Skip to main content
Top
Published in: European Radiology 1/2015

01-01-2015 | Computed Tomography

Osteoporosis markers on low-dose lung cancer screening chest computed tomography scans predict all-cause mortality

Authors: C. F. Buckens, Y. van der Graaf, H. M. Verkooijen, W. P. Mali, I. Isgum, C. P. Mol, H. J. Verhaar, R. Vliegenthart, M. Oudkerk, C. M. van Aalst, H. J. de Koning, P. A. de Jong

Published in: European Radiology | Issue 1/2015

Login to get access

Abstract

Objectives

Further survival benefits may be gained from low-dose chest computed tomography (CT) by assessing vertebral fractures and bone density. We sought to assess the association between CT-measured vertebral fractures and bone density with all-cause mortality in lung cancer screening participants.

Methods

Following a case-cohort design, lung cancer screening trial participants (N = 3,673) who died (N = 196) during a median follow-up of 6 years (inter-quartile range: 5.7–6.3) were identified and added to a random sample of N = 383 from the trial. We assessed vertebral fractures using Genant´s semiquantative method on sagittal reconstructions and measured bone density (Hounsfield Units (HU)) in vertebrae. Cox proportional hazards modelling was used to determine if vertebral fractures or bone density were independently predictive of mortality.

Results

The prevalence of vertebral fractures was 35 % (95 % confidence interval 30–40 %) among survivors and 51 % (44–58 %) amongst cases. After adjusting for age, gender, smoking status, pack years smoked, coronary and aortic calcium volume and pulmonary emphysema, the adjusted hazard ratio (HR) for vertebral fracture was 2.04 (1.43–2.92). For each 10 HU decline in trabecular bone density, the adjusted HR was 1.08 (1.02–1.15).

Conclusions

Vertebral fractures and bone density are independently associated with all-cause mortality.

Key Points

Lung cancer screening chest computed tomography contains additional, potentially useful information.
Vertebral fractures and bone density are independently predictive of mortality.
This finding has implications for screening and management decisions.
Appendix
Available only for authorised users
Literature
1.
go back to reference Team NLSTR, Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD et al (2011) Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 365:395–409CrossRef Team NLSTR, Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD et al (2011) Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 365:395–409CrossRef
2.
go back to reference Bach PB, Mirkin JN, Oliver TK, Azzoli CG, Berry DA, Brawley OW et al (2012) Benefits and harms of CT screening for lung cancer: a systematic review. JAMA J Am Med Assoc 307:2418–2429CrossRef Bach PB, Mirkin JN, Oliver TK, Azzoli CG, Berry DA, Brawley OW et al (2012) Benefits and harms of CT screening for lung cancer: a systematic review. JAMA J Am Med Assoc 307:2418–2429CrossRef
3.
go back to reference Mets OM, de Jong PA, Prokop M (2012) Computed tomographic screening for lung cancer: an opportunity to evaluate other diseases. JAMA J Am Med Assoc 308:1433–1434CrossRef Mets OM, de Jong PA, Prokop M (2012) Computed tomographic screening for lung cancer: an opportunity to evaluate other diseases. JAMA J Am Med Assoc 308:1433–1434CrossRef
4.
go back to reference Mets OM, Buckens CFM, Zanen P, Isgum I, van Ginneken B, Prokop M et al (2011) Identification of chronic obstructive pulmonary disease in lung cancer screening computed tomographic scans. JAMA J Am Med Assoc 306:1775–1781CrossRef Mets OM, Buckens CFM, Zanen P, Isgum I, van Ginneken B, Prokop M et al (2011) Identification of chronic obstructive pulmonary disease in lung cancer screening computed tomographic scans. JAMA J Am Med Assoc 306:1775–1781CrossRef
5.
go back to reference Mets OM, Vliegenthart R, Gondrie MJ, Viergever MA, Oudkerk M, de Koning HJ et al (2013) Lung cancer screening CT-based prediction of cardiovascular events. JACC Cardiovasc Imaging 6:899–907. doi:10.1016/j.jcmg.2013.02.008 Mets OM, Vliegenthart R, Gondrie MJ, Viergever MA, Oudkerk M, de Koning HJ et al (2013) Lung cancer screening CT-based prediction of cardiovascular events. JACC Cardiovasc Imaging 6:899–907. doi:10.​1016/​j.​jcmg.​2013.​02.​008
6.
go back to reference McEvoy JW, Blaha MJ, Rivera JJ, Budoff MJ, Khan AN, Shaw LJ et al (2012) Mortality rates in smokers and nonsmokers in the presence or absence of coronary artery calcification. JACC Cardiovasc Imaging 5:1037–1045PubMedCrossRef McEvoy JW, Blaha MJ, Rivera JJ, Budoff MJ, Khan AN, Shaw LJ et al (2012) Mortality rates in smokers and nonsmokers in the presence or absence of coronary artery calcification. JACC Cardiovasc Imaging 5:1037–1045PubMedCrossRef
7.
go back to reference Xie X, Zhao Y, de Bock GH, de Jong PA, Mali WP, Oudkerk M et al (2013) Validation and prognosis of coronary artery calcium scoring in non-triggered thoracic computed tomography: systematic review and meta-analysis. Circ Cardiovasc Imaging 6:514–521. doi:10.1161/CIRCIMAGING.113.000092 Xie X, Zhao Y, de Bock GH, de Jong PA, Mali WP, Oudkerk M et al (2013) Validation and prognosis of coronary artery calcium scoring in non-triggered thoracic computed tomography: systematic review and meta-analysis. Circ Cardiovasc Imaging 6:514–521. doi:10.​1161/​CIRCIMAGING.​113.​000092
8.
go back to reference Centers for Disease Control and Prevention (CDC) (2005) Annual smoking-attributable mortality, years of potential life lost, and productivity losses--United States, 1997–2001. MMWR Morb Mortal Wkly Rep 54:625–628 Centers for Disease Control and Prevention (CDC) (2005) Annual smoking-attributable mortality, years of potential life lost, and productivity losses--United States, 1997–2001. MMWR Morb Mortal Wkly Rep 54:625–628
9.
go back to reference Gan WQ, Man SFP, Senthilselvan A, Sin DD (2004) Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax 59:574–580PubMedCentralPubMedCrossRef Gan WQ, Man SFP, Senthilselvan A, Sin DD (2004) Association between chronic obstructive pulmonary disease and systemic inflammation: a systematic review and a meta-analysis. Thorax 59:574–580PubMedCentralPubMedCrossRef
10.
go back to reference Pickhardt PJ, Pooler BD, Lauder T, del Rio AM, Bruce RJ, Binkley N (2013) Opportunistic screening for osteoporosis using abdominal computed tomography scans obtained for other indications. Ann Intern Med 158:588–595PubMedCentralPubMedCrossRef Pickhardt PJ, Pooler BD, Lauder T, del Rio AM, Bruce RJ, Binkley N (2013) Opportunistic screening for osteoporosis using abdominal computed tomography scans obtained for other indications. Ann Intern Med 158:588–595PubMedCentralPubMedCrossRef
11.
go back to reference Romme EAPM, Murchison JT, Phang KF, Jansen FH, Rutten EPA, Wouters EFM et al (2012) Bone attenuation on routine chest CT correlates with bone mineral density on DXA in patients with COPD. J Bone Miner Res Off J Am Soc Bone Miner Res 27:2338–2343CrossRef Romme EAPM, Murchison JT, Phang KF, Jansen FH, Rutten EPA, Wouters EFM et al (2012) Bone attenuation on routine chest CT correlates with bone mineral density on DXA in patients with COPD. J Bone Miner Res Off J Am Soc Bone Miner Res 27:2338–2343CrossRef
12.
go back to reference Johansson C, Black D, Johnell O, Odén A, Mellström D (1998) Bone mineral density is a predictor of survival. Calcif Tissue Int 63:190–196PubMedCrossRef Johansson C, Black D, Johnell O, Odén A, Mellström D (1998) Bone mineral density is a predictor of survival. Calcif Tissue Int 63:190–196PubMedCrossRef
13.
go back to reference Buckens CF, de Jong PA, Mol C, Bakker E, Stallman HP, Mali WP et al (2013) Intra and interobserver reliability and agreement of semiquantitative vertebral fracture assessment on chest computed tomography. Woloschak GE, ed. PLoS ONE 8:e71204PubMedCentralPubMedCrossRef Buckens CF, de Jong PA, Mol C, Bakker E, Stallman HP, Mali WP et al (2013) Intra and interobserver reliability and agreement of semiquantitative vertebral fracture assessment on chest computed tomography. Woloschak GE, ed. PLoS ONE 8:e71204PubMedCentralPubMedCrossRef
14.
go back to reference Jalava T, Sarna S, Pylkkänen L, Mawer B, Kanis JA, Selby P et al (2003) Association between vertebral fracture and increased mortality in osteoporotic patients. J Bone Miner Res Off J Am Soc Bone Miner Res 18:1254–1260CrossRef Jalava T, Sarna S, Pylkkänen L, Mawer B, Kanis JA, Selby P et al (2003) Association between vertebral fracture and increased mortality in osteoporotic patients. J Bone Miner Res Off J Am Soc Bone Miner Res 18:1254–1260CrossRef
15.
go back to reference Hasserius R, Karlsson MK, Nilsson BE, Redlund-Johnell I, Johnell O (2003) Prevalent vertebral deformities predict increased mortality and increased fracture rate in both men and women: a 10-year population-based study of 598 individuals from the Swedish cohort in the European Vertebral Osteoporosis Study. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 14:61–68CrossRef Hasserius R, Karlsson MK, Nilsson BE, Redlund-Johnell I, Johnell O (2003) Prevalent vertebral deformities predict increased mortality and increased fracture rate in both men and women: a 10-year population-based study of 598 individuals from the Swedish cohort in the European Vertebral Osteoporosis Study. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 14:61–68CrossRef
16.
go back to reference Trone DW, Kritz-Silverstein D, von Mühlen DG, Wingard DL, Barrett-Connor E (2007) Is radiographic vertebral fracture a risk factor for mortality? Am J Epidemiol 166:1191–1197PubMedCrossRef Trone DW, Kritz-Silverstein D, von Mühlen DG, Wingard DL, Barrett-Connor E (2007) Is radiographic vertebral fracture a risk factor for mortality? Am J Epidemiol 166:1191–1197PubMedCrossRef
17.
go back to reference Puisto V, Rissanen H, Heliövaara M, Knekt P, Helenius I (2008) Mortality in the presence of a vertebral fracture, scoliosis, or Scheuermann’s disease in the thoracic spine. Ann Epidemiol 18:595–601PubMedCrossRef Puisto V, Rissanen H, Heliövaara M, Knekt P, Helenius I (2008) Mortality in the presence of a vertebral fracture, scoliosis, or Scheuermann’s disease in the thoracic spine. Ann Epidemiol 18:595–601PubMedCrossRef
18.
go back to reference Ikeda Y, Sudo A, Yamada T, Uchida A (2010) Mortality after vertebral fractures in a Japanese population. J Orthop Surg Hong Kong 18:148–152PubMed Ikeda Y, Sudo A, Yamada T, Uchida A (2010) Mortality after vertebral fractures in a Japanese population. J Orthop Surg Hong Kong 18:148–152PubMed
19.
go back to reference Waterloo S, Ahmed LA, Center JR, Eisman JA, Morseth B, Nguyen ND et al (2012) Prevalence of vertebral fractures in women and men in the population-based Tromsø Study. BMC Musculoskelet Disord 13:3PubMedCentralPubMedCrossRef Waterloo S, Ahmed LA, Center JR, Eisman JA, Morseth B, Nguyen ND et al (2012) Prevalence of vertebral fractures in women and men in the population-based Tromsø Study. BMC Musculoskelet Disord 13:3PubMedCentralPubMedCrossRef
20.
go back to reference Buckens C, de Jong P, Mali W, Verhaar H, van der Graaf Y, Verkooijen H (2014) Prevalent vertebral fractures on chest CT: higher risk for future hip fracture. J Bone Miner Res Off J Am Soc Bone Miner Res 29:392–398. doi:10.1002/jbmr.2028 Buckens C, de Jong P, Mali W, Verhaar H, van der Graaf Y, Verkooijen H (2014) Prevalent vertebral fractures on chest CT: higher risk for future hip fracture. J Bone Miner Res Off J Am Soc Bone Miner Res 29:392–398. doi:10.​1002/​jbmr.​2028
21.
go back to reference Woo EK, Mansoubi H, Alyas F (2008) Incidental vertebral fractures on multidetector CT images of the chest: prevalence and recognition. Clin Radiol 63:160–164PubMedCrossRef Woo EK, Mansoubi H, Alyas F (2008) Incidental vertebral fractures on multidetector CT images of the chest: prevalence and recognition. Clin Radiol 63:160–164PubMedCrossRef
22.
go back to reference Bartalena T, Giannelli G, Rinaldi MF, Rimondi E, Rinaldi G, Sverzellati N et al (2009) Prevalence of thoracolumbar vertebral fractures on multidetector CT: underreporting by radiologists. Eur J Radiol 69:555–559PubMedCrossRef Bartalena T, Giannelli G, Rinaldi MF, Rimondi E, Rinaldi G, Sverzellati N et al (2009) Prevalence of thoracolumbar vertebral fractures on multidetector CT: underreporting by radiologists. Eur J Radiol 69:555–559PubMedCrossRef
23.
go back to reference Williams AL, Al-Busaidi A, Sparrow PJ, Adams JE, Whitehouse RW (2009) Under-reporting of osteoporotic vertebral fractures on computed tomography. Eur J Radiol 69:179–183PubMedCrossRef Williams AL, Al-Busaidi A, Sparrow PJ, Adams JE, Whitehouse RW (2009) Under-reporting of osteoporotic vertebral fractures on computed tomography. Eur J Radiol 69:179–183PubMedCrossRef
24.
go back to reference Müller D, Bauer JS, Zeile M, Rummeny EJ, Link TM (2008) Significance of sagittal reformations in routine thoracic and abdominal multislice CT studies for detecting osteoporotic fractures and other spine abnormalities. Eur Radiol 18:1696–1702PubMedCrossRef Müller D, Bauer JS, Zeile M, Rummeny EJ, Link TM (2008) Significance of sagittal reformations in routine thoracic and abdominal multislice CT studies for detecting osteoporotic fractures and other spine abnormalities. Eur Radiol 18:1696–1702PubMedCrossRef
25.
go back to reference Chan PL, Reddy T, Milne D, Bolland MJ (2012) Incidental vertebral fractures on computed tomography. N Z Med J 125:45–50PubMed Chan PL, Reddy T, Milne D, Bolland MJ (2012) Incidental vertebral fractures on computed tomography. N Z Med J 125:45–50PubMed
26.
go back to reference Bolland MJ, Grey AB, Gamble GD, Reid IR (2010) Effect of osteoporosis treatment on mortality: a meta-analysis. J Clin Endocrinol Metab 95:1174–1181PubMedCrossRef Bolland MJ, Grey AB, Gamble GD, Reid IR (2010) Effect of osteoporosis treatment on mortality: a meta-analysis. J Clin Endocrinol Metab 95:1174–1181PubMedCrossRef
27.
go back to reference Van Iersel CA, de Koning HJ, Draisma G, Mali WPTM, Scholten ET, Nackaerts K et al (2007) Risk-based selection from the general population in a screening trial: selection criteria, recruitment and power for the Dutch-Belgian randomised lung cancer multi-slice CT screening trial (NELSON). Int J Cancer J Int Cancer 120:868–874CrossRef Van Iersel CA, de Koning HJ, Draisma G, Mali WPTM, Scholten ET, Nackaerts K et al (2007) Risk-based selection from the general population in a screening trial: selection criteria, recruitment and power for the Dutch-Belgian randomised lung cancer multi-slice CT screening trial (NELSON). Int J Cancer J Int Cancer 120:868–874CrossRef
28.
go back to reference Onland-Moret NC, van der A DL, van der Schouw YT, Buschers W, Elias SG, van Gils CH et al (2007) Analysis of case-cohort data: a comparison of different methods. J Clin Epidemiol 60:350–355PubMedCrossRef Onland-Moret NC, van der A DL, van der Schouw YT, Buschers W, Elias SG, van Gils CH et al (2007) Analysis of case-cohort data: a comparison of different methods. J Clin Epidemiol 60:350–355PubMedCrossRef
29.
go back to reference Van Rikxoort EM, de Hoop B, Viergever MA, Prokop M, van Ginneken B (2009) Automatic lung segmentation from thoracic computed tomography scans using a hybrid approach with error detection. Med Phys 36:2934–2947PubMedCrossRef Van Rikxoort EM, de Hoop B, Viergever MA, Prokop M, van Ginneken B (2009) Automatic lung segmentation from thoracic computed tomography scans using a hybrid approach with error detection. Med Phys 36:2934–2947PubMedCrossRef
30.
go back to reference Schilham AMR, van Ginneken B, Gietema H, Prokop M (2006) Local noise weighted filtering for emphysema scoring of low-dose CT images. IEEE Trans Med Imaging 25:451–463PubMedCrossRef Schilham AMR, van Ginneken B, Gietema H, Prokop M (2006) Local noise weighted filtering for emphysema scoring of low-dose CT images. IEEE Trans Med Imaging 25:451–463PubMedCrossRef
31.
go back to reference Gevenois PA, De Vuyst P, de Maertelaer V, Zanen J, Jacobovitz D, Cosio MG et al (1996) Comparison of computed density and microscopic morphometry in pulmonary emphysema. Am J Respir Crit Care Med 154:187–192PubMedCrossRef Gevenois PA, De Vuyst P, de Maertelaer V, Zanen J, Jacobovitz D, Cosio MG et al (1996) Comparison of computed density and microscopic morphometry in pulmonary emphysema. Am J Respir Crit Care Med 154:187–192PubMedCrossRef
32.
go back to reference Newell JD Jr, Hogg JC, Snider GL (2004) Report of a workshop: quantitative computed tomography scanning in longitudinal studies of emphysema. Eur Respir J 23:769–775PubMedCrossRef Newell JD Jr, Hogg JC, Snider GL (2004) Report of a workshop: quantitative computed tomography scanning in longitudinal studies of emphysema. Eur Respir J 23:769–775PubMedCrossRef
33.
go back to reference Isgum I, Rutten A, Prokop M, Staring M, Klein S, Pluim JPW et al (2010) Automated aortic calcium scoring on low-dose chest computed tomography. Med Phys 37:714–723PubMedCrossRef Isgum I, Rutten A, Prokop M, Staring M, Klein S, Pluim JPW et al (2010) Automated aortic calcium scoring on low-dose chest computed tomography. Med Phys 37:714–723PubMedCrossRef
34.
go back to reference Isgum I, Prokop M, Niemeijer M, Viergever MA, van Ginneken B (2012) Automatic coronary calcium scoring in low-dose chest computed tomography. IEEE Trans Med Imaging 31:2322–2334PubMedCrossRef Isgum I, Prokop M, Niemeijer M, Viergever MA, van Ginneken B (2012) Automatic coronary calcium scoring in low-dose chest computed tomography. IEEE Trans Med Imaging 31:2322–2334PubMedCrossRef
35.
go back to reference Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res Off J Am Soc Bone Miner Res 8:1137–1148CrossRef Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res Off J Am Soc Bone Miner Res 8:1137–1148CrossRef
36.
go back to reference Siris ES, Genant HK, Laster AJ, Chen P, Misurski DA, Krege JH (2007) Enhanced prediction of fracture risk combining vertebral fracture status and BMD. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 18:761–770CrossRef Siris ES, Genant HK, Laster AJ, Chen P, Misurski DA, Krege JH (2007) Enhanced prediction of fracture risk combining vertebral fracture status and BMD. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 18:761–770CrossRef
37.
go back to reference De Bruin A, Karduan J, Gast F, De Bruin E, van Sijl M, Verweij G (2004) Record linkage of hospital discharge register with population register: experiences at Statistics Netherlands. Stat J United Nations Econ Comm Eur 1:23–32 De Bruin A, Karduan J, Gast F, De Bruin E, van Sijl M, Verweij G (2004) Record linkage of hospital discharge register with population register: experiences at Statistics Netherlands. Stat J United Nations Econ Comm Eur 1:23–32
38.
go back to reference Tromp M, Ravelli AC, Bonsel GJ, Hasman A, Reitsma JB (2011) Results from simulated data sets: probabilistic record linkage outperforms deterministic record linkage. J Clin Epidemiol 64:565–572PubMedCrossRef Tromp M, Ravelli AC, Bonsel GJ, Hasman A, Reitsma JB (2011) Results from simulated data sets: probabilistic record linkage outperforms deterministic record linkage. J Clin Epidemiol 64:565–572PubMedCrossRef
39.
go back to reference Prentice R (1986) A case-cohort design for epidemiologic cohort studies and disease prevention trials. Biometrika 73:1–11CrossRef Prentice R (1986) A case-cohort design for epidemiologic cohort studies and disease prevention trials. Biometrika 73:1–11CrossRef
40.
41.
go back to reference Pongchaiyakul C, Nguyen ND, Jones G, Center JR, Eisman JA, Nguyen TV (2005) Asymptomatic vertebral deformity as a major risk factor for subsequent fractures and mortality: a long-term prospective study. J Bone Miner Res Off J Am Soc Bone Miner Res 20:1349–1355CrossRef Pongchaiyakul C, Nguyen ND, Jones G, Center JR, Eisman JA, Nguyen TV (2005) Asymptomatic vertebral deformity as a major risk factor for subsequent fractures and mortality: a long-term prospective study. J Bone Miner Res Off J Am Soc Bone Miner Res 20:1349–1355CrossRef
42.
go back to reference Nasto LA, Fusco A, Colangelo D, Mormando M, Di Giacomo G, Rossi B et al (2012) Clinical predictors of vertebral osteoporotic fractures in post-menopausal women: a cross-sectional analysis. Eur Rev Med Pharmacol Sci 16:1227–1234PubMed Nasto LA, Fusco A, Colangelo D, Mormando M, Di Giacomo G, Rossi B et al (2012) Clinical predictors of vertebral osteoporotic fractures in post-menopausal women: a cross-sectional analysis. Eur Rev Med Pharmacol Sci 16:1227–1234PubMed
44.
go back to reference Kiyokawa H, Muro S, Oguma T, Sato S, Tanabe N, Takahashi T et al (2012) Impact of COPD exacerbations on osteoporosis assessed by chest CT scan. COPD 9:235–242PubMedCentralPubMedCrossRef Kiyokawa H, Muro S, Oguma T, Sato S, Tanabe N, Takahashi T et al (2012) Impact of COPD exacerbations on osteoporosis assessed by chest CT scan. COPD 9:235–242PubMedCentralPubMedCrossRef
45.
go back to reference Sennerby U, Melhus H, Gedeborg R, Byberg L, Garmo H, Ahlbom A et al (2009) Cardiovascular diseases and risk of hip fracture. JAMA J Am Med Assoc 302:1666–1673CrossRef Sennerby U, Melhus H, Gedeborg R, Byberg L, Garmo H, Ahlbom A et al (2009) Cardiovascular diseases and risk of hip fracture. JAMA J Am Med Assoc 302:1666–1673CrossRef
46.
go back to reference Nuti R, Siviero P, Maggi S, Guglielmi G, Caffarelli C, Crepaldi G et al (2009) Vertebral fractures in patients with chronic obstructive pulmonary disease: the EOLO Study. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 20:989–998CrossRef Nuti R, Siviero P, Maggi S, Guglielmi G, Caffarelli C, Crepaldi G et al (2009) Vertebral fractures in patients with chronic obstructive pulmonary disease: the EOLO Study. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 20:989–998CrossRef
47.
go back to reference Ensrud KE, Thompson DE, Cauley JA, Nevitt MC, Kado DM, Hochberg MC et al (2000) Prevalent vertebral deformities predict mortality and hospitalization in older women with low bone mass. Fracture Intervention Trial Research Group. J Am Geriatr Soc 48:241–249PubMed Ensrud KE, Thompson DE, Cauley JA, Nevitt MC, Kado DM, Hochberg MC et al (2000) Prevalent vertebral deformities predict mortality and hospitalization in older women with low bone mass. Fracture Intervention Trial Research Group. J Am Geriatr Soc 48:241–249PubMed
48.
go back to reference Puisto V, Rissanen H, Heliövaara M, Impivaara O, Jalanko T, Kröger H et al (2011) Vertebral fracture and cause-specific mortality: a prospective population study of 3,210 men and 3,730 women with 30 years of follow-up. Eur Spine J Off Publ Eur Spine Soc Eur Spinal Deform Soc Eur Sect Cerv Spine Res Soc 20:2181–2186CrossRef Puisto V, Rissanen H, Heliövaara M, Impivaara O, Jalanko T, Kröger H et al (2011) Vertebral fracture and cause-specific mortality: a prospective population study of 3,210 men and 3,730 women with 30 years of follow-up. Eur Spine J Off Publ Eur Spine Soc Eur Spinal Deform Soc Eur Sect Cerv Spine Res Soc 20:2181–2186CrossRef
49.
go back to reference Masunari N, Fujiwara S, Kasagi F, Takahashi I, Yamada M, Nakamura T (2012) Height loss starting in middle age predicts increased mortality in the elderly. J Bone Miner Res Off J Am Soc Bone Miner Res 27:138–145CrossRef Masunari N, Fujiwara S, Kasagi F, Takahashi I, Yamada M, Nakamura T (2012) Height loss starting in middle age predicts increased mortality in the elderly. J Bone Miner Res Off J Am Soc Bone Miner Res 27:138–145CrossRef
50.
go back to reference Wannamethee SG, Shaper AG, Lennon L, Whincup PH (2006) Height loss in older men: associations with total mortality and incidence of cardiovascular disease. Arch Intern Med 166:2546–2552PubMedCrossRef Wannamethee SG, Shaper AG, Lennon L, Whincup PH (2006) Height loss in older men: associations with total mortality and incidence of cardiovascular disease. Arch Intern Med 166:2546–2552PubMedCrossRef
51.
go back to reference Hillier TA, Lui L-Y, Kado DM, LeBlanc ES, Vesco KK, Bauer DC et al (2012) Height loss in older women: risk of hip fracture and mortality independent of vertebral fractures. J Bone Miner Res Off J Am Soc Bone Miner Res 27:153–159CrossRef Hillier TA, Lui L-Y, Kado DM, LeBlanc ES, Vesco KK, Bauer DC et al (2012) Height loss in older women: risk of hip fracture and mortality independent of vertebral fractures. J Bone Miner Res Off J Am Soc Bone Miner Res 27:153–159CrossRef
52.
go back to reference Kovalchik SA, Tammemagi M, Berg CD, Caporaso NE, Riley TL, Korch M et al (2013) Targeting of low-dose CT screening according to the risk of lung-cancer death. N Engl J Med 369:245–254PubMedCentralPubMedCrossRef Kovalchik SA, Tammemagi M, Berg CD, Caporaso NE, Riley TL, Korch M et al (2013) Targeting of low-dose CT screening according to the risk of lung-cancer death. N Engl J Med 369:245–254PubMedCentralPubMedCrossRef
53.
go back to reference Young RP, Hopkins RJ (2012) Chronic obstructive pulmonary disease detection during lung cancer screening. JAMA J Am Med Assoc 307:664, author reply 664–665CrossRef Young RP, Hopkins RJ (2012) Chronic obstructive pulmonary disease detection during lung cancer screening. JAMA J Am Med Assoc 307:664, author reply 664–665CrossRef
54.
go back to reference Young RP, Hopkins RJ, Midthun DE (2012) Computed tomographic screening for lung cancer. JAMA J Am Med Assoc 308:1320, author reply 1320–1321CrossRef Young RP, Hopkins RJ, Midthun DE (2012) Computed tomographic screening for lung cancer. JAMA J Am Med Assoc 308:1320, author reply 1320–1321CrossRef
55.
go back to reference Bazzocchi A, Spinnato P, Albisinni U et al (2012) A careful evaluation of scout CT lateral radiograph may prevent unreported vertebral fractures. Eur J Radiol 81:2353–2357PubMedCrossRef Bazzocchi A, Spinnato P, Albisinni U et al (2012) A careful evaluation of scout CT lateral radiograph may prevent unreported vertebral fractures. Eur J Radiol 81:2353–2357PubMedCrossRef
56.
go back to reference Bazzocchi A, Fuzzi F, Garzillo G et al (2013) Reliability and accuracy of scout CT in the detection of vertebral fractures. Br J Radiol 86:20130373PubMedCrossRef Bazzocchi A, Fuzzi F, Garzillo G et al (2013) Reliability and accuracy of scout CT in the detection of vertebral fractures. Br J Radiol 86:20130373PubMedCrossRef
Metadata
Title
Osteoporosis markers on low-dose lung cancer screening chest computed tomography scans predict all-cause mortality
Authors
C. F. Buckens
Y. van der Graaf
H. M. Verkooijen
W. P. Mali
I. Isgum
C. P. Mol
H. J. Verhaar
R. Vliegenthart
M. Oudkerk
C. M. van Aalst
H. J. de Koning
P. A. de Jong
Publication date
01-01-2015
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 1/2015
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-014-3361-0

Other articles of this Issue 1/2015

European Radiology 1/2015 Go to the issue