Skip to main content

Advertisement

SpringerLink
Log in

Technical and clinical feasibility of contrast-enhanced ultrasound evaluation of long bone non-infected nonunion healing

  • MUSCULOSKELETAL RADIOLOGY
  • Published:
La radiologia medica Aims and scope Submit manuscript

Abstract

Purpose

To assess the technical feasibility of contrast-enhanced ultrasound (CEUS) in the monitoring of non-infected long bone nonunion healing.

Methods

Twenty-five patients (16 males; mean age: 40.4 ± 11.7) with long bone nonunion were treated using surgery and mesenchymal stem cells and platelet-rich plasma. They performed CEUS up to 15 days before, 7 days, 4 and 8 weeks after treatment. To categorize the angiogenesis around the fracture site, the microvascular blood flow from CEUS was classified into four categories, depending on the portion of the investigated area that was involved in the neovascularization process: grade 0 = 0%; grade 1 = 0–30%; grade 2 = 30–70%; grade 3 = 70–100%. Nonparametric Friedman and Wilcoxon statistics were used.

Results

Before treatment, neovascularization was graded as 0 in 15/25 patients, as 1 in 10/25. Vascularity significantly increased over time (P < 0.001), namely: 1 (25th–75th percentile = 1–2) at 7 days; 2 (1–2) at 4 weeks; 3 (0–2) at 8 weeks. All patients but one showed early progressive increase in neovascularization well identified with CEUS at the fracture site.

Conclusion

CEUS is a feasible method to monitor healing in patients with long bone nonunion.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Calori GM, Colombo M, Mazza EL et al (2014) Validation of the Non-Union Scoring System in 300 long bone non-unions. Injury 45(Suppl 6):S93–S97

    Article  PubMed  Google Scholar 

  2. Giannoudis PV, Einhorn TA, Schmidmaier G, Marsh D (2008) The diamond concept—open questions. Injury 39(Suppl 2):S5–S8

    Article  PubMed  Google Scholar 

  3. Muinos-López E, Ripalda-Cemboráin P et al (2016) Hypoxia and reactive oxygen species homeostasis in mesenchymal progenitor cells define a molecular mechanism for fracture nonunion. Stem Cells 34:2342–2353

    Article  PubMed  CAS  Google Scholar 

  4. Berner A, Reichert JC, Muller MB et al (2012) Treatment of long bone defects and non-unions: from research to clinical practice. Cell Tissue Res 347:501–519

    Article  PubMed  Google Scholar 

  5. Catapano M, Albano D, Pozzi G et al (2017) Differences between orthopaedic evaluation and radiological reports of conventional radiographs in patients with minor trauma admitted to the emergency department. Injury 48:2451–2456

    Article  PubMed  Google Scholar 

  6. Augat P, Morgan EF, Lujan TJ, MacGillivray TJ, Cheung WH (2014) Imaging techniques for the assessment of fracture repair. Injury 45(Suppl 2):S16–S22

    Article  PubMed  Google Scholar 

  7. Young JW, Kostrubiak IS, Resnik CS, Paley D (1990) Sonographic evaluation of bone production at the distraction site in Ilizarov limb-lengthening procedures. AJR Am J Roentgenol 154:125–128

    Article  PubMed  CAS  Google Scholar 

  8. Fischer C, Preuss EM, Tanner M et al (2016) Dynamic contrast-enhanced sonography and dynamic contrast-enhanced magnetic resonance imaging for preoperative diagnosis of infected nonunions. J Ultrasound Med 35:933–942

    Article  PubMed  Google Scholar 

  9. Silvestri E, Barile A, Albano D et al (2018) Interventional therapeutic procedures in the musculoskeletal system: an Italian Survey by the Italian College of Musculoskeletal Radiology. Radiol Med 123:314–321

    Article  PubMed  Google Scholar 

  10. Pountos I, Corscadden D, Emery P, Giannoudis PV (2007) Mesenchymal stem cell tissue engineering: techniques for isolation, expansion and application. Injury 38(Suppl 4):S23–S33

    Article  PubMed  Google Scholar 

  11. Prockop DJ (2009) Repair of tissues by adult stem/progenitor cells (MSCs): controversies, myths, and changing paradigms. Mol Ther 17:939–946

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Orlandi D, Corazza A, Arcidiacono A et al (2016) Ultrasound-guided procedures to treat sport-related muscle injuries. Br J Radiol 89:20150484

    Article  PubMed  Google Scholar 

  13. Ferrero G, Fabbro E, Orlandi D et al (2012) Ultrasound-guided injection of platelet-rich plasma in chronic Achilles and patellar tendinopathy. J Ultrasound 15:260–266

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Boswell SG, Cole BJ, Sundman EA, Karas V, Fortier LA (2012) Platelet rich plasma: a milieu of bioactive factors. Arthroscopy 28:429–439

    Article  PubMed  Google Scholar 

  15. deVos RJ, Weir A, Tol JL, Verhaar JA, Weinans H, van Schie HT (2011) No effects of PRP on ultrasonographic tendon structure and neovascularization in chronic midportion Achilles tendinopathy. Br J Sports Med 45:387–392

    Article  CAS  Google Scholar 

  16. Albano D, Messina C, Usuelli FG (2017) Magnetic resonance and ultrasound in Achilles tendinopathy: predictive role and response assessment to platelet-rich plasma and adipose-derived stromal vascular fraction injection. Eur J Radiol 95:130–135

    Article  PubMed  Google Scholar 

  17. Eppley BL, Woodell JE, Higgins J (2004) Platelet quantification and growth factor analysis from platelet-rich plasma: implications for wound healing. Plast Reconstr Surg 114:1502–1508

    Article  PubMed  Google Scholar 

  18. Albano D, Messina C, Usuelli FG et al (2017) Magnetic resonance and ultrasound in Achilles tendinopathy:predictive role and response assessment to platelet-rich plasma and adipose-derived stromal vascular fractioninjection. Eur J Radiol 95:130–135

    Article  PubMed  Google Scholar 

  19. De Marchi A, Pozza S, Sutera R et al (2011) Study of neurinomas with ultrasound contrast media: review of a case series to identify characteristic imaging patterns. Radiol Med 116:634–643

    Article  PubMed  Google Scholar 

  20. De Marchi A, Prever EB, Cavallo F et al (2015) Perfusion pattern and time of vascularisation with CEUS increase accuracy in differentiating between benign and malignant tumours in 216 musculoskeletal soft tissue masses. Eur J Radiol 84:142–150

    Article  PubMed  Google Scholar 

  21. Orlandi D, Gitto S, Perugin Bernardi S et al (2017) Advanced power doppler technique increases synovial vascularity detection in patients with rheumatoid arthritis. Ultrasound Med Biol 43:1880–1887

    Article  PubMed  Google Scholar 

  22. Burchardt H, Enneking WF (1978) Transplantation of bone. Surg Clin North Am 58:403–427

    Article  PubMed  CAS  Google Scholar 

  23. Hu K, Olsen BR (2016) The roles of vascular endothelial growth factor in bone repair and regeneration. Bone 91:30–38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Engin G, Yekeler E, Guloglu R, Acunas B, Acunas G (2000) US versus conventional radiology in the diagnosis of sternal fractures. Acta Radiol 41:296–299

    Article  PubMed  CAS  Google Scholar 

  25. Herneth AM, Siegmeth A, Bader TR et al (2001) Scaphoid fractures: evaluation with high-spatial-resolution US—initial results. Radiology 220:231–235

    Article  PubMed  CAS  Google Scholar 

  26. Sconfienza LM, Albano D, Allen G et al (2018) Clinical indications for musculoskeletal ultrasound updated in 2017 by European Society of Musculoskeletal Radiology (ESSR) consensus. Eur Radiol. https://doi.org/10.1007/s00330-018-5474-3

    Article  PubMed  Google Scholar 

  27. Hubner U, Schlicht W, Outzen S, Barthel M, Halsband H (2000) Ultrasound in the diagnosis of fractures in children. J Bone Jt Surg Br 82:1170–1173

    Article  CAS  Google Scholar 

  28. Craig JG, Jacobson JA, Moed BR (1999) Ultrasound of fracture and bone healing. Radiol Clin North Am 37:737–751

    Article  PubMed  CAS  Google Scholar 

  29. Sartoris R, Orlandi D, Corazza A et al (2017) In vivo feasibility of real-time MR–US fusion imaging lumbar facet joint injections. J Ultrasound 20:23–31

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

At the moment the work was conducted, Domenico Aloj was affiliated with the Department of Orthopedics and Traumatology, I Clinic, Azienda Ospedaliera Universitaria Città della Salute e della Scienza, CTO Hospital, Via Zuretti 29, 10126 Turin, Italy.

Author information

Authors and Affiliations

  1. Department of Imaging, Azienda Ospedaliera Universitaria Città della Salute e della Scienza, CTO Hospital, Via Zuretti 29, 10126, Turin, Italy

    Simona Pozza & Armanda De Marchi

  2. Department of Imaging, Ospedale Humanitas Gradenigo, C.so Regina Margherita 8, 10153, Turin, Italy

    Chiara Albertin

  3. Department of Radiology, Di.Bi.Med., University of Palermo, Via del Vespro 127, 90127, Palermo, Italy

    Domenico Albano

  4. Institute of Molecular Genetics, National Research Council of Italy, Via Ferrata, 27100, Pavia, Italy

    Ginevra Biino

  5. Department of Orthopedics and Traumatology, Sant’Andrea Hospital, C.so Abbiate 21, 13100, Vercelli, Italy

    Domenico Aloj

  6. Unit of Diagnostic and Interventional Radiology, IRCCS Istituto Ortopedico Galeazzi, Via R. Galeazzi 4, 20166, Milan, Italy

    Luca Maria Sconfienza

  7. Department of Biomedical Sciences for Health, University of Milano, Via Pascal 36, 20135, Milan, Italy

    Luca Maria Sconfienza

Authors
  1. Simona Pozza
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Armanda De Marchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chiara Albertin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Domenico Albano
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ginevra Biino
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Domenico Aloj
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Maria Sconfienza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Domenico Albano.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors. Institutional review board approval for retrospective publication of data was obtained, and patients’ informed consent was waived.

Informed consent

For this type of study, formal consent was waived.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pozza, S., De Marchi, A., Albertin, C. et al. Technical and clinical feasibility of contrast-enhanced ultrasound evaluation of long bone non-infected nonunion healing. Radiol med 123, 703–709 (2018). https://doi.org/10.1007/s11547-018-0902-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11547-018-0902-7

Keywords

Search

Navigation