Skip to main content
Springer Nature Link
Log in

Incidence of Vertebral Fractures in Women with Systemic Lupus Erythematosus After 8 Years of Follow-Up

  • Original Research
  • Published:
Calcified Tissue International Aims and scope Submit manuscript

Abstract

The aim of this study was to evaluate possible associations between potential risk factors and the occurrence of established vertebral fractures (VF) in Mexican patients with systemic lupus erythematosus (SLE). Consecutive patients with SLE were enrolled in a prospective, observational study from 2006 to 2015. Information on potential risk factors, including demographics, clinical data, and bone mineral density (BMD) at the lumbar spine and hip on dual-energy X-ray absorptiometry was collected at baseline and follow-up. Semiquantitative analysis was used to determine incident VF on lateral thoracic and lumbar radiographs, defined as any vertebral body graded normal at baseline and at least mildly deformed (20–25% reduction or more in any vertebral height) during follow-up. Differences in baseline characteristics were assessed in patients with and without new radiographic VF. Of 110 SLE patients included, with a median follow-up of 8 (IQR 8–9) years, 22 (20%) had radiographic VF at baseline; 35 (32%) patients had a new VF. The annual incidence rate of new morphometric VF was 3.5 (95% CI 2.4–4.91) per 100 patient/years. Most fractures were mild or moderate and biconcave shaped. Incident VF were significantly associated with baseline BMD at the total hip and longer disease duration. Cumulative glucocorticoid dose, postmenopausal status, and previous prevalent VF were not associated with VF. In this SLE cohort in daily clinical practice, new VF were frequently present in SLE patients, especially those with longer disease duration and low-hip BMD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Lems WF (2007) Clinical relevance of vertebral fractures. Ann Rheum Dis 66:2–4. doi:10.1136/ard.2006.058313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Black DM, Arden NK, Palermo L et al (1999) Prevalent vertebral deformities predict hip fractures and new vertebral deformities but not wrist fractures. Study of Osteoporotic Fractures Research Group. J Bone Miner Res 14:821–828. doi:10.1359/jbmr.1999.14.5.821

    Article  CAS  PubMed  Google Scholar 

  3. Lindsay R, Silverman SL, Cooper C et al (2001) Risk of new vertebral fracture in the year following a fracture. JAMA 285:320–323

    Article  CAS  PubMed  Google Scholar 

  4. Borba VZC, Matos PG, da Silva Viana PR et al (2005) High prevalence of vertebral deformity in premenopausal systemic lupus erythematosus patients. Lupus 14:529–533. doi:10.1191/0961203305lu2154oa

    Article  CAS  PubMed  Google Scholar 

  5. Weiss RJ, Wick MC, Ackermann PW, Montgomery SM (2010) Increased fracture risk in patients with rheumatic disorders and other inflammatory diseases: a case-control study with 53,108 patients with fracture. J Rheumatol 37:2247–2250. doi:10.3899/jrheum.100363

    Article  PubMed  Google Scholar 

  6. Li EK, Tam LS, Griffith JF et al (2009) High prevalence of asymptomatic vertebral fractures in Chinese women with systemic lupus erythematosus. J Rheumatol 36:1646–1652. doi:10.3899/jrheum.081337

    Article  PubMed  Google Scholar 

  7. Mendoza-Pinto C, García-Carrasco M, Sandoval-Cruz H et al (2009) Risk factors of vertebral fractures in women with systemic lupus erythematosus. Clin Rheumatol 28:579–585. doi:10.1007/s10067-009-1105-3

    Article  PubMed  Google Scholar 

  8. Furukawa M, Kiyohara C, Horiuchi T et al (2013) Prevalence and risk factors of vertebral fracture in female Japanese patients with systemic lupus erythematosus. Mod Rheumatol 23:765–773. doi:10.1007/s10165-012-0735-5

    Article  PubMed  Google Scholar 

  9. Bultink IEM, Lems WF, Kostense PJ et al (2005) Prevalence of and risk factors for low bone mineral density and vertebral fractures in patients with systemic lupus erythematosus. Arthritis Rheum 52:2044–2050. doi:10.1002/art.21110

    Article  PubMed  Google Scholar 

  10. Almehed K, Hetenyi S, Ohlsson C et al (2010) Prevalence and risk factors of vertebral compression fractures in female SLE patients. Arthritis Res Ther 12:R153. doi:10.1186/ar3104

    Article  PubMed  PubMed Central  Google Scholar 

  11. Zhu T, Griffith J, Au S-K et al (2014) Incidence of and risk factors for non-vertebral and vertebral fracture in female Chinese patients with systemic lupus erythematosus: a five-year cohort study. Lupus. doi:10.1177/0961203314528555

    Google Scholar 

  12. Yeap SS, Fauzi AR, Kong NCT et al (2008) A comparison of calcium, calcitriol, and alendronate in corticosteroid-treated premenopausal patients with systemic lupus erythematosus. J Rheumatol 35:2344–2347. doi:10.3899/jrheum.080634

    Article  CAS  PubMed  Google Scholar 

  13. Seno T, Yamamoto A, Kukida Y et al (2016) Once-weekly teriparatide improves glucocorticoid-induced osteoporosis in patients with inadequate response to bisphosphonates. Springerplus 5:1056. doi:10.1186/s40064-016-2704-5

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sawamura M, Komatsuda A, Togashi M et al (2017) Effects of denosumab on bone metabolic markers and bone mineral density in patients treated with glucocorticoids. Intern Med 56:631–636. doi:10.2169/internalmedicine.56.7797

    Article  PubMed  PubMed Central  Google Scholar 

  15. Feng Z, Zeng S, Wang Y et al (2013) Bisphosphonates for the prevention and treatment of osteoporosis in patients with rheumatic diseases: a systematic review and meta-analysis. PLoS ONE 8:e80890. doi:10.1371/journal.pone.0080890

    Article  PubMed  PubMed Central  Google Scholar 

  16. Li EK, Zhu TY, Hung VY et al (2010) Ibandronate increases cortical bone density in patients with systemic lupus erythematosus on long-term glucocorticoid. Arthritis Res Ther 12:R198. doi:10.1186/ar3170

    Article  PubMed  PubMed Central  Google Scholar 

  17. Nzeusseu Toukap A, Depresseux G, Devogelaer J-P, Houssiau FA (2005) Oral pamidronate prevents high-dose glucocorticoid-induced lumbar spine bone loss in premenopausal connective tissue disease (mainly lupus) patients. Lupus 14:517–520. doi:10.1191/0961203305lu2149oa

    Article  CAS  PubMed  Google Scholar 

  18. Lambrinoudaki I, Chan DT, Lau CS et al (2000) Effect of calcitriol on bone mineral density in premenopausal Chinese women taking chronic steroid therapy. A randomized, double blind, placebo controlled study. J Rheumatol 27:1759–1765

    CAS  PubMed  Google Scholar 

  19. Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725. doi:10.1002/1529-0131(199709)40:9<1725:AID-ART29>3.0.CO;2-Y

    Article  CAS  PubMed  Google Scholar 

  20. Guzman J, Cardiel MH, Arce-Salinas A et al (1992) Measurement of disease activity in systemic lupus erythematosus. Prospective validation of 3 clinical indices. J Rheumatol 19:1551–1558

    CAS  PubMed  Google Scholar 

  21. Gladman D, Ginzler E, Goldsmith C et al (1996) The development and initial validation of the Systemic Lupus International Collaborating Clinics/American College of Rheumatology damage index for systemic lupus erythematosus. Arthritis Rheum 39:363–369

    Article  CAS  PubMed  Google Scholar 

  22. Holick MF (2007) Vitamin D deficiency. N Engl J Med 357:266–281. doi:10.1056/NEJMra070553

    Article  CAS  PubMed  Google Scholar 

  23. Schousboe JT, Shepherd JA, Bilezikian JP, Baim S (2013) Executive summary of the 2013 international society for clinical densitometry position development conference on bone densitometry. J Clin Densitom 16:455–466. doi:10.1016/j.jocd.2013.08.004

    Article  PubMed  Google Scholar 

  24. Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8:1137–1148. doi:10.1002/jbmr.5650080915

    Article  CAS  PubMed  Google Scholar 

  25. Felsenberg D, Silman AJ, Lunt M et al (2002) Incidence of vertebral fracture in europe: results from the European Prospective Osteoporosis Study (EPOS). J Bone Miner Res 17:716–724. doi:10.1359/jbmr.2002.17.4.716

    Article  CAS  PubMed  Google Scholar 

  26. Vis M, Haavardsholm EA, Bøyesen P et al (2011) High incidence of vertebral and non-vertebral fractures in the OSTRA cohort study: a 5-year follow-up study in postmenopausal women with rheumatoid arthritis. Osteoporos Int 22:2413–2419. doi:10.1007/s00198-010-1517-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Woo J, Li M, Lau E (2001) Population bone mineral density measurements for Chinese women and men in Hong Kong. Osteoporos Int 12:289–295. doi:10.1007/s001980170118

    Article  CAS  PubMed  Google Scholar 

  28. Xiaoge D, Eryuan L, Xianping W et al (2000) Bone mineral density differences at the femoral neck and Ward’s triangle: a comparison study on the reference data between Chinese and Caucasian women. Calcif Tissue Int 67:195–198

    Article  CAS  PubMed  Google Scholar 

  29. Walker MD, Babbar R, Opotowsky AR et al (2006) A referent bone mineral density database for Chinese American women. Osteoporos Int 17:878–887. doi:10.1007/s00198-005-0059-9

    Article  PubMed  Google Scholar 

  30. Xu L, Lu A, Zhao X et al (1996) Very low rates of hip fracture in Beijing, People’s Republic of China the Beijing Osteoporosis Project. Am J Epidemiol 144:901–907

    Article  CAS  PubMed  Google Scholar 

  31. Lauderdale DS, Jacobsen SJ, Furner SE et al (1997) Hip fracture incidence among elderly Asian-American populations. Am J Epidemiol 146:502–509

    Article  CAS  PubMed  Google Scholar 

  32. Lau EM, Chan HH, Woo J et al (1996) Normal ranges for vertebral height ratios and prevalence of vertebral fracture in Hong Kong Chinese: a comparison with American Caucasians. J Bone Miner Res 11:1364–1368. doi:10.1002/jbmr.5650110922

    Article  CAS  PubMed  Google Scholar 

  33. Barrett-Connor E, Siris ES, Wehren LE et al (2005) Osteoporosis and fracture risk in women of different ethnic groups. J Bone Miner Res 20:185–194. doi:10.1359/JBMR.041007

    Article  PubMed  Google Scholar 

  34. Lee C, Almagor O, Dunlop DD et al (2007) Association between African American race/ethnicity and low bone mineral density in women with systemic lupus erythematosus. Arthritis Rheum 57:585–592. doi:10.1002/art.22668

    Article  PubMed  Google Scholar 

  35. Cooper C, Atkinson EJ, O’Fallon WM, Melton LJ 3rd (1992) Incidence of clinically diagnosed vertebral fractures: a population-based study in Rochester, Minnesota, 1985–1989. J Bone Miner Res 7:221–227. doi:10.1002/jbmr.5650070214

    Article  CAS  PubMed  Google Scholar 

  36. Melton LJ 3rd, Lane AW, Cooper C et al (1993) Prevalence and incidence of vertebral deformities. Osteoporos Int 3:113–119

    Article  PubMed  Google Scholar 

  37. Briggs AM, Greig AM, Wark JD (2007) The vertebral fracture cascade in osteoporosis: a review of aetiopathogenesis. Osteoporos Int 18:575–584. doi:10.1007/s00198-006-0304-x

    Article  CAS  PubMed  Google Scholar 

  38. Almehed K, Hetényi S (2010) Prevalence and risk factors of vertebral compression fractures in female SLE patients. Arthritis Res Ther 12(4):153

    Article  Google Scholar 

  39. Stoll D, Dudler J, Lamy O et al (2011) High prevalence of hypovitaminosis D in a Swiss rheumatology outpatient population. Swiss Med Wkly 141:w13196. doi:10.4414/smw.2011.13196

    PubMed  Google Scholar 

  40. Mehat P, Atiquzzaman M, Esdaile JM et al (2017) Medication non-adherence in systemic lupus erythematosus: a systematic review. Arthritis Care Res (Hoboken). doi:10.1002/acr.23191

    Google Scholar 

  41. Angeli A, Guglielmi G, Dovio A et al (2006) High prevalence of asymptomatic vertebral fractures in post-menopausal women receiving chronic glucocorticoid therapy: a cross-sectional outpatient study. Bone 39:253–259. doi:10.1016/j.bone.2006.02.005

    Article  CAS  PubMed  Google Scholar 

  42. Van Staa TP, Laan RF, Barton IP et al (2003) Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 48:3224–3229. doi:10.1002/art.11283

    Article  PubMed  Google Scholar 

  43. Bultink IEM, Lems WF (2015) Systemic lupus erythematosus and fractures. RMD Open 1:e000069. doi:10.1136/rmdopen-2015-000069

    Article  PubMed  PubMed Central  Google Scholar 

  44. Lems WF, Jahangier ZN, Jacobs JW, Bijlsma JW (1995) Vertebral fractures in patients with rheumatoid arthritis treated with corticosteroids. Clin Exp Rheumatol 13:293–297

    CAS  PubMed  Google Scholar 

  45. de Nijs RN, Jacobs JW, Bijlsma JW et al (2001) Prevalence of vertebral deformities and symptomatic vertebral fractures in corticosteroid treated patients with rheumatoid arthritis. Rheumatology 40:1375–1383

    Article  PubMed  Google Scholar 

  46. Frediani B, Falsetti P, Bisogno S et al (2004) Effects of high dose methylprednisolone pulse therapy on bone mass and biochemical markers of bone metabolism in patients with active rheumatoid arthritis: a 12-month randomized prospective controlled study. J Rheumatol 31:1083–1087

    CAS  PubMed  Google Scholar 

  47. Bultink IEM (2012) Osteoporosis and fractures in systemic lupus erythematosus. Arthritis Care Res 64:2–8. doi:10.1002/acr.20568

    Article  Google Scholar 

  48. Schousboe JT, Fink HA, Taylor BC et al (2005) Association between self-reported prior wrist fractures and risk of subsequent hip and radiographic vertebral fractures in older women: a prospective study. J Bone Miner Res 20:100–106. doi:10.1359/JBMR.041025

    Article  PubMed  Google Scholar 

  49. Ismail AA, O’Neill TW, Cockerill W et al (2000) Validity of self-report of fractures: results from a prospective study in men and women across Europe. EPOS Study Group. European Prospective Osteoporosis Study Group. Osteoporos Int 11:248–254

    Article  CAS  PubMed  Google Scholar 

  50. Genant HK, Jergas M (2003) Assessment of prevalent and incident vertebral fractures in osteoporosis research. Osteoporos Int 14(Suppl 3):S43–S55. doi:10.1007/s00198-002-1348-1

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank all patients who participated in this study for their patience and understanding. We would like to thank David Buss for his valuable guidance and advice during this project. This work was in part supported by a grant from “Programa para el Desarrollo Profesional Docente, para el Tipo Superior” (SEP-PRODEP) “Integración de redes temáticas de colaboración académica”.

Funding

This work was supported in part by grant from FIS/IMSS/PROT/MD15/1500. This funding source had no role in the design and conduct of the study, in the collection, analysis, and interpretation of the data, or in the preparation, review, or approval of the manuscript.

Author information

Authors and Affiliations

  1. Systemic Autoimmune Diseases Research Unit, Hospital General Regional 36-CIBIOR, Instituto Mexicano del Seguro Social, Av. 10 Poniente 2721, Amor, 72090, Puebla, Puebla, Mexico

    Mario García-Carrasco, Claudia Mendoza-Pinto, María de la Luz León-Vázquez, Ivet Etchegaray-Morales & Pamela Soto-Santillán

  2. Department of Immunology and Rheumatology, Medicine School, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    Mario García-Carrasco & Claudia Mendoza-Pinto

  3. State Research Department, Instituto Mexicano del Seguro Social, Puebla, Mexico

    Socorro Méndez-Martínez

  4. Jefatura de División de Investigación en Salud, UMAE, Hospital de Traumatología, Instituto Mexicano del Seguro Social, Puebla, Puebla, Mexico

    Álvaro Montiel-Jarquín

  5. Cuerpo Académico de Facultad de Medicina, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    Miguel Angel Enriquez-Guerra

  6. Secretary of Research and Postgraduate Studies, Medicine School, Benemérita Universidad Autónoma de Puebla, Puebla, Mexico

    Margarita Muñóz-Guarneros

  7. Immunology Department, Hospital Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Puebla, Mexico

    José Luis Gálvez-Romero

  8. Department of Autoimmune Diseases, Hospital Clinic, Catalonia, Spain

    Ricard Cervera

Authors
  1. Mario García-Carrasco
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Claudia Mendoza-Pinto
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. María de la Luz León-Vázquez
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Socorro Méndez-Martínez
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Ivet Etchegaray-Morales
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Álvaro Montiel-Jarquín
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Miguel Angel Enriquez-Guerra
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Margarita Muñóz-Guarneros
    View author publications

    You can also search for this author inPubMed Google Scholar

  9. José Luis Gálvez-Romero
    View author publications

    You can also search for this author inPubMed Google Scholar

  10. Pamela Soto-Santillán
    View author publications

    You can also search for this author inPubMed Google Scholar

  11. Ricard Cervera
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Claudia Mendoza-Pinto.

Ethics declarations

Conflict of interest

Mario García-Carrasco, Claudia Mendoza-Pinto, María de la Luz León-Vázquez, Socorro Méndez-Martínez, Ivet Etchegaray-Morales, Álvaro Montiel-Jarquín, Miguel Angel Enriquez-Guerra, Margarita Muñóz-Guarneros, José Luis Gálvez-Romero, Pamela Soto-Santillán and Ricard Cervera declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

The study was reviewed and approved by our local institutional ethics committee. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the Helsinki declaration.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 120 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García-Carrasco, M., Mendoza-Pinto, C., León-Vázquez, M.d. et al. Incidence of Vertebral Fractures in Women with Systemic Lupus Erythematosus After 8 Years of Follow-Up. Calcif Tissue Int 101, 291–299 (2017). https://doi.org/10.1007/s00223-017-0286-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00223-017-0286-z

Keywords