Skip to main content
Top
Published in: Calcified Tissue International 6/2020

01-06-2020 | Lymphoma | Original Research

Increased Risk of Hip Fracture in Patients with Lymphoma, a Swedish Population Study of 37,236 Lymphoma Patients

Authors: Peter Johansson, Hallgerdur Lind Kristjansdottir, Helena Johansson, Ana Jakir, Dan Mellström, Catharina Lewerin

Published in: Calcified Tissue International | Issue 6/2020

Login to get access

Abstract

Increased bone loss has been noted in lymphoma patients; however, the incidence of hip fracture is not known. The aim of our study was to explore the risk for hip fracture in patients with lymphoma compared with the entire Swedish population. The risk of hip fracture was determined in a retrospective population cohort study of adult Swedish lymphoma patients (n = 37,236), diagnosed 1995–2015 and compared with the entire Swedish population during the same period. The incidence of hip fracture in lymphoma patients was higher in women than in men, increased by age, and decreased by calendar year as also demonstrated in the total population. 2.2% of the men and 4.7% of women with lymphoma sustained a hip fracture. For the total group of females, the hazard ratio (HR) was 1.19 (95% CI 1.11–1.28) and for men, the hazard ratio was 1.06 (95% CI 0.97–1.17) compared with the Swedish population. The HR for hip fracture (2016) was 2.80 (95% CI 1.20–6.53), 2.04 (95% CI 1.30–3.20), 1.56 (95% CI 1.21–2.01), 1.08 (95% CI 0.89–1.30), and 1.07 (95% CI 0.92–1.25) in females aged 40, 50, 60, 70, and 80 years, respectively. Corresponding figures for men were not significant in 2016. Unmarried men with lymphoma had a two times higher risk for hip fracture (HR 2.02 95% CI 1.63–2.50) compared with married men. Patients with lymphoma had an increased risk of hip fracture, especially younger women and unmarried men. The incidence of hip fracture is decreased by calendar year in the lymphoma patients and the entire Swedish population.
Literature
1.
go back to reference Kanis JA, Oden A, McCloskey EV, Johansson H, Wahl DA, Cooper C (2012) A systematic review of hip fracture incidence and probability of fracture worldwide. Osteoporos Int 23:2239–2256CrossRef Kanis JA, Oden A, McCloskey EV, Johansson H, Wahl DA, Cooper C (2012) A systematic review of hip fracture incidence and probability of fracture worldwide. Osteoporos Int 23:2239–2256CrossRef
2.
go back to reference Oden A, Kanis JA, McCloskey EV, Johansson H (2014) The effect of latitude on the risk and seasonal variation in hip fracture in Sweden. J Bone Miner Res 29:2217–2223CrossRef Oden A, Kanis JA, McCloskey EV, Johansson H (2014) The effect of latitude on the risk and seasonal variation in hip fracture in Sweden. J Bone Miner Res 29:2217–2223CrossRef
3.
4.
go back to reference Svendsen P, Shekhrajka N, Nielsen KL, Vestergaard P, Poulsen MO, Vistisen AK, Munksgaard PS, Severinsen MT, Jensen P, Johnsen HE, Jakobsen LH, Bogsted M, Frokjaer JB, El-Galaly TC (2017) R-CHOP(-like) treatment of diffuse large B-cell lymphoma significantly reduces CT-assessed vertebral bone density: a single center study of 111 patients. Leuk Lymphoma 58:1105–1113CrossRef Svendsen P, Shekhrajka N, Nielsen KL, Vestergaard P, Poulsen MO, Vistisen AK, Munksgaard PS, Severinsen MT, Jensen P, Johnsen HE, Jakobsen LH, Bogsted M, Frokjaer JB, El-Galaly TC (2017) R-CHOP(-like) treatment of diffuse large B-cell lymphoma significantly reduces CT-assessed vertebral bone density: a single center study of 111 patients. Leuk Lymphoma 58:1105–1113CrossRef
5.
go back to reference van Staa TP (2006) The pathogenesis, epidemiology and management of glucocorticoid-induced osteoporosis. Calcif Tissue Int 79:129–137CrossRef van Staa TP (2006) The pathogenesis, epidemiology and management of glucocorticoid-induced osteoporosis. Calcif Tissue Int 79:129–137CrossRef
6.
go back to reference Seland M, Smeland KB, Bjoro T, Falk RS, Fossa SD, Gjesdal CG, Godang K, Holte H, Svartberg J, Syversen U, Bollerslev J, Kiserud CE (2017) Bone mineral density is close to normal for age in long-term lymphoma survivors treated with high-dose therapy with autologous stem cell transplantation. Acta Oncol 56:590–598CrossRef Seland M, Smeland KB, Bjoro T, Falk RS, Fossa SD, Gjesdal CG, Godang K, Holte H, Svartberg J, Syversen U, Bollerslev J, Kiserud CE (2017) Bone mineral density is close to normal for age in long-term lymphoma survivors treated with high-dose therapy with autologous stem cell transplantation. Acta Oncol 56:590–598CrossRef
7.
go back to reference Ruchlemer R, Amit-Kohn M, Tvito A, Sindelovsky I, Zimran A, Raveh-Brawer D (2018) Bone loss and hematological malignancies in adults: a pilot study. Support Care Cancer 26:3013–3020CrossRef Ruchlemer R, Amit-Kohn M, Tvito A, Sindelovsky I, Zimran A, Raveh-Brawer D (2018) Bone loss and hematological malignancies in adults: a pilot study. Support Care Cancer 26:3013–3020CrossRef
8.
go back to reference Cabanillas ME, Lu H, Fang S, Du XL (2007) Elderly patients with non-Hodgkin lymphoma who receive chemotherapy are at higher risk for osteoporosis and fractures. Leuk Lymphoma 48:1514–1521CrossRef Cabanillas ME, Lu H, Fang S, Du XL (2007) Elderly patients with non-Hodgkin lymphoma who receive chemotherapy are at higher risk for osteoporosis and fractures. Leuk Lymphoma 48:1514–1521CrossRef
9.
go back to reference Svedbom A, Borgstom F, Hernlund E, Strom O, Alekna V, Bianchi ML, Clark P, Curiel MD, Dimai HP, Jurisson M, Kallikorm R, Lember M, Lesnyak O, McCloskey E, Sanders KM, Silverman S, Solodovnikov A, Tamulaitiene M, Thomas T, Toroptsova N, Uuskula A, Tosteson ANA, Jonsson B, Kanis JA (2018) Quality of life for up to 18 months after low-energy hip, vertebral, and distal forearm fractures-results from the ICUROS. Osteoporos Int 29:557–566CrossRef Svedbom A, Borgstom F, Hernlund E, Strom O, Alekna V, Bianchi ML, Clark P, Curiel MD, Dimai HP, Jurisson M, Kallikorm R, Lember M, Lesnyak O, McCloskey E, Sanders KM, Silverman S, Solodovnikov A, Tamulaitiene M, Thomas T, Toroptsova N, Uuskula A, Tosteson ANA, Jonsson B, Kanis JA (2018) Quality of life for up to 18 months after low-energy hip, vertebral, and distal forearm fractures-results from the ICUROS. Osteoporos Int 29:557–566CrossRef
10.
go back to reference Katsoulis M, Benetou V, Karapetyan T, Feskanich D, Grodstein F, Pettersson-Kymmer U, Eriksson S, Wilsgaard T, Jorgensen L, Ahmed LA, Schottker B, Brenner H, Bellavia A, Wolk A, Kubinova R, Stegeman B, Bobak M, Boffetta P, Trichopoulou A (2017) Excess mortality after hip fracture in elderly persons from Europe and the USA: the CHANCES project. J Intern Med 281:300–310CrossRef Katsoulis M, Benetou V, Karapetyan T, Feskanich D, Grodstein F, Pettersson-Kymmer U, Eriksson S, Wilsgaard T, Jorgensen L, Ahmed LA, Schottker B, Brenner H, Bellavia A, Wolk A, Kubinova R, Stegeman B, Bobak M, Boffetta P, Trichopoulou A (2017) Excess mortality after hip fracture in elderly persons from Europe and the USA: the CHANCES project. J Intern Med 281:300–310CrossRef
11.
go back to reference 3) Osteoporosis - Prevention, Diagnosis and Treatment: A Systematic Review. 2003 by the Swedish Council on Health Technology Assessment., Stockholm 3) Osteoporosis - Prevention, Diagnosis and Treatment: A Systematic Review. 2003 by the Swedish Council on Health Technology Assessment., Stockholm
12.
go back to reference Hektoen LF, Saltvedt I, Sletvold O, Helbostad JL, Luras H, Halsteinli V (2016) One-year health and care costs after hip fracture for home-dwelling elderly patients in Norway: Results from the Trondheim Hip Fracture Trial. Scand J Public Health 44:791–798CrossRef Hektoen LF, Saltvedt I, Sletvold O, Helbostad JL, Luras H, Halsteinli V (2016) One-year health and care costs after hip fracture for home-dwelling elderly patients in Norway: Results from the Trondheim Hip Fracture Trial. Scand J Public Health 44:791–798CrossRef
13.
go back to reference Williamson S, Landeiro F, McConnell T, Fulford-Smith L, Javaid MK, Judge A, Leal J (2017) Costs of fragility hip fractures globally: a systematic review and meta-regression analysis. Osteoporos Int 28:2791–2800CrossRef Williamson S, Landeiro F, McConnell T, Fulford-Smith L, Javaid MK, Judge A, Leal J (2017) Costs of fragility hip fractures globally: a systematic review and meta-regression analysis. Osteoporos Int 28:2791–2800CrossRef
14.
go back to reference Paccou J, Merlusca L, Henry-Desailly I, Parcelier A, Gruson B, Royer B, Charbonnier A, Ursu D, Desailloud R, Garidi R, Kamel S, Sevestre H, Marolleau JP, Fardellone P, Damaj G (2014) Alterations in bone mineral density and bone turnover markers in newly diagnosed adults with lymphoma receiving chemotherapy: a 1-year prospective pilot study. Ann Oncol 25:481–486CrossRef Paccou J, Merlusca L, Henry-Desailly I, Parcelier A, Gruson B, Royer B, Charbonnier A, Ursu D, Desailloud R, Garidi R, Kamel S, Sevestre H, Marolleau JP, Fardellone P, Damaj G (2014) Alterations in bone mineral density and bone turnover markers in newly diagnosed adults with lymphoma receiving chemotherapy: a 1-year prospective pilot study. Ann Oncol 25:481–486CrossRef
15.
go back to reference Albertsson-Wikland K, Martensson A, Savendahl L, Niklasson A, Bang P, Dahlgren J, Gustafsson J, Kristrom B, Norgren S, Pehrsson NG, Oden A (2016) Mortality Is Not Increased in Recombinant Human Growth Hormone-treated Patients When Adjusting for Birth Characteristics. J Clin Endocrinol Metab 101:2149–2159CrossRef Albertsson-Wikland K, Martensson A, Savendahl L, Niklasson A, Bang P, Dahlgren J, Gustafsson J, Kristrom B, Norgren S, Pehrsson NG, Oden A (2016) Mortality Is Not Increased in Recombinant Human Growth Hormone-treated Patients When Adjusting for Birth Characteristics. J Clin Endocrinol Metab 101:2149–2159CrossRef
16.
go back to reference Breslow NE, Day NE (1987) Statistical methods in cancer research. Volume II--The design and analysis of cohort studies. IARC Sci Publ:1–406 Breslow NE, Day NE (1987) Statistical methods in cancer research. Volume II--The design and analysis of cohort studies. IARC Sci Publ:1–406
17.
go back to reference Curtis EM, van der Velde R, Moon RJ, van den Bergh JP, Geusens P, de Vries F, van Staa TP, Cooper C, Harvey NC (2016) Epidemiology of fractures in the United Kingdom 1988–2012: Variation with age, sex, geography, ethnicity and socioeconomic status. Bone 87:19–26CrossRef Curtis EM, van der Velde R, Moon RJ, van den Bergh JP, Geusens P, de Vries F, van Staa TP, Cooper C, Harvey NC (2016) Epidemiology of fractures in the United Kingdom 1988–2012: Variation with age, sex, geography, ethnicity and socioeconomic status. Bone 87:19–26CrossRef
18.
go back to reference Tao L, Foran JM, Clarke CA, Gomez SL, Keegan TH (2014) Socioeconomic disparities in mortality after diffuse large B-cell lymphoma in the modern treatment era. Blood 123:3553–3562CrossRef Tao L, Foran JM, Clarke CA, Gomez SL, Keegan TH (2014) Socioeconomic disparities in mortality after diffuse large B-cell lymphoma in the modern treatment era. Blood 123:3553–3562CrossRef
19.
go back to reference Hansen L, Judge A, Javaid MK, Cooper C, Vestergaard P, Abrahamsen B, Harvey NC (2018) Social inequality and fractures-secular trends in the Danish population: a case-control study. Osteoporos Int 29:2243–2250CrossRef Hansen L, Judge A, Javaid MK, Cooper C, Vestergaard P, Abrahamsen B, Harvey NC (2018) Social inequality and fractures-secular trends in the Danish population: a case-control study. Osteoporos Int 29:2243–2250CrossRef
20.
go back to reference Handforth C, D'Oronzo S, Coleman R, Brown J (2018) Cancer Treatment and Bone Health. Calcif Tissue Int 102:251–264CrossRef Handforth C, D'Oronzo S, Coleman R, Brown J (2018) Cancer Treatment and Bone Health. Calcif Tissue Int 102:251–264CrossRef
21.
go back to reference Pfeilschifter J, Diel IJ (2000) Osteoporosis due to cancer treatment: pathogenesis and management. J Clin Oncol 18:1570–1593CrossRef Pfeilschifter J, Diel IJ (2000) Osteoporosis due to cancer treatment: pathogenesis and management. J Clin Oncol 18:1570–1593CrossRef
22.
go back to reference Zhao D, Wang C, Zhao Y, Shu B, Jia Y, Liu S, Wang H, Chang J, Dai W, Lu S, Shi Q, Yang Y, Zhang Y, Wang Y (2017) Cyclophosphamide causes osteoporosis in C57BL/6 male mice: suppressive effects of cyclophosphamide on osteoblastogenesis and osteoclastogenesis. Oncotarget 8:98163–98183PubMedPubMedCentral Zhao D, Wang C, Zhao Y, Shu B, Jia Y, Liu S, Wang H, Chang J, Dai W, Lu S, Shi Q, Yang Y, Zhang Y, Wang Y (2017) Cyclophosphamide causes osteoporosis in C57BL/6 male mice: suppressive effects of cyclophosphamide on osteoblastogenesis and osteoclastogenesis. Oncotarget 8:98163–98183PubMedPubMedCentral
23.
go back to reference Leib ES, Saag KG, Adachi JD, Geusens PP, Binkley N, McCloskey EV, Hans DB (2011) Official Positions for FRAX((R)) clinical regarding glucocorticoids: the impact of the use of glucocorticoids on the estimate by FRAX((R)) of the 10 year risk of fracture from Joint Official Positions Development Conference of the International Society for Clinical Densitometry and International Osteoporosis Foundation on FRAX((R)). J Clin Densitom 14:212–219CrossRef Leib ES, Saag KG, Adachi JD, Geusens PP, Binkley N, McCloskey EV, Hans DB (2011) Official Positions for FRAX((R)) clinical regarding glucocorticoids: the impact of the use of glucocorticoids on the estimate by FRAX((R)) of the 10 year risk of fracture from Joint Official Positions Development Conference of the International Society for Clinical Densitometry and International Osteoporosis Foundation on FRAX((R)). J Clin Densitom 14:212–219CrossRef
24.
go back to reference Van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C (2005) Use of oral corticosteroids and risk of fractures. June, 2000. J Bone Miner Res 20:1487–1494; discussion 1486 Van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C (2005) Use of oral corticosteroids and risk of fractures. June, 2000. J Bone Miner Res 20:1487–1494; discussion 1486
25.
go back to reference Ratcliffe MA, Lanham SA, Reid DM, Dawson AA (1992) Bone mineral density (BMD) in patients with lymphoma: the effects of chemotherapy, intermittent corticosteroids and premature menopause. Hematol Oncol 10:181–187CrossRef Ratcliffe MA, Lanham SA, Reid DM, Dawson AA (1992) Bone mineral density (BMD) in patients with lymphoma: the effects of chemotherapy, intermittent corticosteroids and premature menopause. Hematol Oncol 10:181–187CrossRef
26.
go back to reference Asada N, Katayama Y (2014) Regulation of hematopoiesis in endosteal microenvironments. Int J Hematol 99:679–684CrossRef Asada N, Katayama Y (2014) Regulation of hematopoiesis in endosteal microenvironments. Int J Hematol 99:679–684CrossRef
27.
go back to reference Fulzele K, Krause DS, Panaroni C, Saini V, Barry KJ, Liu X, Lotinun S, Baron R, Bonewald L, Feng JQ, Chen M, Weinstein LS, Wu JY, Kronenberg HM, Scadden DT, Divieti Pajevic P (2013) Myelopoiesis is regulated by osteocytes through Gsalpha-dependent signaling. Blood 121:930–939CrossRef Fulzele K, Krause DS, Panaroni C, Saini V, Barry KJ, Liu X, Lotinun S, Baron R, Bonewald L, Feng JQ, Chen M, Weinstein LS, Wu JY, Kronenberg HM, Scadden DT, Divieti Pajevic P (2013) Myelopoiesis is regulated by osteocytes through Gsalpha-dependent signaling. Blood 121:930–939CrossRef
28.
go back to reference Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841–846CrossRef Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841–846CrossRef
29.
go back to reference Jantzen C, Madsen CM, Lauritzen JB, Jorgensen HL (2018) Temporal trends in hip fracture incidence, mortality, and morbidity in Denmark from 1999 to 2012. Acta Orthop 89:170–176CrossRef Jantzen C, Madsen CM, Lauritzen JB, Jorgensen HL (2018) Temporal trends in hip fracture incidence, mortality, and morbidity in Denmark from 1999 to 2012. Acta Orthop 89:170–176CrossRef
30.
go back to reference Lewiecki EM, Wright NC, Curtis JR, Siris E, Gagel RF, Saag KG, Singer AJ, Steven PM, Adler RA (2018) Hip fracture trends in the United States, 2002 to 2015. Osteoporos Int 29:717–722CrossRef Lewiecki EM, Wright NC, Curtis JR, Siris E, Gagel RF, Saag KG, Singer AJ, Steven PM, Adler RA (2018) Hip fracture trends in the United States, 2002 to 2015. Osteoporos Int 29:717–722CrossRef
31.
go back to reference Leslie WD, O'Donnell S, Jean S, Lagace C, Walsh P, Bancej C, Morin S, Hanley DA, Papaioannou A (2009) Trends in hip fracture rates in Canada. JAMA 302:883–889CrossRef Leslie WD, O'Donnell S, Jean S, Lagace C, Walsh P, Bancej C, Morin S, Hanley DA, Papaioannou A (2009) Trends in hip fracture rates in Canada. JAMA 302:883–889CrossRef
Metadata
Title
Increased Risk of Hip Fracture in Patients with Lymphoma, a Swedish Population Study of 37,236 Lymphoma Patients
Authors
Peter Johansson
Hallgerdur Lind Kristjansdottir
Helena Johansson
Ana Jakir
Dan Mellström
Catharina Lewerin
Publication date
01-06-2020
Publisher
Springer US
Keyword
Lymphoma
Published in
Calcified Tissue International / Issue 6/2020
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-020-00674-7

Other articles of this Issue 6/2020

Calcified Tissue International 6/2020 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.