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Published in: Arthritis Research & Therapy 1/2018

Open Access 01-12-2018 | Research article

Effect of combined treatment with bisphosphonate and vitamin D on atherosclerosis in patients with systemic lupus erythematosus: a propensity score-based analysis

Authors: Kazumasa Ohmura, Masaru Kato, Toshiyuki Watanabe, Kenji Oku, Toshiyuki Bohgaki, Tetsuya Horita, Shinsuke Yasuda, Yoichi M. Ito, Norihiro Sato, Tatsuya Atsumi

Published in: Arthritis Research & Therapy | Issue 1/2018

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Abstract

Background

Premature atherosclerosis is one of the major complications of systemic lupus erythematosus (SLE). Recently, the biological linkage between atherosclerosis and osteoporosis has garnered much attention. The aim of this study is to explore correlation between the development of atherosclerosis and anti-osteoporotic treatment.

Methods

Consecutive patients with SLE (n = 117) who underwent carotid ultrasonography were retrospectively analyzed using propensity scoring.

Results

Of the 117 patients, 42 (36%), 27 (23%), and 30 (26%) were receiving bisphosphonates and vitamin D (BP + VD), bisphosphonates alone, or vitamin D alone, respectively. Low bone mineral density was more frequent, and carotid plaque was less prevalent in the BP + VD group compared with other treatment groups. Age (OR = 1.57) and BP + VD treatment (OR = 0.24) were shown by multivariate analysis to be associated with the presence of carotid plaque. In all strata divided using the propensity score, carotid plaque was statistically significantly less prevalent (p = 0.015, Mantel-Haenszel test) in the BP + VD group relative to the other treatment groups.

Conclusion

Combined treatment with bisphosphonate and vitamin D may have a role in preventing atherosclerosis in patients with SLE.
Appendix
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Literature
1.
go back to reference Gustafsson JT, Svenungsson E. Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity. 2014;47(2):67–76.CrossRefPubMed Gustafsson JT, Svenungsson E. Definitions of and contributions to cardiovascular disease in systemic lupus erythematosus. Autoimmunity. 2014;47(2):67–76.CrossRefPubMed
2.
go back to reference Hyder JA, Allison MA, Barrett-Connor E, Detrano R, Wong ND, Sirlin C, Gapstur SM, Ouyang P, Carr JJ, Criqui MH. Bone mineral density and atherosclerosis: the multi-ethnic study of atherosclerosis, abdominal aortic calcium study. Atherosclerosis. 2010;209(1):283–9.CrossRefPubMed Hyder JA, Allison MA, Barrett-Connor E, Detrano R, Wong ND, Sirlin C, Gapstur SM, Ouyang P, Carr JJ, Criqui MH. Bone mineral density and atherosclerosis: the multi-ethnic study of atherosclerosis, abdominal aortic calcium study. Atherosclerosis. 2010;209(1):283–9.CrossRefPubMed
3.
go back to reference Ye C, Xu M, Wang S, Jiang S, Chen X, Zhou X, He R. Decreased bone mineral density is an independent predictor for the development of atherosclerosis: a systematic review and meta-analysis. PLoS One. 2016;11(5):e0154740.CrossRefPubMedPubMedCentral Ye C, Xu M, Wang S, Jiang S, Chen X, Zhou X, He R. Decreased bone mineral density is an independent predictor for the development of atherosclerosis: a systematic review and meta-analysis. PLoS One. 2016;11(5):e0154740.CrossRefPubMedPubMedCentral
4.
go back to reference Rogers MJ, Crockett JC, Coxon FP, Monkkonen J. Biochemical and molecular mechanisms of action of bisphosphonates. Bone. 2011;49(1):34–41.CrossRefPubMed Rogers MJ, Crockett JC, Coxon FP, Monkkonen J. Biochemical and molecular mechanisms of action of bisphosphonates. Bone. 2011;49(1):34–41.CrossRefPubMed
5.
go back to reference Wang TJ, Pencina MJ, Booth SL, Jacques PF, Ingelsson E, Lanier K, Benjamin EJ, D'Agostino RB, Wolf M, Vasan RS. Vitamin D deficiency and risk of cardiovascular disease. Circulation. 2008;117(4):503–11.CrossRefPubMed Wang TJ, Pencina MJ, Booth SL, Jacques PF, Ingelsson E, Lanier K, Benjamin EJ, D'Agostino RB, Wolf M, Vasan RS. Vitamin D deficiency and risk of cardiovascular disease. Circulation. 2008;117(4):503–11.CrossRefPubMed
6.
go back to reference Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25(11):1271–7.CrossRefPubMed Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25(11):1271–7.CrossRefPubMed
7.
go back to reference Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus eryhematosus. Arthritis Rheumatol. 1997;40:1725.CrossRef Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus eryhematosus. Arthritis Rheumatol. 1997;40:1725.CrossRef
8.
go back to reference Terminology and Diagnostic Criteria Committee, Japan Society of Ultrasonics in Medicine. Standard method for ultrasound evaluation of carotid artery lesions. J Med Ultrason. 2009;36(4):219–26. Terminology and Diagnostic Criteria Committee, Japan Society of Ultrasonics in Medicine. Standard method for ultrasound evaluation of carotid artery lesions. J Med Ultrason. 2009;36(4):219–26.
9.
go back to reference Kanis JA. An update on the diagnosis and assessment of osteoporosis with densitometry. Osteoporos Int. 2000;11:192–202.CrossRefPubMed Kanis JA. An update on the diagnosis and assessment of osteoporosis with densitometry. Osteoporos Int. 2000;11:192–202.CrossRefPubMed
10.
go back to reference Ajeganova S, Gustafsson T, Jogestrand T, Frostegard J, Hafstrom I. Bone mineral density and carotid atherosclerosis in systemic lupus erythematosus: a controlled cross-sectional study. Arthritis Res Ther. 2015;17:84.CrossRefPubMedPubMedCentral Ajeganova S, Gustafsson T, Jogestrand T, Frostegard J, Hafstrom I. Bone mineral density and carotid atherosclerosis in systemic lupus erythematosus: a controlled cross-sectional study. Arthritis Res Ther. 2015;17:84.CrossRefPubMedPubMedCentral
11.
go back to reference van Leuven SI, Mendez-Fernandez YV, Stroes ES, Tak PP, Major AS. Statin therapy in lupus-mediated atherogenesis: two birds with one stone? Ann Rheum Dis. 2011;70(2):245–8.CrossRefPubMed van Leuven SI, Mendez-Fernandez YV, Stroes ES, Tak PP, Major AS. Statin therapy in lupus-mediated atherogenesis: two birds with one stone? Ann Rheum Dis. 2011;70(2):245–8.CrossRefPubMed
12.
go back to reference Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS. Lupus atherosclerosis prevention study (LAPS). Ann Rheum Dis. 2011;70(5):760–5.CrossRefPubMed Petri MA, Kiani AN, Post W, Christopher-Stine L, Magder LS. Lupus atherosclerosis prevention study (LAPS). Ann Rheum Dis. 2011;70(5):760–5.CrossRefPubMed
13.
go back to reference Dominguez LJ, Di Bella G, Belvedere M, Barbagallo M. Physiology of the aging bone and mechanisms of action of bisphosphonates. Biogerontology. 2011;12(5):397–408.CrossRefPubMed Dominguez LJ, Di Bella G, Belvedere M, Barbagallo M. Physiology of the aging bone and mechanisms of action of bisphosphonates. Biogerontology. 2011;12(5):397–408.CrossRefPubMed
14.
go back to reference Kang YM, Hong SH, Yang JH, Oh JC, Park JO, Lee BH, Lee SY, Kim HS, Lee HM, Moon SH. Pamidronate down-regulates tumor necrosis factor-alpha induced matrix metalloproteinases expression in human intervertebral disc cells. J Bone Metab. 2016;23(3):165–73.CrossRefPubMedPubMedCentral Kang YM, Hong SH, Yang JH, Oh JC, Park JO, Lee BH, Lee SY, Kim HS, Lee HM, Moon SH. Pamidronate down-regulates tumor necrosis factor-alpha induced matrix metalloproteinases expression in human intervertebral disc cells. J Bone Metab. 2016;23(3):165–73.CrossRefPubMedPubMedCentral
15.
go back to reference Talaat RM, Sidek A, Mosalem A, Kholief A. Effect of bisphosphonates treatment on cytokine imbalance between TH17 and Treg in osteoporosis. Inflammopharmacology. 2015;23(2–3):119–25.CrossRefPubMed Talaat RM, Sidek A, Mosalem A, Kholief A. Effect of bisphosphonates treatment on cytokine imbalance between TH17 and Treg in osteoporosis. Inflammopharmacology. 2015;23(2–3):119–25.CrossRefPubMed
16.
go back to reference Sharma D, Hamlet SM, Petcu EB, Ivanovski S. The effect of bisphosphonates on the endothelial differentiation of mesenchymal stem cells. Sci Rep. 2016;6:20580.CrossRefPubMedPubMedCentral Sharma D, Hamlet SM, Petcu EB, Ivanovski S. The effect of bisphosphonates on the endothelial differentiation of mesenchymal stem cells. Sci Rep. 2016;6:20580.CrossRefPubMedPubMedCentral
17.
go back to reference Lang M, Zhou Z, Shi L, Niu J, Xu S, Lin W, Chen Z, Wang Y. Influence of zoledronic acid on proliferation, migration, and apoptosis of vascular endothelial cells. Br J Oral Maxillofac Surg. 2016;54(8):889–93.CrossRefPubMed Lang M, Zhou Z, Shi L, Niu J, Xu S, Lin W, Chen Z, Wang Y. Influence of zoledronic acid on proliferation, migration, and apoptosis of vascular endothelial cells. Br J Oral Maxillofac Surg. 2016;54(8):889–93.CrossRefPubMed
18.
go back to reference Tanko LB, Qin G, Alexandersen P, Bagger YZ, Christiansen C. Effective doses of ibandronate do not influence the 3-year progression of aortic calcification in elderly osteoporotic women. Osteoporos Int. 2005;16(2):184–90.CrossRefPubMed Tanko LB, Qin G, Alexandersen P, Bagger YZ, Christiansen C. Effective doses of ibandronate do not influence the 3-year progression of aortic calcification in elderly osteoporotic women. Osteoporos Int. 2005;16(2):184–90.CrossRefPubMed
19.
go back to reference Kranenburg G, Bartstra JW, Weijmans M, de Jong PA, Mali WP, Verhaar HJ, Visseren FL, Spiering W. Bisphosphonates for cardiovascular risk reduction: a systematic review and meta-analysis. Atherosclerosis. 2016;252:106–15.CrossRefPubMed Kranenburg G, Bartstra JW, Weijmans M, de Jong PA, Mali WP, Verhaar HJ, Visseren FL, Spiering W. Bisphosphonates for cardiovascular risk reduction: a systematic review and meta-analysis. Atherosclerosis. 2016;252:106–15.CrossRefPubMed
20.
go back to reference Kawahara T, Nishikawa M, Kawahara C, Inazu T, Sakai K, Suzuki G. Atorvastatin, etidronate, or both in patients at high risk for atherosclerotic aortic plaques: a randomized, controlled trial. Circulation. 2013;127(23):2327–35.CrossRefPubMed Kawahara T, Nishikawa M, Kawahara C, Inazu T, Sakai K, Suzuki G. Atorvastatin, etidronate, or both in patients at high risk for atherosclerotic aortic plaques: a randomized, controlled trial. Circulation. 2013;127(23):2327–35.CrossRefPubMed
21.
go back to reference Manson JE, Bassuk SS, Lee IM, Cook NR, Albert MA, Gordon D, Zaharris E, Macfadyen JG, Danielson E, Lin J, et al. The VITamin D and OmegA-3 TriaL (VITAL): rationale and design of a large randomized controlled trial of vitamin D and marine omega-3 fatty acid supplements for the primary prevention of cancer and cardiovascular disease. Contemp Clin Trials. 2012;33(1):159–71.CrossRefPubMed Manson JE, Bassuk SS, Lee IM, Cook NR, Albert MA, Gordon D, Zaharris E, Macfadyen JG, Danielson E, Lin J, et al. The VITamin D and OmegA-3 TriaL (VITAL): rationale and design of a large randomized controlled trial of vitamin D and marine omega-3 fatty acid supplements for the primary prevention of cancer and cardiovascular disease. Contemp Clin Trials. 2012;33(1):159–71.CrossRefPubMed
22.
go back to reference Lima GL, Paupitz J, Aikawa NE, Takayama L, Bonfa E, Pereira RM. Vitamin D supplementation in adolescents and young adults with juvenile Systemic lupus erythematosus for improvement in disease activity and fatigue scores: a randomized, double-blind, placebo-controlled trial. Arthritis Care Res (Hoboken). 2016;68(1):91–8.CrossRef Lima GL, Paupitz J, Aikawa NE, Takayama L, Bonfa E, Pereira RM. Vitamin D supplementation in adolescents and young adults with juvenile Systemic lupus erythematosus for improvement in disease activity and fatigue scores: a randomized, double-blind, placebo-controlled trial. Arthritis Care Res (Hoboken). 2016;68(1):91–8.CrossRef
23.
go back to reference Gepner AD, Ramamurthy R, Krueger DC, Korcarz CE, Binkley N, Stein JH. A prospective randomized controlled trial of the effects of vitamin D supplementation on cardiovascular disease risk. PLoS One. 2012;7(5):e36617.CrossRefPubMedPubMedCentral Gepner AD, Ramamurthy R, Krueger DC, Korcarz CE, Binkley N, Stein JH. A prospective randomized controlled trial of the effects of vitamin D supplementation on cardiovascular disease risk. PLoS One. 2012;7(5):e36617.CrossRefPubMedPubMedCentral
24.
go back to reference Robinson AB, Tangpricha V, Yow E, Gurion R, Schanberg LE, McComsey GA, Investigators A. Vitamin D status is a determinant of atorvastatin effect on carotid intima medial thickening progression rate in children with lupus: an atherosclerosis prevention in pediatric lupus erythematosus (APPLE) substudy. Lupus Sci Med. 2014;1(1):e000037.CrossRefPubMedPubMedCentral Robinson AB, Tangpricha V, Yow E, Gurion R, Schanberg LE, McComsey GA, Investigators A. Vitamin D status is a determinant of atorvastatin effect on carotid intima medial thickening progression rate in children with lupus: an atherosclerosis prevention in pediatric lupus erythematosus (APPLE) substudy. Lupus Sci Med. 2014;1(1):e000037.CrossRefPubMedPubMedCentral
Metadata
Title
Effect of combined treatment with bisphosphonate and vitamin D on atherosclerosis in patients with systemic lupus erythematosus: a propensity score-based analysis
Authors
Kazumasa Ohmura
Masaru Kato
Toshiyuki Watanabe
Kenji Oku
Toshiyuki Bohgaki
Tetsuya Horita
Shinsuke Yasuda
Yoichi M. Ito
Norihiro Sato
Tatsuya Atsumi
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2018
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/s13075-018-1589-9

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