Lung Function Impairment, Associating Hyperinflation with Impaired Diffusion Capacity and Transfer Coefficient, Is a Risk Factor for Hip Osteoporosis in Patients with Chronic Obstructive Pulmonary Disease
by
, , ,
Olivier Malaise
1,*
,
Cécile André
1,
Caroline Van Durme
2,3,
Laurence Seidel
4,
Florence Schleich
5,
Renaud Louis
5,
Michel Malaise
1 and
Clio Ribbens
1 1
Department of Rheumatology, University Hospital of Liège, 4000 Liège, Belgium
2
Department of Physical Medicine and Rheumatology, Centre Hospitalier Chrétien, 4000 Liège, Belgium
3
Department of Internal Medicine, Maastricht University Medical Centre, 6229 Maastricht, The Netherlands
4
Biostatistics and Research Method Center, ULiège and University Hospital of Liège, 4000 Liège, Belgium
5
Department of Respiratory Medicine, University Hospital of Liège, 4000 Liège, Belgium
*
Author to whom correspondence should be addressed.
J. Clin. Med. 2023, 12(6), 2383; https://doi.org/10.3390/jcm12062383
Submission received: 1 February 2023
/
Revised: 27 February 2023
/
Accepted: 15 March 2023
/
Published: 20 March 2023
(This article belongs to the Special Issue Update in Osteoporosis and Related Bone Metabolic Disease)
Abstract
:Chronic obstructive pulmonary disease (COPD) is a risk factor for osteoporosis. Our objective is to determine if functional indices associated with emphysema on pulmonary function tests (DLCO—diffusion capacity of the lung for CO-; DLCO/AV—DLCO corrected for alveolar volume- and TLC—total lung capacity), considered alone or together, can identify COPD patients with osteoporosis. Methods: 90 COPD patients underwent dual-energy X-ray absorptiometry (DEXA) and pulmonary function tests. Results: 26% of the COPD patients were osteoporotic. In univariate analysis, each functional parameter associated with emphysema, analyzed separately, was not associated with osteoporosis. In contrast, patients with hyperinflation associated with impaired diffusion capacity and transfer coefficient, defined by the association of the three functional indices (DLCO < 70%, DLCO/AV < 80% and CPT > 115%), had significantly more osteoporosis at the total hip (OR: 5.9, CI: 1.5–23.8, p = 0.013). In multivariate analysis, this phenotype was confirmed as an independent factor associated with hip osteoporosis. In contrast, COPD airway obstruction severity, based on FEV1 (%), was not associated with osteoporosis. A lower BMI, female gender and age were also identified as osteoporosis risk factors. Conclusions: COPD patients with hyperinflation associated with impaired diffusion capacity and transfer coefficient are at higher risk for osteoporosis. Pulmonary function tests associated with emphysema detection can help to identify COPD patients with osteoporosis, in addition to the classical risk factors.
1. Introduction
Chronic obstructive pulmonary disease (COPD) is a heterogeneous lung condition characterized by chronic respiratory symptoms (dyspnea, cough, sputum production, exacerbations) due to abnormalities of the airway (bronchitis, bronchiolitis) and/or alveoli (emphysema) that cause persistent, often progressive, airflow obstruction [1]. COPD is also characterized by systemic inflammation and extra-pulmonary manifestations, such as osteoporosis [2]. As in the general population, osteoporosis is linked with mortality and morbidity in COPD patients: lower T-scores are associated with a 5% increase in mortality [3], fractures are linked with higher mortality [4] and retrospective analysis of our local COPD cohort identifies osteoporosis as a mortality risk factor among patients receiving long-term oxygen therapy [5]. Morbidity is increased with higher hospitalization rates [4] and a decline in lung function is associated with vertebral fractures [6,7]. Despite these data, osteoporosis detection is still an unmet problem and studies confirm that the rate of COPD patients treated for osteoporosis is low with regard to osteoporosis prevalence [8,9].
It is well established that osteoporosis prevalence is higher in COPD patients than in the healthy population [10], and numerous risks factors of osteoporosis are found in patients with COPD: aging, smoking, physical inactivity, systemic inflammation, malnutrition, low body-mass index (BMI), corticosteroids … [10,11]. COPD patients are heterogenous and have different phenotypes (emphysema, chronic bronchitis, frequent exacerbator …), with variations in terms of demographics, disease characteristics and health outcomes [12]. The emphysema phenotype is described to be associated with more dyspnea [13], more exacerbation [14] and more disease progression [2]. Several studies indicate that CT quantification of emphysema [15,16,17,18] is associated with low bone mineral density (BMD) or osteoporosis, but there is no reliable information about the functional characteristics associated with emphysema based on functional respiratory tests.
Our objective is to analyze whether a higher probability of osteoporosis is found in COPD patients who exhibit functional respiratory tests parameters that reflect emphysema (DLCO -diffusion capacity of the lung for CO- <70%; DLCO/AV -DLCO corrected for alveolar volume- <70%; and TLC -total lung capacity- >115%). We also evaluated the hypothesis that a combination of these three functional parameters could help to identify COPD patients with osteoporosis.
2. Materials and Methods
2.1. Subjects
Ninety consecutive ambulatory COPD patients were evaluated by dual-energy X-ray absorptiometry (DEXA) and pulmonary function tests. The diagnosis of COPD had to be established by a respiratory physician and patients had to be followed in pneumology consultation.
2.2. Measurements
All subjects filed a questionnaire about their smoking habits, alcohol consumption, fracture history and use of corticosteroids (current or previous use, systemic and/or inhaled). All bone examinations were performed by the same Discovery A DEXA system (Hologic®, Bedford, MA, USA), with lumbar spine (L1–L4) and left total hip and femoral neck analysis. T-score values were considered osteoporotic if ≤−2.5. Standardization procedures were performed according to the International Society for Clinical Densitometry. In particular, quality controls with phantom were performed daily to ensure that these values were located at a maximum of ±1.5% of the mean value of calibration. The total bone mineral density (BMD) coefficient of variation (CV) of the DEXA (Hologic®, Bedford, MA, USA) = 1.0%.
The same day, patients underwent functional respiratory tests with spirometric measurements, lung volume and lung diffusion analysis: FEV1 (fraction of expired volume in 1 s) (%) stratification for COPD severity (mild if >80%; moderate if ≥50 and ≤80; severe if ≥30 and <50; and very severe if <30); DLCO (diffusion capacity of the lung for CO); DLCO/AV (DLCO corrected for alveolar volume); and TLC (total lung capacity) for parameters associated with functional emphysematous. DLCO, DLCO/AV and TLC were considered pathological if <70%, <80% or >115%, respectively.
Approval was submitted to the local ethical committee of the University Hospital of Liège but was not mandatory because all examinations performed (functional respiratory test and DEXA) were part of the standard of care of COPD management. All procedures performed in studies involving human participants were undertaken in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
2.3. Statistical Analysis
Results are presented as mean ± standard deviation (SD) or as median (minimum–maximum) for continuous variables and as frequency tables for qualitative variables. Univariate logistic regression models investigated the relationship between osteoporosis risk and demographic/respiratory variables (odds ratio ± 95% confidence interval). Multivariate logistic regression model (including the following variables: gender, age, BMI, corticosteroids (chronic use), corticosteroids history of use, active smoking, FEV1 and association of DLCO < 70%, DLCO/AV < 80% and TLC > 115%) was applied on these factors Results were considered significant at the uncertainty level of 5% (p < 0.05). Calculations were performed using SAS software version 9.4 (SAS Institute, Cary, NC, USA).
3. Results
3.1. Demographics
Ninety COPD patients were included (Table 1). Of these, 62.2% were male, with a mean (±SD) age of 63.4 (±10.1) years and a mean BMI of 24.1 (±5.2) kg/m2. Forty (44%) were active smokers. In total, 68.9% had a chronic use of corticosteroids: 62.2% had only chronic inhaled treatment and 6.7% also received more than 2 systemic courses per year. Finally, 71.1% had a history of glucocorticoid use as defined by the FRAX (current or previous treatment for >3 months at a prednisone dose ≥5 mg/day).
3.2. DEXA Results and Pulmonary Function Tests
Osteoporosis in at least one of the three sites was identified in 23 patients (25.6%). At each anatomical location, osteoporosis rates were as follows: 15.6% at lumbar spine, 15.7% at femoral neck and 13.5% at total hip. BMD and T-scores are shown in Table 2. COPD patients were characterized by pulmonary function tests (Supplementary Data: Table S1). For lung functional parameters associated with emphysema (DLCO, DLCO/AV and TLC), each parameter was first considered separately. We also decided to consider the association of these three functional parameters and created a sub-group of patients (20/80, 25%) exhibiting “DLCO < 70%, DLCO/AV < 80% and TLC > 115%”. Of these patients, seven (35.0%) had global osteoporosis. At the subtype level, four (20.0%) had L1L4 osteoporosis, four (20.0%) had femoral neck osteoporosis and six (30.0%) had total hip osteoporosis.
3.3. Osteoporosis Risk Factors: Univariate Analyses
In univariate analysis, the severity of airway obstruction (FEV1) was not associated with osteoporosis diagnosis (Table 3). While each functional parameter associated with emphysema (DLCO, DLCO/AV, TLC), taken separately, was not associated with a diagnosis of osteoporosis, patients that had associated hyperinflation with impaired diffusion capacity and transfer coefficient (DLCO < 70%, DLCO/AV < 80% and TLC > 115%) were more likely to exhibit total hip osteoporosis, with an OR of 5.89 (IC95%: 1.46–23.77, p = 0.013). No significant association was observed for the lumbar spine or the femoral neck. A higher BMI was less likely to be associated with osteoporosis at all the sites analyzed (OR:0.74, 0.61–0.89, p = 0.002; OR:0.82, 0.70–0.96, p = 0.016; OR:0.66, 0.51–0.84, p = 0.0007 for lumbar spine, femoral neck and total hip, respectively), while active smoking was more likely to be associated with osteoporosis (OR:5.94, 1.52–23.11, p = 0.01; OR:3.97, 1.14–13.83, p = 0.031 for lumbar spine and femoral neck, respectively). Association with glucocorticoid use was restricted to total hip osteoporosis.
3.4. Osteoporosis Risk Factors: Multivariate Analyses
The multivariate analysis for osteoporosis risk included eight variables: gender, age, BMI, chronic use of corticosteroids, history of corticosteroids use, active smoking, FEV1 and association of “DLCO < 70%, DLCO/AV < 80% and TLC > 115%” (Table 4). COPD severity (FEV1) was not associated with osteoporosis. Hyperinflation with impaired diffusion capacity and transfer coefficient remained a significant risk factor for total hip osteoporosis: patients that associated DLCO < 70%, DLCO/AV < 80% and TLC > 115% were more likely to exhibit total hip osteoporosis (OR, IC95%: 12.1, 1.1–138.8, p = 0.045). A higher BMI was more likely to be associated with less lumbar spine and total hip osteoporosis, while male gender was also less likely to be associated with osteoporosis at the femoral neck and total hip. A higher age was linked with total hip osteoporosis.
4. Discussion
In this study, we analyzed the association between functional lung parameters and bone mineral density in COPD patients. When we considered separately the functional parameters associated with emphysema (DLCO, DLCO/AV or TLC), none of these three factors was associated with osteoporosis. However, hyperinflation with impaired diffusion capacity and transfer coefficient (the association of DLCO < 70%, DLCO/VA < 80% and TLC > 115%) was as an independent risk factor for hip osteoporosis, even after adjustment for clinical and spirometric factors.
The influence of pulmonary emphysema on bone metabolism had already been analyzed in previous studies. In four different studies [15,16,17,18], authors found a link between pulmonary emphysema and low BMD, but pulmonary emphysema was assessed by chest CT, which is less accessible than functional respiratory tests and not routinely repeated in daily clinics. Ohara et al. have confirmed that this association was independent of BMI and FEV1 [18]. All these studies were based on CT data and supported the “holes in the lung, holes in the bone” theory. None of these studies analyzed the emphysematous parameters using functional respiratory tests. There are a few exceptions, with Fouda et al. in 2017, who also made functional respiratory tests to determine emphysematous patients among 52 COPD patients [19]. Twenty-seven were emphysematous (definition based on DLCO/AV < 80%), but there was no difference in terms of BMD. Another study found no influence of DLCO/AV or TLC and T-score, but included only 50 patients and none with a mild disease stage [20]. In our study, emphysema was investigated with respiratory functional tests, available in daily practice. Complete functional emphysema parameters using pulmonary respiratory tests (hyperinflation with impaired diffusion capacity and transfer coefficient) were associated with osteoporosis at the total hip in univariate analysis and confirmed in multivariate analysis. We have also analyzed two of three parameters, but no correlation was found. Fouda et al. considered that emphysema was not a determinant of osteoporosis and suggested a link between FEV1 and emphysematous status to explain that emphysema was significant in some studies [19]. In our study, COPD severity of obstruction (analyzed with FEV1%) was not a risk factor for bone disease associated with COPD and could not interfere. COPD severity has been associated with bone disease in individual studies (e.g., lower T-scores in patients with GOLD D COPD, links between BMD and FEV1 (%) [20]), but not in meta-analyses. In our population, FEV1 was not associated with osteoporosis diagnosis or demineralization, meaning that COPD obstruction severity is not a significant factor to consider in osteoporosis risk.
In our cohort, lumbar spine BMD density was not associated with the spirometric diffusion value, while there was a correlation for the total hip. A first explanation can be that tobacco, which is the main driver of COPD, could have a direct negative effect on cortical bone, rather than on trabecular bone (negative correlation between femoral neck BMD and both cigarette consumption (per-day) and packets-years according to [21]; association between smoking and reduced cortical thickness in young men according to [22]). On the other hand, lumbar spine analysis is less reliable in the elderly, with overestimation in the case of vertebral fracture or spine osteoarthritis (the mean age of our cohort was 64.5 years, with 80 for the oldest patient).
Our patients with higher BMI had less osteoporosis. This is consistent with the pooled data by Chen et al. that associated BMI < 18.5 kg/m2 with an OR of having osteoporosis of 4.26 and an increase of BMI by 1 kg/m2 with an OR of 0.8 [9]. We previously identified low BMI as one of the most potent drivers of osteoporosis in the overall population of our hospital [23]. This is of particular importance in the COPD population with regard to the high rate of low BMI and sarcopenia (sarcopenia being more important in COPD patients with osteoporosis or osteopenia than in COPD patients with normal BMD [7]).
Osteoporosis prevalence was 25.6% in our COPD population. Two recent meta-analyses [10,11] estimated this prevalence at 38 and 37%, more than our data. This could be related to geographic particularities since a COPD cohort coming from a neighboring country showed a very close incidence to ours (21%) [8]. Lower osteoporosis prevalence could perhaps be explained by the recruitment of our population, which was ambulatory with regular follow-up. The ambulatory COPD population could be in better health than people with sub-optimal follow-up.
In conclusion, our data show that lung function impairment, associating hyperinflation with impaired diffusion capacity and transfer coefficient (DLCO < 70%, DLCO/AV < 80% and TLC > 115%), is an independent risk factor for hip osteoporosis. In contrast, the severity of airway obstruction was not associated with bone density parameters. Pulmonary function tests with emphysema detection could help to identify patients that need osteoporosis screening.
Supplementary Materials
The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jcm12062383/s1, Table S1: Description of pulmonary parameters on functional respiratory tests. N = number. SD = standard deviation. FEV1 = fraction of expired volume in 1 s. FVC = forced vital capacity. TLC = total lung capacity. DLCO = diffusion capacity of the lung for CO. AV = alveolar volume. N = number. SD = standard deviation.
Author Contributions
Conceptualization: O.M., R.L., C.R. and M.M.; methodology: L.S.; original draft preparation: O.M. and C.A.; review and editing: O.M., C.A., C.V.D., L.S., F.S., R.L., C.R. and M.M.; project administration: R.L., C.R. and M.M. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding.
Institutional Review Board Statement
Approval was not mandatory because all examinations performed (functional respiratory test and DEXA) were part of the standard of care of COPD management.
Informed Consent Statement
Informed Consent Statement was not mandatory because all examinations performed (functional respiratory test and DEXA) were part of the standard of care of COPD management.
Data Availability Statement
The data presented in this study are available on reasonable request from the corresponding author.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Celli, B.; Fabbri, L.; Criner, G.; Martinez, F.; Mannino, D.; Vogelmeier, C.; Montes de Oca, M.; Papi, A.; Sin, D.; Han, M.; et al. Definition and nomenclature of chronic obstructive pulmonary disease: Time for its revision. Am. J. Respir. Crit. Care Med. 2022, 206, 1317–1325. [Google Scholar] [CrossRef]
- Vestbo, J.; Agusti, A.; Wouters, E.F.; Bakke, P.; Calverley, P.M.; Celli, B.; Coxson, H.; Crim, C.; Edwards, L.D.; Locantore, N.; et al. Should we view chronic obstructive pulmonary disease differently after ECLIPSE? A clinical perspective from the study team. Am. J. Respir. Crit. Care Med. 2014, 189, 1022–1030. [Google Scholar] [CrossRef] [Green Version]
- Vikjord, S.A.A.; Brumpton, B.M.; Mai, X.M.; Bhatta, L.; Vanfleteren, L.; Langhammer, A. The Association of Bone Mineral Density with Mortality in a COPD Cohort. The HUNT Study, Norway. Copd 2019, 16, 321–329. [Google Scholar] [CrossRef] [PubMed]
- Pascual-Guardia, S.; Badenes-Bonet, D.; Martin-Ontiyuelo, C.; Zuccarino, F.; Marin-Corral, J.; Rodriguez, A.; Barreiro, E.; Gea, J. Hospital admissions and mortality in patients with COPD exacerbations and vertebral body compression fractures. Int. J. Chronic Obstr. Pulm. Dis. 2017, 12, 1837–1845. [Google Scholar] [CrossRef] [Green Version]
- Van Cauwenberge, H.; Thonnard, A.S.; Nguyen Dang, D.; Corhay, J.L.; Louis, R. Long-term oxygen therapy: Mortality rate, short-term predictive mortality factors. Rev. Des Mal. Respir. 2018, 35, 939–947. [Google Scholar] [CrossRef]
- Schlaich, C.; Minne, H.W.; Bruckner, T.; Wagner, G.; Gebest, H.J.; Grunze, M.; Ziegler, R.; Leidig-Bruckner, G. Reduced pulmonary function in patients with spinal osteoporotic fractures. Osteoporos. Int. 1998, 8, 261–267. [Google Scholar] [CrossRef] [PubMed]
- Harrison, R.A.; Siminoski, K.; Vethanayagam, D.; Majumdar, S.R. Osteoporosis-related kyphosis and impairments in pulmonary function: A systematic review. J. Bone Miner. Res. Off. J. Am. Soc. Bone Miner. Res. 2007, 22, 447–457. [Google Scholar] [CrossRef] [PubMed]
- Graat-Verboom, L.; Spruit, M.A.; van den Borne, B.E.; Smeenk, F.W.; Martens, E.J.; Lunde, R.; Wouters, E.F.; Network, C. Correlates of osteoporosis in chronic obstructive pulmonary disease: An underestimated systemic component. Respir. Med. 2009, 103, 1143–1151. [Google Scholar] [CrossRef] [Green Version]
- Ferguson, G.T.; Calverley, P.M.A.; Anderson, J.A.; Jenkins, C.R.; Jones, P.W.; Willits, L.R.; Yates, J.C.; Vestbo, J.; Celli, B. Prevalence and progression of osteoporosis in patients with COPD: Results from the TOwards a Revolution in COPD Health study. Chest 2009, 136, 1456–1465. [Google Scholar] [CrossRef]
- Chen, Y.W.; Ramsook, A.H.; Coxson, H.O.; Bon, J.; Reid, W.D. Prevalence and Risk Factors for Osteoporosis in Individuals with COPD: A Systematic Review and Meta-analysis. Chest 2019, 156, 1092–1110. [Google Scholar] [CrossRef]
- Bitar, A.N.; Syed Sulaiman, S.A.; Ali, I.A.H.; Khan, I.; Khan, A.H. Osteoporosis among Patients with Chronic Obstructive Pulmonary Disease: Systematic Review and Meta-analysis of Prevalence, Severity, and Therapeutic Outcomes. J. Pharm. Bioallied Sci. 2019, 11, 310–320. [Google Scholar] [CrossRef] [PubMed]
- Allen-Ramey, F.C.; Gupta, S.; DiBonaventura, M.D. Patient characteristics, treatment patterns, and health outcomes among COPD phenotypes. Int. J. Chronic Obstr. Pulm. Dis. 2012, 7, 779–787. [Google Scholar] [CrossRef] [Green Version]
- Izquierdo-Alonso, J.L.; Rodriguez-Gonzalezmoro, J.M.; de Lucas-Ramos, P.; Unzueta, I.; Ribera, X.; Anton, E.; Martin, A. Prevalence and characteristics of three clinical phenotypes of chronic obstructive pulmonary disease (COPD). Respir. Med. 2013, 107, 724–731. [Google Scholar] [CrossRef] [Green Version]
- Oh, Y.M.; Sheen, S.S.; Park, J.H.; Jin, U.R.; Yoo, J.W.; Seo, J.B.; Yoo, K.H.; Lee, J.H.; Kim, T.H.; Lim, S.Y.; et al. Emphysematous phenotype is an independent predictor for frequent exacerbation of COPD. Int. J. Tuberc. Lung Dis. 2014, 18, 1407–1414. [Google Scholar] [CrossRef]
- Bai, P.; Sun, Y.; Jin, J.; Hou, J.; Li, R.; Zhang, Q.; Wang, Y. Disturbance of the OPG/RANK/RANKL pathway and systemic inflammation in COPD patients with emphysema and osteoporosis. Respir. Res. 2011, 12, 157. [Google Scholar] [CrossRef] [Green Version]
- Bon, J.; Fuhrman, C.R.; Weissfeld, J.L.; Duncan, S.R.; Branch, R.A.; Chang, C.C.; Zhang, Y.; Leader, J.K.; Gur, D.; Greenspan, S.L.; et al. Radiographic emphysema predicts low bone mineral density in a tobacco-exposed cohort. Am. J. Respir. Crit. Care Med. 2011, 183, 885–890. [Google Scholar] [CrossRef] [Green Version]
- Jaramillo, J.D.; Wilson, C.; Stinson, D.S.; Lynch, D.A.; Bowler, R.P.; Lutz, S.; Bon, J.M.; Arnold, B.; McDonald, M.L.; Washko, G.R.; et al. Reduced Bone Density and Vertebral Fractures in Smokers. Men and COPD Patients at Increased Risk. Ann. Am. Thorac. Soc. 2015, 12, 648–656. [Google Scholar] [CrossRef] [Green Version]
- Ohara, T.; Hirai, T.; Muro, S.; Haruna, A.; Terada, K.; Kinose, D.; Marumo, S.; Ogawa, E.; Hoshino, Y.; Niimi, A.; et al. Relationship between pulmonary emphysema and osteoporosis assessed by CT in patients with COPD. Chest 2008, 134, 1244–1249. [Google Scholar] [CrossRef] [PubMed]
- Fouda, M.A.; Alhamad, E.H.; Al-Hajjaj, M.S.; Shaik, S.A.; Alboukai, A.A.; Al-Kassimi, F.A. A study of chronic obstructive pulmonary disease-specific causes of osteoporosis with emphasis on the emphysema phenotype. Ann. Thorac. Med. 2017, 12, 101–106. [Google Scholar] [CrossRef] [PubMed]
- Sakurai-Iesato, Y.; Kawata, N.; Tada, Y.; Iesato, K.; Matsuura, Y.; Yahaba, M.; Suzuki, T.; Ikari, J.; Yanagawa, N.; Kasahara, Y.; et al. The Relationship of Bone Mineral Density in Men with Chronic Obstructive Pulmonary Disease Classified According to the Global Initiative for Chronic Obstructive Lung Disease (GOLD) Combined Chronic Obstructive Pulmonary Disease (COPD) Assessment System. Intern. Med. 2017, 56, 1781–1790. [Google Scholar] [CrossRef] [Green Version]
- Uçar, R.M.; Marakoğlu, K.; Kara, G.; Kızmaz, M.; Levendoğlu, F. The Comparison of Bone Mineral Density Between Male Smokers and Non-Smokers. Anatol. J. Fam. Med. 2019, 2, 19–26. [Google Scholar]
- Lorentzon, M.; Mellström, D.; Haug, E.; Ohlsson, C. Smoking Is Associated with Lower Bone Mineral Density and Reduced Cortical Thickness in Young Men. J. Clin. Endocrinoly Med. 2007, 92, 497–503. [Google Scholar]
- Malaise, O.; Detroz, M.; Leroy, M.; Leonori, L.; Seidel, L.; Malaise, M.G. High detection rate of osteoporosis with screening of a general hospitalized population: A 6-year study in 6406 patients in a university hospital setting. BMC Musculoskelet. Disord. 2020, 21, 90. [Google Scholar] [CrossRef] [Green Version]
Table 1.
Demographic and clinical data for the 90 COPD patients.
| Variable | N | Mean | SD | Min | Median | Max |
|---|---|---|---|---|---|---|
| Age (year) | 90 | 63.4 | 10.1 | 40.0 | 64.00 | 83.0 |
| Height (cm) | 90 | 167.4 | 9.1 | 149.0 | 167.00 | 185.5 |
| Weight (kg) | 90 | 68.1 | 17.3 | 35.0 | 66.00 | 118.5 |
| BMI (kg/m2) | 90 | 24.1 | 5.2 | 14.5 | 23.40 | 44.0 |
| Variable | N | Categories | N (%) | |||
| Sex | 90 | Male | 56 (62.2) | |||
| Smoking | 90 | No (non-smoker) | 1 (1.1) | |||
| No (ex-smoker) | 49 (54.4) | |||||
| Yes (active smoker) | 40 (44.4) | |||||
| Alcohol | 90 | No | 28 (31.1) | |||
| Yes | 30 (33.3) | |||||
| Occasional | 32 (35.6) | |||||
| Corticosteroids (history of use) | 90 | No | 64 (71.1) | |||
| Yes | 26 (28.9) | |||||
| Corticosteroids (chronic use) | 90 | No | 28 (31.1) | |||
| Yes (total) | 62 (68.9) | |||||
| Yes (inhaled only) | 56 (62.2) | |||||
| Yes (also systemic) | 6 (6.7) | |||||
| Fracture history | 90 | No | 41 (45.6) | |||
| Yes | 49 (54.4) | |||||
| Hip fracture history | 90 | No | 85 (94.4) | |||
| Yes | 5 (5.6) | |||||
| Vertebral fracture history | 90 | No | 83 (92.2) | |||
| Yes | 7 (7.8) | |||||
“Corticosteroids history of use” was defined as described in the FRAX algorithm (current or previous treatment for >3 months at a prednisone dose 35 mg/day). N = number. SD = standard deviation.
Table 2.
Description of bone mineral density, T-scores and DEXA diagnosis (normal, osteopenia or osteoporosis). N = number. SD = standard deviation. BMD = Bone Mineral Density.
Table 2.
Description of bone mineral density, T-scores and DEXA diagnosis (normal, osteopenia or osteoporosis). N = number. SD = standard deviation. BMD = Bone Mineral Density.
| Variable | N | Mean | SD | Min | Median | Max |
|---|---|---|---|---|---|---|
| BMD lumbar spine (g/cm2) | 90 | 0.937 | 0.181 | 0.6 | 0.92 | 1.5 |
| BMD femoral neck (g/cm2) | 89 | 0.687 | 0.123 | 0.4 | 0.68 | 1.0 |
| BMD total hip (g/cm2) | 89 | 0.819 | 0.151 | 0.4 | 0.82 | 1.1 |
| T-score lumbar spine | 90 | −0.959 | 1.647 | −4.2 | −1.30 | 3.9 |
| T-score femoral neck | 89 | −1.547 | 0.996 | −4.3 | −1.60 | 0.7 |
| T-score total hip | 89 | −1.258 | 1.025 | −4.2 | −1.30 | 0.8 |
| Variable | N | Categories | N (%) | |||
| Global diagnosis | 90 | Normal | 18 (20.0) | |||
| Osteopenia | 49 (54.4) | |||||
| Osteoporosis | 23 (25.6) | |||||
| Lumbar spine diagnostic | 90 | Normal | 39 (43.3) | |||
| Osteopenia | 37 (41.1) | |||||
| Osteoporosis | 14 (15.6) | |||||
| Femoral neck diagnostic | 89 | Normal | 22 (24.7) | |||
| Osteopenia | 53 (59.6) | |||||
| Osteoporosis | 14 (15.7) | |||||
| Total hip diagnostic | 89 | Normal | 32 (36.0) | |||
| Osteopenia | 45 (50.6) | |||||
| Osteoporosis | 12 (13.5) | |||||
Table 3.
Correlation between clinical/respiratory parameters and osteoporosis diagnosis (univariate analyses).
Table 3.
Correlation between clinical/respiratory parameters and osteoporosis diagnosis (univariate analyses).
| Lumbar Spine | Femoral Neck | Total Hip | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Osteoporosis L1–L4 (vs. Osteopenic/Normal) | Osteoporosis Femoral Neck (vs. Osteopenic/Normal) | Osteoporosis Total Hip (vs. Osteopenic/Normal) | ||||||||||
| OR | CI 95% | p-Value | OR | CI 95% | p-Value | OR | CI 95% | p-Value | ||||
| Gender (male) | 0.39 | 0.122 | 1.244 | 0.11 | 0.069 | 0.014 | 0.335 | 0.0009 | 0.16 | 0.04 | 0.644 | 0.0099 |
| Age (year) | 0.991 | 0.936 | 1.048 | 0.75 | 0.997 | 0.942 | 1.055 | 0.91 | 1.041 | 0.975 | 1.111 | 0.23 |
| BMI (kg/m2) | 0.735 | 0.606 | 0.893 | 0.002 | 0.820 | 0.698 | 0.963 | 0.016 | 0.655 | 0.513 | 0.837 | 0.0007 |
| Corticosteroids (chronic use) | 1.154 | 0.328 | 4.053 | 0.82 | 1.106 | 0.314 | 3.895 | 0.88 | 2.404 | 0.49 | 11.803 | 0.28 |
| Corticosteroids (history of use) | 1.455 | 0.437 | 4.847 | 0.54 | 2.947 | 0.915 | 9.494 | 0.070 | 4.274 | 1.213 | 15.054 | 0.024 |
| Active smoking | 5.943 | 1.528 | 23.105 | 0.010 | 3.965 | 1.137 | 13.829 | 0.031 | 2.968 | 0.822 | 10.714 | 0.097 |
| FEV1 (%) | 1.014 | 0.98 | 1.048 | 0.43 | 1.008 | 0.975 | 1.042 | 0.65 | 0.992 | 0.957 | 1.028 | 0.66 |
| TLC (%) | 1.011 | 0.977 | 1.047 | 0.53 | 1.003 | 0.969 | 1.038 | 0.88 | 1.029 | 0.991 | 1.07 | 0.14 |
| TLC > 115% | 1.154 | 0.331 | 4.017 | 0.82 | 0.741 | 0.203 | 2.706 | 0.65 | 2.640 | 0.680 | 10.256 | 0.16 |
| DLCO (%) | 1.017 | 0.976 | 1.06 | 0.43 | 0.99 | 0.95 | 1.033 | 0.65 | 0.968 | 0.922 | 1.015 | 0.18 |
| DLCO < 70% | 2.185 | 0.496 | 9.628 | 0.30 | 0.463 | 0.054 | 3.96 | 0.48 | 0.586 | 0.067 | 5.101 | 0.63 |
| DLCO/AV (%) | 0.997 | 0.973 | 1.021 | 0.78 | 0.992 | 0.967 | 1.017 | 0.51 | 0.972 | 0.942 | 1.003 | 0.081 |
| DLCO/AV < 80% | 1.429 | 0.417 | 4.889 | 0.57 | 0.936 | 0.269 | 3.251 | 0.92 | 0.525 | 0.125 | 2.202 | 0.38 |
| DLCO < 70%, DLCO/AV < 80% and TLC > 115% | 1.625 | 0.432 | 6.111 | 0.47 | 1.594 | 0.424 | 5.997 | 0.49 | 5.894 | 1.461 | 23.769 | 0.013 |
OR = odds ratio. CI = confidence interval. BMI = body mass index. FEV1 = fraction of expired volume in 1 s. FVC = forced vital capacity. TLC = total lung capacity. DLCO = diffusion capacity of the lung for CO. AV = alveolar volume. In grey and bold, significant correlation (p < 0.05). Lumbar spine: N = 90 (N = 80 for TPC, DLCO, DLCO/AV and association). Femoral neck and total hip: N = 89 (N = 79 for TPC, DLCO, DLCO/AV and association).
Table 4.
Correlation between clinical/respiratory parameters and osteoporosis diagnosis (multivariate analyses).
Table 4.
Correlation between clinical/respiratory parameters and osteoporosis diagnosis (multivariate analyses).
| Lumbar Spine | Femoral Neck | Total Hip | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Osteoporosis L1–L4 (vs. Osteopenic/Normal) (AUC = 0.817) | Osteoporosis Femoral Neck (vs. Osteopenic/Normal) (AUC = 0.872) | Osteoporosis Total Hip (vs. Osteopenic/Normal) (AUC = 0.946) | ||||||||||
| OR | CI95% | p-Value | OR | CI95% | p-Value | OR | CI95% | p-Value | ||||
| Gender (male) | 0.503 | 0.099 | 2.549 | 0.41 | 0.049 | 0.006 | 0.393 | 0.005 | 0.034 | 0.001 | 0.905 | 0.043 |
| Age (year) | 1.029 | 0.958 | 1.105 | 0.43 | 1.027 | 0.950 | 1.111 | 0.50 | 1.110 | 1.001 | 1.231 | 0.047 |
| BMI (kg/m2) | 0.795 | 0.635 | 0.996 | 0.047 | 0.850 | 0.690 | 1.048 | 0.13 | 0.635 | 0.448 | 0.899 | 0.011 |
| Corticosteroids (chronic use) | 1.029 | 0.205 | 5.156 | 0.97 | 0.761 | 0.129 | 4.487 | 0.76 | 0.866 | 0.066 | 11.393 | 0.91 |
| Corticosteroids (history of use) | 1.079 | 0.181 | 6.425 | 0.93 | 1.366 | 0.246 | 7.574 | 0.72 | 4.675 | 0.458 | 47.727 | 0.19 |
| Active smoking | 4.715 | 0.990 | 22.453 | 0.052 | 4.856 | 0.856 | 27.566 | 0.074 | 7.255 | 0.363 | 144.891 | 0.19 |
| FEV1 (%) | 1.015 | 0.971 | 1.061 | 0.50 | 0.991 | 0.942 | 1.041 | 0.71 | 0.968 | 0.895 | 1.047 | 0.42 |
| DLCO < 70%, DLCO/AV < 80% and TLC > 115% | 1.194 | 0.235 | 6.057 | 0.83 | 1.539 | 0.291 | 8.150 | 0.61 | 12.143 | 1.062 | 138.806 | 0.045 |
OR = odds ratio. CI = confidence interval. BMI = body mass index. FEV1 = fraction of expired volume in 1 s. Lumbar spine: N = 80. Femoral neck and total hip: N = 79.
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Malaise, O.; André, C.; Van Durme, C.; Seidel, L.; Schleich, F.; Louis, R.; Malaise, M.; Ribbens, C. Lung Function Impairment, Associating Hyperinflation with Impaired Diffusion Capacity and Transfer Coefficient, Is a Risk Factor for Hip Osteoporosis in Patients with Chronic Obstructive Pulmonary Disease. J. Clin. Med. 2023, 12, 2383. https://doi.org/10.3390/jcm12062383
AMA Style
Malaise O, André C, Van Durme C, Seidel L, Schleich F, Louis R, Malaise M, Ribbens C. Lung Function Impairment, Associating Hyperinflation with Impaired Diffusion Capacity and Transfer Coefficient, Is a Risk Factor for Hip Osteoporosis in Patients with Chronic Obstructive Pulmonary Disease. Journal of Clinical Medicine. 2023; 12(6):2383. https://doi.org/10.3390/jcm12062383
Chicago/Turabian StyleMalaise, Olivier, Cécile André, Caroline Van Durme, Laurence Seidel, Florence Schleich, Renaud Louis, Michel Malaise, and Clio Ribbens. 2023. "Lung Function Impairment, Associating Hyperinflation with Impaired Diffusion Capacity and Transfer Coefficient, Is a Risk Factor for Hip Osteoporosis in Patients with Chronic Obstructive Pulmonary Disease" Journal of Clinical Medicine 12, no. 6: 2383. https://doi.org/10.3390/jcm12062383
APA StyleMalaise, O., André, C., Van Durme, C., Seidel, L., Schleich, F., Louis, R., Malaise, M., & Ribbens, C. (2023). Lung Function Impairment, Associating Hyperinflation with Impaired Diffusion Capacity and Transfer Coefficient, Is a Risk Factor for Hip Osteoporosis in Patients with Chronic Obstructive Pulmonary Disease. Journal of Clinical Medicine, 12(6), 2383. https://doi.org/10.3390/jcm12062383
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