Effects of low-intensity pulsed ultrasound on soft tissue micro-circulation in the foot

Abstract

Purpose

Low-intensity pulsed ultrasound (LIPUS) has been shown to accelerate bone healing and is considered to increase blood flow. The aim of this study was to assess changes in micro-circulation of the foots’ soft tissue in response to LIPUS intervention. We hypothesised improved micro-circulation in response to LIPUS.

Methods

Micro-circulation was assessed in 2 mm and 8 mm-deep skin of 50 healthy volunteers using non-invasive laser-doppler spectrophotometry (O2C-device). Measurements were performed before LIPUS-intervention (pre), directly after intervention (post) and 20, 40 and 60 minutes after LIPUS.

Results

All parameter of micro-circulation increased directly after LIPUS intervention at 8 mm depth. Participants with a low pre-intervention flow showed the largest changes (p < 0.001) with an increased post-flow of 38%. SO2 levels increased significantly after intervention (p = 0.045) and decreased after 60 minutes in comparison to pre-intervention status. rHb levels after 60 min were significantly higher in comparison to pre-intervention levels.

Conclusion

In healthy volunteers, low-intensity pulsed ultrasound led to significant short-term changes in microcirculation of the foot. Younger subjects with a low pre-flow level and smokers showed a higher potential to increase blood flow after LIPUS.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Shakked RJ, Tejwani NC (2013) Surgical treatment of talus fractures. Orthop Clin North Am 44(4):521–528

    Article  PubMed  Google Scholar 

  2. 2.

    Hopf HW, Hunt TK, West JM, Blomquist P, Goodson WH 3rd, Jensen JA, Jonsson K, Paty PB, Rabkin JM, Upton RA, von Smitten K, Whitney JD (1997) Wound tissue oxygen tension predicts the risk of wound infection in surgical patients. Arch Surg 132(9):997–1004 discussion 1005

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Haliburton RA, Sullivan CR, Kelly PJ, Peterson LF (1958) The extra-osseous and intra-osseous blood supply of the talus. J Bone Joint Surg Am 40-A(5):1115–1120

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Cicco G, Giorgino F, Cicco S (2011) Wound healing in diabetes: hemorheological and microcirculatory aspects. Adv Exp Med Biol 701:263–269

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Arya AK, Tripathi R, Kumar S, Tripathi K (2014) Recent advances on the association of apoptosis in chronic non healing diabetic wound. World J Diabetes 5(6):756–762

    Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Rutten S, Nolte PA, Korstjens CM, van Duin MA, Klein-Nulend J (2008) Low-intensity pulsed ultrasound increases bone volume, osteoid thickness and mineral apposition rate in the area of fracture healing in patients with a delayed union of the osteotomized fibula. Bone 43(2):348–354

    Article  PubMed  Google Scholar 

  7. 7.

    Heckman JD, Ryaby JP, McCabe J, Frey JJ, Kilcoyne RF (1994) Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J Bone Joint Surg Am 76(1):26–34

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Cook SD, Ryaby JP, McCabe J, Frey JJ, Heckman JD, Kristiansen TK (1997) Acceleration of tibia and distal radius fracture healing in patients who smoke. Clin Orthop Relat Res 337:198–207

    Article  Google Scholar 

  9. 9.

    Busse JW, Kaur J, Mollon B, Bhandari M, Tornetta P 3rd, Schunemann HJ, Guyatt GH (2009) Low intensity pulsed ultrasonography for fractures: systematic review of randomised controlled trials. BMJ 338:b351

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Watanabe Y, Matsushita T, Bhandari M, Zdero R, Schemitsch EH (2010) Ultrasound for fracture healing: current evidence. J Orthop Trauma 24(Suppl 1):S56–S61

    Article  PubMed  Google Scholar 

  11. 11.

    Salem KH, Schmelz A (2014) Low-intensity pulsed ultrasound shortens the treatment time in tibial distraction osteogenesis. Int Orthop 38(7):1477–1482

    Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Toyama Y, Sasaki K, Tachibana K, Ueno T, Kajimoto H, Yokoyama S, Ohtsuka M, Koiwaya H, Nakayoshi T, Mitsutake Y, Chibana H, Itaya N, Imaizumi T (2012) Ultrasound stimulation restores impaired neovascularization-related capacities of human circulating angiogenic cells. Cardiovasc Res 95(4):448–459

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Coords M, Breitbart E, Paglia D, Kappy N, Gandhi A, Cottrell J, Cedeno N, Pounder N, O'Connor JP, Lin SS (2011) The effects of low-intensity pulsed ultrasound upon diabetic fracture healing. J Orthop Res 29(2):181–188

    Article  PubMed  Google Scholar 

  14. 14.

    Zhou S, Schmelz A, Seufferlein T, Li Y, Zhao J, Bachem MG (2004) Molecular mechanisms of low intensity pulsed ultrasound in human skin fibroblasts. J Biol Chem 279(52):54463–54469

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Biglari B, Yildirim TM, Swing T, Bruckner T, Danner W, Moghaddam A (2016) Failed treatment of long bone nonunions with low intensity pulsed ultrasound. Arch Orthop Trauma Surg 136(8):1121–1134

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Rutten S, van den Bekerom MP, Sierevelt IN, Nolte PA (2016) Enhancement of bone-healing by low-intensity pulsed ultrasound: a systematic review. JBJS Rev 29:4(3)

    Google Scholar 

  17. 17.

    Poolman RW, Agoritsas T, Siemieniuk RA, Harris IA, Schipper IB, Mollon B, Smith M, Albin A, Nador S, Sasges W, Schandelmaier S, Lytvyn L, Kuijpers T, van Beers LW, Verhofstad MH, Vandvik PO (2017) Low intensity pulsed ultrasound (LIPUS) for bone healing: a clinical practice guideline. BMJ 356:j576

    Article  PubMed  Google Scholar 

  18. 18.

    Aleem IS, Bhandari M (2016) Cochrane in CORR ((R)): ultrasound and shockwave therapy for acute fractures in adults (review). Clin Orthop Relat Res 474(7):1553–1559

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Krug A (2006) CME: Mikrozirkulation und Sauerstoffversorgung des Gewebes-Methode des sogenannten O2C (oxygen to see). Phlebologie 6(277-336):300–312

  20. 20.

    Beckert S, Witte MB, Konigsrainer A, Coerper S (2004) The impact of the micro-Lightguide O2C for the quantification of tissue ischemia in diabetic foot ulcers. Diabetes Care 27(12):2863–2867

    Article  PubMed  Google Scholar 

  21. 21.

    Pastor T, Gradl G, Klos K, Ganse B, Horst K, Andruszkow H, Hildebrand F, Pape HC, Knobe M (2016) Displaced intra-articular calcaneal fractures: is there a consensus on treatment in Germany? Int Orthop 40(10):2181–2190

    Article  PubMed  Google Scholar 

  22. 22.

    Thorn CE, Kyte H, Slaff DW, Shore AC (2011) An association between vasomotion and oxygen extraction. Am J Physiol Heart Circ Physiol 301(2):H442–H449

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Pfander D, Cramer T, Swoboda B (2005) Hypoxia and HIF-1alpha in osteoarthritis. Int Orthop 29(1):6–9

    Article  PubMed  Google Scholar 

  24. 24.

    Gassmann M, Muckenthaler MU (2015) Adaptation of iron requirement to hypoxic conditions at high altitude. J Appl Physiol 119(12):1432–1440

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Park DH, Hwang JW, Jang KS, Han DG, Ahn KY (1997) Mapping of the human body skin with laser Doppler flowmetry. Ann Plast Surg 39(6):597–602

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Gardner AW, Montgomery PS, Blevins SM, Parker DE (2010) Gender and ethnic differences in arterial compliance in patients with intermittent claudication. J Vasc Surg 51(3):610–615

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Khanna A, Nelmes RT, Gougoulias N, Maffulli N, Gray J (2009) The effects of LIPUS on soft-tissue healing: a review of literature. Br Med Bull 89:169–182

    Article  PubMed  Google Scholar 

  28. 28.

    Meidinger G, Imhoff AB, Paul J, Kirchhoff C, Sauerschnig M, Hinterwimmer S (2011) May smokers and overweight patients be treated with a medial open-wedge HTO? Risk factors for non-union. Knee Surg Sports Traumatol Arthrosc 19(3):333–339

    Article  PubMed  Google Scholar 

  29. 29.

    Diesen DL, Hess DT, Stamler JS (2008) Hypoxic vasodilation by red blood cells: evidence for an snitrosothiol-based signal. Circ Res 103(5):545–553

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We would like to thank Daniel Timo Behrens for his consultation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Matthias Knobe.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

None.

Ethical approval

Ethics committee of the RWTH Aachen University Hospital, ethics approval EK 346/14.

Informed consent

Each author certifies that his or her institution approved the human protocol for this investigation, that all investigations were conducted in conformity with the ethical principles of research, and that informed consent for participation in the study was obtained.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kösters, A.K., Ganse, B., Gueorguiev, B. et al. Effects of low-intensity pulsed ultrasound on soft tissue micro-circulation in the foot. International Orthopaedics (SICOT) 41, 2067–2074 (2017). https://doi.org/10.1007/s00264-017-3574-3

Download citation

Keywords

  • Low-intensity pulsed ultrasound
  • O2C
  • Micro-circulation
  • Blood flow
  • Soft tissue
  • Hindfoot