Pulmonary function tests, respiratory muscle strength, and endurance of patients with osteoporosis. (Original Article).

Background: It has been shown that patients with thoracic kyphosis due to osteoporosis have diminished pulmonary function. The aim of this study was to determine the pulmonary function, respiratory muscle strength, and endurance of patients with osteoporosis who did not have compression fractures.

Methods: The patient group consisted of 88 recently diagnosed postmenopausal osteoporotic women without spinal fractures. They were matched for age and body mass index with 54 healthy women, who formed the control group. Bone mineral density, pulmonary function test (PFT), maximum voluntary ventilation (MVV), maximal inspiratory pressure (MIP), and maximal expiratory pressure (MEP) measurements of both groups were performed.

Results: There were no significant differences between the two groups regarding PFT parameters and MIP and MEP. However, osteoporotic patients had significantly lower MVV values.

Conclusion: Women with postmenopausal osteoporosis without spinal compression fractures have normal PFT, MIP, and MEP values, but they have reduced respiratory muscle endurance.

Key Words: maximum expiratory pressure, maximum inspiratory pressure, osteoporosis, pulmonary function tests, respiratory muscle evaluation

**********

Key Points

* Vertebral deformity in spinal osteoporosis results in spinal and thoracic deformity, causing pain, disability, and an overall decrease in quality of life.

* The alteration of the musculoskeletal system due to osteoporosis affects the thoracic cage as a whole and may cause imbalanced functioning of respiratory muscles as well.

* Pulmonary function tests and maximal inspiratory and expiratory pressure measurements are not affected in early stages of osteoporosis and are diminished after osteoporosis advances and thoracic compression fractures occur.

* Patients with osteoporosis have lower respiratory muscle endurance even if they have no vertebral fractures.

Osteoporosis is defined as a systemic skeletal disease characterized by decreased bone mass and microarchitectural deterioration of bone tissue, with a consequent increase in bone fragility and susceptibility to fracture risk. (1) Vertebral deformity in spinal osteoporosis results in spinal and thoracic deformity, causing pain, disability, and an overall decrease in quality of life. (2) The alteration of the musculoskeletal system due to osteoporosis affects the thoracic cage as a whole and may cause imbalanced functioning of respiratory muscles as well. (2) It has been previously shown that pulmonary function is significantly diminished in patients with osteoporotic spinal fractures and thoracic kyphosis, (2,3) but there are few data about the respiratory function of osteoporotic patients without compression fractures. The aim of this study was to investigate the pulmonary function tests (PFTs), respiratory muscle strength, and endurance of women with postmenopausal osteoporosis but without any osteoporotic thoracic or lumbar spinal compression fractures. We also aimed to determine the relationship between PFT, respiratory muscle strength, endurance, and bone mineral density (BMD).

Patients and Methods

Eighty-eight patients admitted to our outpatient physical medicine and rehabilitation clinic were included in this study. All patients were recently diagnosed with osteoporosis according to the World Health Organization osteoporosis diagnosis criteria. (4) None of the patients were taking any medication for osteoporosis, and none of them had any spinal compression fractures. Fifty-four healthy volunteer women without any evidence of osteoporosis formed the control group. All patients and control subjects underwent a standardized interview regarding their medical history. To rule out other causes of muscle dysfunction, potential participants in both the patient and control groups were excluded from the study if they had secondary osteoporosis, a known history of primary pulmonary disease (pulmonary fibrosis, emphysema, bronchial asthma, cardiothoracic surgery, chronic bronchitis), cardiac disease, diabetes mellitus, thyroid function disorders, inflammatory diseases, or neurologic disorders. None of the patien ts or control subjects had engaged in a regular exercise program in the preceding 6 months. As part of the study protocol, women in both groups underwent detailed clinical examinations, and complete blood cell counts, routine biochemical tests, erythrocyte sedimentation rates, C-reactive protein levels and electrocardiograms (ECGs) were obtained to ensure that there were no contraindications to study participation.

Anteroposterior and lateral x-rays of the thoracic and lumbar spine were evaluated to determine the presence of any compression fractures. Measurements of BMD at the lumbar spine and femur were performed using dual-energy x-ray absorptiometry (DXA) (QDR 4500; Hologic Inc., Bedford, MA). Pulmonary function tests were performed using a computerized spirometer (Vmax 22; Sensor Medics, Yorba Linda, CA). Vital capacity (VC), forced expiratory volume during the first second ([FEV.sub.1]), [FEV.sub.1]/forced vital capacity (FVC), maximal midexpiratory flow rate ([FEF.sub.25-75%]), and maximum voluntary ventilation (MVV) were recorded. The values were expressed as percentages of the predicted normal values, according to European Respiratory Society (ERS) criteria. (5) Acceptable recordings were obtained from each maneuver, and the highest values were used for further analyses. (6,7)

The maximum respiratory pressures were obtained using a digital mouth pressure meter (MPM; Sensor Medics). The maximum inspiratory pressure (MIP) was measured with the subject sitting in a chair and inhaling through a mouthpiece connected to the digital meter, just after clamping the nose. The maximum expiratory pressure (MEP) was measured following end-inspiration by the same procedure. Both measurements were taken three times, and mean values were calculated as MIP and MEP (in cm [H.sub.2]O). (8) Chest expansion was measured (in cm) with a tape measure placed circumferentially around the chest wall at the fourth intercostal space. (9) All subjects were given information about the study before the measurements were taken.

Statistical evaluations were assessed using SPSS for Windows 6.0 (SPSS Inc., Chicago, IL). An independent-samples t test was used for intergroup comparisons. Values were correlated using Pearson correlation analysis.

Results

There were no significant differences between the patients and the control group regarding age and body mass index (BMI). Patients had significantly lower lumbar and total femur BMD values than the controls (P < 0.001 for both femur and lumbar spine BMD). Their lumbar spine and femur T-scores were significantly lower than those of the control group (P < 0.001 for both femur and lumbar spine T-scores). When the PFT values were compared, no statistically significant differences were found in VC, [FEV.sub.1], [FEV.sub.1]/FVC, or [FEF.sub.25-75%]. We found no significant differences between groups regarding MIP and MEP values (Table 1). Osteoporotic patients had significantly lower MVV values compared with controls (P < 0.025) (Fig. 1). No significant difference was determined in arm-span measurement values between groups. We found no correlation between PFT values and lumbar BMD, total femur BMD, lumbar spine T-scores, and total femur T-scores. MEP was correlated with femur T-score (P < 0.052; r = 0.22). Chest e xpansion was correlated with both MIP (P < 0.001; r = 0.37) and MEP (P < 0.001; r = 0.36). MVV was also correlated with both MIP (P < 0.00 1; r 0.45) and MEP (P < 0.001; r = 0.53).

Discussion

Our study revealed that pulmonary function is not reduced in postmenopausal osteoporotic women who have no spinal compression fractures, compared with age-matched women without osteoporosis. The respiratory muscle strength of women with osteoporosis, which was measured as MIP and MEP, did not show any significant difference compared with controls. Respiratory muscle strength of patients with thoracic kyphosis due to osteoporosis was investigated previously by Leech et al. (10) Their estimation of MIP was between 41 and 54 cm [H.sub.2]O, and MEP was between 44 and 47 cm [H.sub.2]0/ Patients with osteoporosis have reduced isometric muscle strength (measured by hand-grip strength) and reduced quadriceps and hamstring muscle strength (measured with dynamometers). (11) We did not find any report of respiratory muscle strength of patients with osteoporosis without spinal fractures.

Pulmonary function of osteoporotic women has been investigated previously. (2,3,10) Schlaich et al (2) measured the VC and [FEV.sub.1] values in a group of patients with advanced osteoporosis and reported that they had reduced VC compared with patients without any evidence of osteoporosis. Culham et al (3) showed that VC, inspiratory capacity, and total lung volume of women with osteoporosis were lower than those of healthy controls. Leech et al (10) observed that kyphosis and thoracic compression fractures produce a decline in VC in women with osteoporosis. However, those are studies of older osteoporotic women with thoracic kyphosis. In this study, we investigated both the respiratory muscle strength and endurance of osteoporotic women as well as PFTs of osteoporotic women without spinal fractures. We wanted to determine the reasons for respiratory system decline other than kyphosis, which produces restrictive pulmonary involvement. For that reason, we measured [FEF.sub.25-75%] to detect modest levels of ai rway obstruction.

Vertebral deformities cause pain, disability, or loss of height only if vertebral ratios fall 4 standard deviations below normal. Therefore, the condition may be advanced by the time the patient is admitted to the clinic.

Compared with the control subjects, our patients with osteoporosis had significantly lower MVV values, which reflect the respiratory muscle endurance. The reduced respiratory muscle endurance of osteoporotic patients could be due to their inactivity, but the age-matched, nonosteoporotic control subjects were also matched for exercise condition to the patients with osteoporosis. Therefore, it would seem that there must be some other factors that reduce the respiratory muscle endurance in patients with osteoporosis. The rhythmic action of the respiratory pump is controlled by an automatic system involving complex anatomic, biochemical, and physiologic reflexes. The diaphragm, intercostal, scalene, sternocleidomastoid, and other accessory muscles (eg, the pectoralis major, latissimus dorsi, serratus anterior, and abdominal muscles) form the muscular part of this pump. (12,13) Some of the respiratory muscles take part in other physiologic activities as well, such as maintenance of posture.

A test of endurance includes more dynamic factors than a test of strength. The lack of cardiopulmonary fitness in patients with osteoporosis may have caused reduced respiratory muscle endurance in our patient population. While their MVV values were lower than those of the control subjects, the mean values of osteoporotic patients were close to normal standards. The setting of this study was not suitable for a cardiopulmonary exercise test to determine the cardiorespiratory fitness and responses. Since the PET values of the osteoporosis group were normal, we could not determine any correlation between PET and BMD parameters.

Conclusion

We can say that PFTs and MIP and MEP measurements are not affected in early stages of osteoporosis. They are diminished after osteoporosis advances and thoracic compression fractures occur. Patients with osteoporosis have lower respiratory muscle endurance, however, even if they have no vertebral fractures. Further studies are needed to investigate the exercise test parameters, aerobic capacity, and their relationship with respiratory muscles and BMD values.

[FIGURE 1 OMITTED]

Table 1

Comparison of parameters in osteoporosis and control group

                             Patient                Control
Parameter                   (n = 88)               (n = 54)

Age                    56.27 [+ or -] 10.97   53.44 [+ or -] 7.09
BMI                    28.27 [+ or -] 6.14    29.96 [+ or -] 4.55
Lomber BMD              0.81 [+ or -] 0.11     1.09 [+ or -] 0.12
Lomber T               -2.85 [+ or -] 0.83    -0.06 [+ or -] 1.05
Femur BMD               0.76 [+ or -] 0.11     0.90 [+ or -] 0.09
Femur T                -1.82 [+ or -] 0.89    -0.17 [+ or -] 0.71
MEP                    81.52 [+ or -] 14.34   83.13 [+ or -] 18.19
MIP                    63.01 [+ or -] 14.44   65.93 [+ or -] 15.08
Chest expansion (cm)    3.41 [+ or -] 1.03     3.10 [+ or -] 0.79
Arm span (cm)         158.32 [+ or -] 7.27   160.60 [+ or -] 5.44
FVC (%)               103.37 [+ or -] 13.95  106.52 [+ or -] 16.95
[FEV.sub.1] (%)        95.63 [+ or -] 12.59   97.84 [+ or -] 15.80
[FEV.sub.1]/FVC (%)    78.26 [+ or -] 5.78    77.23 [+ or -] 6.09
[FEF.sub.25-75%] (%)   69.06 [+ or -] 19.05   66.36 [+ or -] 22.87
MVV (%)                83.35 [+ or -] 19.14   74.74 [+ or -] 21.77


Parameter               P

Age                     NS
BMI                     NS
Lomber BMD            <0.001
Lomber T              <0.001
Femur BMD             <0.001
Femur T               <0.001
MEP                     NS
MIP                     NS
Chest expansion (cm)    NS
Arm span (cm)           NS
FVC (%)                 NS
[FEV.sub.1] (%)         NS
[FEV.sub.1]/FVC (%)     NS
[FEF.sub.25-75%] (%)    NS
MVV (%)               <0.025

NS, not significant.

BMI, body mass index; BMD, bone mineral density; MEP, maximum epiratory
pressure; MIP, maximum inspiratory pressure; FVC, forced vital capacity;
[FEV.sub.1], forced expiratory volume during the first second;
[FEF.sub.25-75%] maximal midexpiratory flow rate; MVV, maximal voluntary
ventilation.

Accepted February 8, 2002.

References

(1.) Kanis JA. Osteoporosis and its consequences, in Osteoporosis. Oxford, Blackwell Science, 1994, pp 1-21.

(2.) Schlaich C, Minne HW, Bruckner T, Wagner G, Gebest HJ, Grunze M, et at. Reduced pulmonary function in patients with spinal osteoporotic fractures. Osteoporos Int 1998;8:261-267.

(3.) Culham EG, Jimenez HA, King CE. Thoracic kyphosis, rib mobility, and lung volumes in normal women and women with osteoporosis. Spine 1994;19:1250-1255.

(4.) World Health Organization. Assessment of Fracture Risk and Its Application to Screening for Postmenopausal Osteoporosis (WHO Technical Report Series). Geneva, World Health Organization, 1994.

(5.) Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC. Lung volumes and forced ventilatory flows: Report of the Working Party Standardization of Lung Function Tests, European Community for Steel and Coal--Official Statement of the European Respiratory Society. Eur Respir J Suppl 1993;16:5-40.

(6.) Ries AL. Measurement of lung volumes. Clin Chest Med 1989;10:177-186.

(7.) Gardner RM, Crapo RO, Nelson SB. Spirometry and flow-volume curves. Clin Chest Med 1989;10:145-154.

(8.) Rochester DF. Test of respiratory muscle function. Clin Chest Med 1988;9:249-261.

(9.) Fisher LR, Cawley MI, Holgate ST. Relation between chest expansion, pulmonary function, and exercise tolerance in patients with ankylosing spondylitis. Ann Rheurn Dis 1990;49:921-925.

(10.) Leech JA, Dulbcrg C, Kellie S, Pattee L, Gay J. Relationship of lung function to severity of osteoporosis in women. Am Rev Respir Dis 1990;141:68-71.

(11.) Kerschan K, Alacamlioglu Y, Kollmitzer J, Wober C, Kaider A, Hartard M, et al. Functional impact of unvarying exercise program in women after menopause. Am .IPhys Med Rehabil 1998;77:326-332.

(12.) Celli BR. Clinical and physiologic evaluation of respiratory muscle function. C/in Chest Med 1989;l0:199-213.

(13.) Guyton AC. Pulmonary ventilation, in Guyton AC, Hall JE (eds): Textbook of Medical Physiology. Philadelphia, W.B. Saunders Co., 2000, ed 10, pp 432-443.

From the Department of Physical Medicine and Rehabilitation and the Department of Chest Disease, University of Mersin Faculty of Medicine, Mersin, Turkey.

Reprint requests to Ozlem Bolgen Cimen, MD, Mersin Universitesi Tip Fakultesi, FTR Anabilim Dali, 33070 Mersin, Turkey.

Copyright [c] 2003 by The Southern Medical Association

0038-4348/03/9605-0423