et al.( 1 0 ) studied 218 patients
categorized as suffering from mild, moderate or severe COPD (as defined by ATS guidelines). The authors compared the influence of disease severity to that of dyspnea severity (defined by the Medical Research Council dyspnea scale) on QOL (as assessed by SGRQ score) and found
strong correlations between FEV1 and SGRQ only
in those patients diagnosed with the severe form of the disease. However, the authors also found that the dyspnea index correlated better with all
SGRQ components than did FEV1.
Tsukino et al.( 6 ) evaluated, among other
factors, the influence of the degree of airway obstruction on the QOL of COPD patients and
concluded that airflow limitation partially
determined COPD patient QOL. Prigatano et al.( 2 0 )
assessed 100 COPD patients using the Sickness
Impact Profile, and Ketelaars et al.( 2 1 ) employed
the SGRQ to assess 126 COPD patients. The
authors of both studies concluded that FEV1 is
one of the most important determinants of QOL among the factors evaluated, which included anxiety, depression and physical capacity.
There is evidence of a correlation between poor nutritional state and worsening of QOL in COPD patients, especially in those with
emphysema( 4 ). In our study, BMI was found to
correlated negatively with “Impact”, “Symptom”, and “Total” scores. However, we found no significant correlation between the percentage of lean body mass and any SGRQ category.
Shoup et al.( 2 2 ) studied the effects of body
weight, lean body mass (determined by dual-energy X-ray absorptiometry) and dyspnea (BDI) on the QOL (SGRQ score) of 50 COPD patients. The “Activity” and “Impact” domain scores, as well as the “Total” scores of patients with body weight below the norm (for their build, etc.) were significantly higher (worse) than those of patients with normal weight, whereas patients with body weight above the norm had higher “Impact” domain and “Total” scores. In addition, patients with a low lean mass index (lean
mass/height2) scored higher in all SGRQ
several variables, including body weight, on the QOL (as assessed by the Nottingham Health Profile and the Chronic Respiratory Questionnaire) of 132 COPD patients and concluded that the relative body weight of the subjects did not influence their QOL. They reported that the main determinants of QOL were airflow obstruction, diffusion capacity, age and life history of cigarette consumption. Yohannes
et al.( 4 ) stated that BMI had only a weak
influence on Breathing Problems Questionnaire scores and no influence on Chronic Respiratory Questionnaire scores.
The weak or nonexistent influence of nutritional state on the QOL of patients diagnosed with COPD may be due to methodological problems, such as the fact that the samples were small in relation to the great number of variables studied. In addition, determining which variables ideally characterize the nutritional state of subjects is problematic.
There was a significant negative correlation
between SpO2 and the SGRQ “Activity” domain.
This suggests that patients suffering from hypoxemia are less capable of performing
physical activities. However, when SpO2 values
were submitted to multiple linear regression, no significant correlation was found between this variable and the “Activity” domain.
Stavem et al.( 2 3 ) categorized 59 male and
female COPD patients into two groups: mild COPD and moderate to severe COPD. They
studied the correlation between PaO2 (measured
through radial artery puncture) and QOL. The authors used a modified version of the Respiratory Quality of Life Questionnaire (RQLQ; modified for COPD patients) as a specific instrument and used the SF-36 as a generic instrument. They reported that, in patients with moderate to severe COPD, there were significant
correlations found between PaO2 and four of the
five RQLQ components. However, in the same
group of patients, PaO2 was found to correlate
significantly with only one of the eight SF-36 domains in the same group. The authors
concluded that PaO2 is a moderate determinant
of QOL for COPD patients. In our study, we
found no significant correlation between PaO2
and any SGRQ domain.
The effect of oxygen therapy on the QOL of COPD patients is controversial. Okubadejo et al.( 2 4 ) made use of the SGRQ in order to evaluate
the influence of a 6-month course of oxygen therapy on the QOL of COPD patients and concluded that there was no improvement in QOL
altered PaO2 and QOL. However, Ferreira et al.( 2 5 )
evaluated the QOL of low-income patients diagnosed with COPD and concluded that those submitted to long-term oxygen therapy had significantly lower QOL (higher SGRQ scores) than did nonhypoxic patients. Further investigation of this subject is warranted.
In the present study, we found indications that exercise tolerance affects the QOL of patients with COPD. The finding that MIP and 6MWT correlate with “Activity” domain score suggests that these variables influence the daily
life of COPD patients. Mahler et al.( 7 ), using a
generic instrument (the SF-20) for assessing QOL found significant correlation between MIP and the physical activity component. Ketelaars et al.( 2 1 ) also found significant negative correlations
between MIP and the SGRQ “Activity” and “Impact” domain scores. Unlike Ketelaars et al.( 2 1 ), showed a correlation between MIP and
“Impact” domain score (a finding unconfirmed in our study) but (as in our study) reported no influence of MIP on the SGRQ when MIP was submitted to multiple regression.
We found that greater distances walked during the 6MWT had a positive influence on “Activity” and “Impact” domain scores, and we confirmed that influence through multiple linear regression. Significant correlations between exercise tolerance and QOL indices in COPD
patients have been previously reported( 7 , 1 0 , 2 0 , 2 1 ).
Ketelaars et al.( 2 1 ) reported significant
negative correlations between the 12-minute walk test and the “Activity” and “Impact” domain scores, a finding which was, as in our study, confirmed by multiple regression. When Hajiro et al.( 1 0 ) studied factors determining the SGRQ
“Total” score of COPD patients categorized according to disease severity, they concluded that maximal oxygen uptake influenced “Total” score only in patients with the mild form of the disease. Patients with severe COPD are usually older, and exercise intolerance can, in part, be associated with age.
Better performance on the 6MWT may indicate less difficulty in performing daily physical activities and, consequently, lower impact of the disease. Moreover, 6MWT may be an important clinical indicator of functional capacity. Distance walked during the 6MWT seems to be one of the factors that influence the QOL of COPD patients, although the extent of this relationship is still unclear.
rehabilitation. This is probably due to the fact that, although both 6MWT and QOL indices improve, the beneficial effects of pulmonary rehabilitation on QOL are related to global
aspects and not to isolated factors( 2 6 , 2 7 ).
Some limitations, such as the sample size and the lack of evaluation of dyspnea sensation, may have influenced the results in the present study. The influence of dyspnea on the QOL of COPD
patients has been previously reported( 7 , 9 , 1 0 , 2 2 ).
These authors found that BMI and 6MWT were the factors exerting the most influence over the QOL of COPD patients selected for pulmonary rehabilitation. Although these factors may not be directly predictive of QOL, improved nutritional state, greater functional capacity and increased exercise tolerance may be conducive to an improved QOL for such patients, since their pulmonary function can only be partially enhanced.
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S t a g e s o f d i s e a s e s e v e r i t y a n d f a c t o r s t h a t a f f e c t t h e h e a l t h s t a tu s o f p a t i e n t s w i t h c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e . R e s p i r M e d . 2 0 0 0 ; 9 4 : 8 4 1 - 6 .
1 1 . J o nes P W. Hea l th s ta tus mea s ur e me nt i n c h r o ni c
o b s t r u c t i v e p u l m o n a r y d i s e a s e . T h o r a x . 2 0 0 1 ; 5 6 : 8 8 0 - 7 .
1 2 . B e r n a r d S , W h i t t o m F , L e b l a n c P , J o b i n J , B e l l e a u R , B é r u b é C , e t a l . A e r o b i c a n d s t r e n g t h t r a i n i n g i n p a t i e n t s w i t h c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e . A m J R e s p i r C r i t C a r e M e d . 1 9 9 9 ; 1 5 9 : 8 9 6 - 9 0 1 .
1 3 . R i e r a H , R u b i o T , R u i z F , R a m o s P , D e l C a s t i l l o O t e r o D , Her na nd e z T , e t a l . I ns p i r a to r y mus c l e tr a i ni ng i n pa tients with COP D : effect on dyspnea , ex ercise p e r f o r m a n c e , a n d q u a l i t y o f l i f e . C h e s t . 2 0 0 1 ; 1 2 0 : 7 4 8 -5 6 .
1 4 . C o o p e r C B . E x e r c i s e i n c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e : a e r o b i c e x e r c i s e p r e s c r i p t i o n. M e d S c i S p o r t s E x e r c . 2 0 0 1 ; 3 3 : S 6 7 1 - 9 .
1 5 . I n i c i a t i v a g l o b a l p a r a a d o e n ç a p u l m o n a r o b s t r u t i v a c r ôni c a . E s t r a t é g i a g l o b a l p a r a o d i a g n ó s t i c o , a c o n d u t a e a p r e v e n ç ão d a d o e n ç a p u l m o n a r o b s t r u t i v a c r ôni c a . R e l a t ó r i o d o p a i n e l d e e s t u d o s d o N H L B I / O M S . P r o j e t o I m p l e m e n t a ç ão G O L D B r a s i l . R e s u m o E x e c u t i v o ; 1 9 9 8 . 1 6 . K y l e U G , P i c h a r d C , R o c h a t T , Slosma n DO, F i tting J -W, T h i e b a l d D . N e w b i o e l e c t r i c a l i m p e d a n c e f o r m u l a f o r p a t i e nt s w i t h r e s p ir a to r y i nsuf f ic ie nc y : c o mpa r i s on to d u a l - e n e r g y X - r a y a b s o r p t i o m e t r y . E u r R e s p i r J . 1 9 9 8 ; 1 2 : 9 6 0 - 6 .
1 7 . B l a c k L F , Hya tt R E . M a x i ma l r e s p i r a to r y p r e s s ur e s : no r ma l v a l ue s a nd r e l a ti o ns h i p to a g e a nd S e x . A m R e v R e s p D i s . 1 9 6 9 ; 9 9 : 6 9 7 - 0 1 .
1 8 . S o u z a T C , J a r d i m J R , J o n e s P . V a l i d a ç ão d o q u e s t i o n ár i o d o H o s p i t a l S a i n t G e o r g e n a d o e n ç a r e s p i r a t ó r i a ( S G R Q ) e m p a c i e n t e s p o r t a d o r e s d e d o e n ç a p u l m o n a r o b s t r u t i v a c r ôni c a n o B r a s i l . J P n e u m o l . 2 0 0 0 ; 2 6 : 1 1 9 - 2 5 .
1 9 . A m e r i c a n T h o r a c i c S o c i e t y . S ta nd a r d s fo r d i a g no s i s a nd c a r e o f p a t i e n t s w i t h c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e . A m J R e s p i r C r i t C a r e M e d . 1 9 9 5 ; 1 5 2 : S 7 7 - S 1 2 1 . 2 0 . P r i g a t a n o G P , W r i g h t E C , L e v i n D . Q u a l i t y o f l i f e a n d
i t s p r e d i c t o r s i n p a t i e n t s w i t h m i l d h y p o x e m i a a n d c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e . A r c h I n t e r n M e d . 1 9 8 4 ; 1 4 4 : 1 6 1 3 - 9 .
2 1 . K e t e l a a r s C A J , S c h l o s s e r M A G , M o s t e r t R , A b u - S a a d H H , Ha l fe ns R J G , Wo ute r s , E F M . D e ter mi na nts o f h e a l th -r e l a t e d q u a l i t y o f l i f e i n p a t i e n t s w i t h c h -r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e . T h o r a x . 1 9 9 6 ; 5 1 : 3 9 - 4 3 . 2 2 . S h o u p R , D a l s k y G , W a r n e r S , D a v i s M , C o n n o r s M , K h a n
M , e t a l . B o d y c o m p o s i t i o n a n d h e a l t h - r e l a t e d q u a l i t y o f l if e in pa t i e nt s w it h ob s t r uc t i v e a i r w a ys d i s e a se . E ur R e s p i r J . 1 9 9 7 ; 1 0 : 1 5 7 6 - 8 0 .
2 3 . S t a v e m K , E r i k s s e n J , B o e J . H e a l t h - r e l a t e d q u a l i t y o f l i fe i s a s s o c i a te d w i th a r ter i a l P O2 i n c h r o ni c
o b s t r u c t i v e p u l m o n a r y d i s e a s e . R e s p i r M e d . 2 0 0 0 ; 9 4 : 7 7 2 - 7 .
2 4 . O k u b a d e j o A A , P a u l E A , J o n e s P W , W e d z i c h a J A . D o e s l o n g - t e r m o x y g e n t h e r a p y a f f e c t q u a l i t y o f l i f e i n p a t i e n t s w i t h c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e a n d s e v e r e h y p o x a e m i a . E u r R e s p i r J . 1 9 9 6 ; 9 : 2 3 3 5 - 9 . 2 5 . F e r r e i r a C A S , S t e l ma c h R , F e l t r i n M I Z, J a c o b - F i l h o W,
C h i b a T , C uk i e r A . E v a l ua ti o n o f h e a l th -r e l a te d q ua l i ty o f l i f e i n l o w - i n c o m e p a t i e n t s w i t h C O P D r e c e i v i n g
long-term oxygen therapy. Chest. 2 0 0 3 ; 1 2 3 : 1 3 6 - 4 1 .
2 6 . Wi j k str a P J , V a n A l tena R , K r a a n J , O tten V , P o stma D S , K o è t e r G H . Q u a l i t y o f l i f e i n p a t i e n t s w i t h c h r o n i c o b s t r u c t i v e p u l m o n a r y d i s e a s e i m p r o v e s a f t e r r e h a b i l i t a t i o n a t h o m e . E u r R e s p i r J . 1 9 9 3 ; 7 : 2 6 9 - 7 3 . 2 7 . F u c h s - C l i m e n t D , L e G a l l a i s D , V a r r a y A , D e s p l a n J ,
