International Orthopaedics

, Volume 41, Issue 10, pp 2067–2074 | Cite as

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

  • Anna Katharina Kösters
  • Bergita Ganse
  • Boyko Gueorguiev
  • Kajetan Klos
  • Ali Modabber
  • Sven Nebelung
  • Bong-Sung S. Kim
  • Matthias KnobeEmail author
Original Paper



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.


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.


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.


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.


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



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

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.



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.


  1. 1.
    Shakked RJ, Tejwani NC (2013) Surgical treatment of talus fractures. Orthop Clin North Am 44(4):521–528CrossRefPubMedGoogle 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 1005CrossRefPubMedGoogle 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):1115–1120CrossRefPubMedGoogle Scholar
  4. 4.
    Cicco G, Giorgino F, Cicco S (2011) Wound healing in diabetes: hemorheological and microcirculatory aspects. Adv Exp Med Biol 701:263–269CrossRefPubMedGoogle 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):756–762CrossRefPubMedPubMedCentralGoogle 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):348–354CrossRefPubMedGoogle 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):26–34CrossRefPubMedGoogle 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 337:198–207CrossRefGoogle 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:b351CrossRefPubMedPubMedCentralGoogle 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–S61CrossRefPubMedGoogle Scholar
  11. 11.
    Salem KH, Schmelz A (2014) Low-intensity pulsed ultrasound shortens the treatment time in tibial distraction osteogenesis. Int Orthop 38(7):1477–1482CrossRefPubMedPubMedCentralGoogle 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):448–459CrossRefPubMedGoogle 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):181–188CrossRefPubMedGoogle 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):54463–54469CrossRefPubMedGoogle 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):1121–1134CrossRefPubMedPubMedCentralGoogle 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:j576CrossRefPubMedGoogle 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):1553–1559CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Krug A (2006) CME: Mikrozirkulation und Sauerstoffversorgung des Gewebes-Methode des sogenannten O2C (oxygen to see). Phlebologie 6(277-336):300–312Google Scholar
  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):2863–2867CrossRefPubMedGoogle 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):2181–2190CrossRefPubMedGoogle 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–H449CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Pfander D, Cramer T, Swoboda B (2005) Hypoxia and HIF-1alpha in osteoarthritis. Int Orthop 29(1):6–9CrossRefPubMedGoogle Scholar
  24. 24.
    Gassmann M, Muckenthaler MU (2015) Adaptation of iron requirement to hypoxic conditions at high altitude. J Appl Physiol 119(12):1432–1440CrossRefPubMedGoogle 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):597–602CrossRefPubMedGoogle 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):610–615CrossRefPubMedPubMedCentralGoogle 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 89:169–182CrossRefPubMedGoogle 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):333–339CrossRefPubMedGoogle 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):545–553CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© SICOT aisbl 2017

Authors and Affiliations

  1. 1.Department of Orthopaedic TraumaUniversity of Aachen Medical CenterAachenGermany
  2. 2.AO Research Institute DavosDavosSwitzerland
  3. 3.Department of Foot and Ankle SurgeryCatholic Hospital MainzMainzGermany
  4. 4.Department of Oral and Maxillofacial SurgeryUniversity of Aachen Medical CenterAachenGermany
  5. 5.Department of RadiologyUniversity of Aachen Medical CenterAachenGermany
  6. 6.Department of Plastic Surgery, Reconstructive and Hand SurgeryUniversity of Aachen Medical CenterAachenGermany

Personalised recommendations