Pitfalls in the study of neovascularisation in achilles and patellar tendinopathy: a review of important factors for clinicians to consider and the need for greater standardisation

References

• Rubin J, Bude R, Carson P, et al. Power Doppler: a potentially useful alterative to mean-frequency based colour Doppler sonography. Radiology 1994;190:853–856.
   PubMed Web of Science ®Google Scholar
• Newman J, Laing T, McCarthy C, et al. Power Doppler sonography of synovitis: assessment of therapeutic response: preliminary observations. Radiology 1996;198:582–584.
   PubMed Web of Science ®Google Scholar
• Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc. 2001;9:233–238.
   PubMed Web of Science ®Google Scholar
• Welsh A. Quantification of power Doppler and the index ‘fractional moving blood volume’ (FMBV). Ultrasound Obstet Gynecol. 2004;23:323–326.
   PubMed Web of Science ®Google Scholar
• Yang X, Pugh ND, Coleman DP, et al. Are Doppler studies a useful method of assessing neovascularization in human Achilles tendinopathy? A systematic review and suggestions for optimizing machine settings. J Med Eng Technol. 2010;34:365–372.
   PubMedGoogle Scholar
• Torp-Pedersen S, Christensen R, Szkudlarek M, et al. Power and colour Doppler ultrasound settings for inflammatory flow. Arthritis Rheum. 2015;65:386–395.
   Google Scholar
• Fox R. Optimization of a digital clutter filter for microvascular volume quantification using power doppler ultrasound. London, ON: Department of Medical Biophysics, Western University; 2012.
   Google Scholar
• Cook JL, Rio E, Purdam CR, et al. Revisiting the continuum model of tendon pathology: what is its merit in clinical practice and research? Br J Sports Med. 2016;50:1187–1191.
   PubMed Web of Science ®Google Scholar
• Morrey M, Dean B, Carr A, et al. Tendinopathy: Same disease different results — why? Oper Tech Orthop. 2013;23:39–49.
   Google Scholar
• Bushberg J, Seibert J, Leidholdt E, et al. The essential physics of medical imaging. 3rd ed. Baltimore, MD: Lippincott, Williams and Wilkins; 2012.
   Google Scholar
• Woo J. A short history of the development of ultrasound in obstetrics and gynaecology. Available from: http://www.ob-ultrasound.net/history1.html.
   Google Scholar
• Weskott HP. Amplitude Doppler US: slow blood flow detection tested with a flow phantom. Radiology 1997;202:125–130.
   PubMed Web of Science ®Google Scholar
• Albrecht K, Grob K, Lange U, et al. Reliability of different Doppler ultrasound quantification methods and devices in the assessment of therapeutic response in arthritis. Rheumatology 2008;47:1521–1526.
   PubMed Web of Science ®Google Scholar
• Browne J, Watson AJ, Hoskins PR, et al. Validation of a sensitivity performance index test protocol and evaluation of colour Doppler sensitivity for a range of ultrasound scanners. Ultrasound Med Biol. 2004;30:1475–1483.
   PubMed Web of Science ®Google Scholar
• Deane C. Doppler ultrasound: principles and practice. Available from: https://sonoworld.com/Client/Fetus/html/doppler/capitulos-html/chapter_01.htm.
   Google Scholar
• Boesen M, Boesen A, Koenig M, et al. Ultrasonographic investigation of the Achilles tendon in elite badminton players using color Doppler. Am J Sports Med. 2006;34:2013–2021.
   PubMed Web of Science ®Google Scholar
• Reiter M, Ulreich N, Dirisamer A, et al. Colour and power Doppler sonography in symptomatic Achilles tendon disease. Int J Sports Med. 2004;25:301–305.
   PubMed Web of Science ®Google Scholar
• Malliaras P, Richards P, Garau G, et al. Achilles tendon Doppler flow may be associated with mechanical loading among active athletes. Am J Sports Med. 2008;36:2210–2215.
   PubMed Web of Science ®Google Scholar
• Ooi CC, Schneider ME, Malliaras P, et al. Prevalence of morphological and mechanical stiffness alterations of mid Achilles tendons in asymptomatic marathon runners before and after a competition. Skeletal Radiol. 2015;44:1119–1127.
   PubMed Web of Science ®Google Scholar
• Ohberg L, Alfredson H. Ultrasound guided sclerosis of neovessels in painful chronic Achilles tendinosis: pilot study of a new treatment. Br J Sports Med. 2002;36:173–175.
   PubMed Web of Science ®Google Scholar
• Sengkerij P, Vos R, de Weir A, et al. Interobserver reliability of neovascularization score using power Doppler ultrasonography in midportion Achilles tendinopathy. Am J Sports Med. 2009;37:1627–1631.
   PubMed Web of Science ®Google Scholar
• Watson J, Barker-Davies RM, Bennett AN, et al. Sport and exercise medicine consultants are reliable in assessing tendon neovascularity using ultrasound Doppler. BMJ Open Sport Exerc Med. 2018;4:e000298.
   PubMedGoogle Scholar
• Boesen M, Koenig M, Torp-Pedersen S, et al. Tendinopathy and Doppler activity: the vascular response of the Achilles tendon to exercise. Scand J Med Sci Sports. 2006;16:463–469.
   PubMed Web of Science ®Google Scholar
• Peers K, Brys P, Lysens R. Correlation between power Doppler ultrasonography and clinical severity in Achilles tendinopathy. Int Orthop. 2003;27:180–183.
   PubMed Web of Science ®Google Scholar
• Malliaras P, Purdam C, Maffulli N, et al. Temporal sequence of greyscale ultrasound changes and their relationship with neovascularity and pain in the patellar tendon. Br J Sports Med. 2010;44:944–947.
   PubMed Web of Science ®Google Scholar
• Cook JL, Malliaras P, De Luca J, et al. Vascularity and pain in the patellar tendon of adult jumping athletes: a 5 month longitudinal study. Br J Sports Med. 2005;39:458–461.
   PubMed Web of Science ®Google Scholar
• Alfredson H, Ohberg L. Sclerosing injections to areas of neo-vascularisation reduce pain in chronic Achilles tendinopathy: a double-blind randomised controlled trial. Knee Surg Sports Traumatol Arthrosc. 2005;13:338–344.
   PubMed Web of Science ®Google Scholar
• Bakkegaard M, Johannsen FE, Højgaard B, et al. Ultrasonography as a prognostic and objective parameter in Achilles tendinopathy: a prospective observational study. Eur J Radiol. 2015;84:458–462.
   PubMed Web of Science ®Google Scholar
• Beyer R, Kongsgaard M, Hougs Kjaer B, et al. Heavy slow resistance versus eccentric training as treatment for Achilles tendinopathy: A randomised controlled trial. Am J Sports Med. 2015;43:1704–1711.
   PubMed Web of Science ®Google Scholar
• Bode G, Hammer T, Karvouniaris N, et al. Patellar tendinopathy in young elite soccer-clinical and sonographical analysis of a German elite soccer academy. BMC Musculoskelet Disord. 2017;18:344–350.
   PubMed Web of Science ®Google Scholar
• Boesen A, Boesen M, Torp-Pedersen S, et al. Associations between abnormal ultrasound color Doppler measures and tendon pain symptoms in badminton players during a season: a prospective cohort study. Am J Sports Med. 2012;40:548–555.
   PubMed Web of Science ®Google Scholar
• Cassel M, Baur H, Hirschmüller A, et al. Prevalence of Achilles and patellar tendinopathy and their association to intratendinous changes in adolescent athletes. Scand J Med Sci Sports. 2015;25:e310–e318.
   PubMed Web of Science ®Google Scholar
• Comin J, Cook JL, Malliaras P, et al. The prevalence and clinical significance of sonographic tendon abnormalities in asymptomatic ballet dancers: a 24-month longitudinal study. Br J Sports Med. 2013;47:89–92.
   PubMed Web of Science ®Google Scholar
• Cook JL, Malliaras P, De Luca J, et al. Neovascularization and pain in abnormal patellar tendons of active jumping athletes. Clin J Sport Med. 2004;14:296–299.
   PubMed Web of Science ®Google Scholar
• Divani K, Chan O, Padhiar N, et al. Site of maximum neovascularisation correlates with the site of pain in recalcitrant mid-tendon Achilles tendinopathy. Manual Therapy. 2010;15:463–468.
   PubMed Web of Science ®Google Scholar
• Giombini A, Dragoni S, Di Cesare A, et al. Asymptomatic Achilles, patellar, and quadriceps tendinopathy: a longitudinal clinical and ultrasonographic study in elite fencers. Scand J Med Sci Sports. 2013;23:311–316.
   PubMed Web of Science ®Google Scholar
• Gisslen K, Alfredson H. Neovascularisation and pain in jumper’s knee: a prospective clinical and sonographic study in elite junior volleyball players. Br J Sports Med. 2005;39:423–428.
   PubMed Web of Science ®Google Scholar
• Jhingan S, Perry M, O'Driscoll G, et al. Thicker Achilles tendons are a risk factor to develop Achilles tendinopathy in elite professional soccer players. Muscles, Ligaments Tendons J. 2011;1:51–56.
   PubMedGoogle Scholar
• de Jonge S, de Vos RJ, Weir A, et al. One-year follow-up of platelet-rich plasma treatment in chronic Achilles tendinopathy: A double-blind randomized placebo-controlled trial. Am J Sports Med. 2011;39:1623–1629.
   PubMed Web of Science ®Google Scholar
• de Jonge S, de Vos RJ, Van Schie HTM, et al. One-year follow-up of a randomised controlled trial on added splinting to eccentric exercises in chronic midportion Achilles tendinopathy. Br J Sports Med. 2010;44:673–677.
   PubMed Web of Science ®Google Scholar
• Khan KM, Forster BB, Robinson J, et al. Are ultrasound and magnetic resonance imaging of value in assessment of Achilles tendon disorders? A two year prospective study. Br J Sports Med. 2003;37:149–153.
   PubMed Web of Science ®Google Scholar
• Lind B, Öhberg L, Alfredson H. Sclerosing polidocanol injections in mid-portion Achilles tendinosis: remaining good clinical results and decreased tendon thickness at 2-year follow-up. Knee Surg Sports Traumatol Arthrosc. 2006;14:1327–1332.
   PubMed Web of Science ®Google Scholar
• Mahieu N, Van Tiggelen D, De Muynck M, et al. Blood flow of the Achilles tendon during military training. Int J Sports Med. 2010;31:901–905.
   PubMed Web of Science ®Google Scholar
• Malliaras P, Chan O, Simran G, et al. Doppler ultrasound signal in achilles tendinopathy reduces immediately after activity. Int J Sports Med. 2012;33:480–484.
   PubMed Web of Science ®Google Scholar
• Ram R, Meeuwisse W, Patel C, et al. The limited effectiveness of a home-based eccentric training for treatment of Achilles tendinopathy. Clin Invest Med. 2013;36:197–E206.
   Web of Science ®Google Scholar
• Sunding K, Fahlström M, Werner S, et al. Evaluation of Achilles and patellar tendinopathy with greyscale ultrasound and colour Doppler: using a four-grade scale. Knee Surg Sports Traumatol Arthrosc. 2016;24:1988–1996.
   PubMed Web of Science ®Google Scholar
• van Snellenberg W, Wiley J, Brunet G. Achilles tendon pain intensity and level of neovascularization in athletes as determined by color Doppler ultrasound. Scand J Med Sci Sports. 2007;17:530–534.
   PubMed Web of Science ®Google Scholar
• Visnes H, Tegnander A, Bahr R. Ultrasound characteristics of the patellar and quadriceps tendons among young elite athletes. Scand J Med Sci Sports. 2015;25:205–215.
   PubMed Web of Science ®Google Scholar
• de Vos RJ, Weir A, Cobben LPJ, et al. The value of power Doppler ultrasonography in Achilles tendinopathy. Am J Sports Med. 2007;35:1696–1701.
   PubMed Web of Science ®Google Scholar
• de Vos RJ, Weir A, Tol JL, e al. No effects of PRP on ultrasonographic tendon structure and neovascularisation in chronic midportion Achilles tendinopathy. Br J Sports Med. 2011;45:387–392.
   PubMed Web of Science ®Google Scholar
• Yang X, Coleman DP, Pugh ND, et al. The volume of the neovascularity and its clinical implications in achilles tendinopathy. Ultrasound Med Biol. 2012;38:1887–1895.
   PubMed Web of Science ®Google Scholar
• Zanetti M, Metzdorf A, Kundert HP, et al. Achilles tendons: clinical relevance of neovascularization diagnosed with power Doppler US. Radiology 2003;227:556–560.
   PubMed Web of Science ®Google Scholar
• Raine-Fenning N, Nordin N, Ramnaine K, et al. Evaluation of the effect of machine settings on quantitative three- dimensional power Doppler angiography: an in-vitro flow phantom experiment. Ultrasound Obstet Gynecol. 2008;32:551–559.
   PubMed Web of Science ®Google Scholar
• Martins W, Raine-Fenning N, Ferriani R, et al. Quantitative three-dimensional power Doppler angiography: a flow-free phantom experiment to evaluate the relationship between color gain, depth and signal artefact. Ultrasound Obstet Gynecol. 2010;35:361–368.
   PubMed Web of Science ®Google Scholar
• Torp-Pedersen ST, Terslev L. Settings and artefacts relevant in colour/power Doppler ultrasound in rheumatology. Ann Rheum Dis. 2008;67:143–149.
   PubMed Web of Science ®Google Scholar
• Theobald P, Benjamin M, Nokes L, et al. Review of the vascularisation of the human Achilles tendon. Injury 2005;36:1267–1272.
   PubMed Web of Science ®Google Scholar
• Ten Cate D, Luime J, Ven M, et al. Very different performance of the power Doppler modalities of several ultrasound machines ascertained by a microvessel flow phantom. Arthritis Res Ther. 2013;15:R162.
   PubMed Web of Science ®Google Scholar
• Browne J. Review of currently available Doppler test devices and what information regarding Doppler performance they provide. Phys Medica. 2013;29:574.
   Google Scholar
• de Vos RJ, Weir A, Visser R, et al. The additional value of a night splint to eccentric exercises in chronic midportion Achilles tendinopathy: a randomised controlled trial. Br J Sports Med. 2007;41:e5.
   PubMed Web of Science ®Google Scholar
• Koenig M, Torp-Pedersen S, Holmich P, et al. Ultrasound Doppler of the Achilles tendon before and after injection of an ultrasound contrast agent-findings in asymptomatic subjects. Ultraschall in Med. 2007;28:52–56.
   PubMed Web of Science ®Google Scholar
• Joshua F, De Carle R, Rayment M, et al. Power Doppler ‘blanching’ after the application of transducer pressure. Australas Radiol. 2005;49:218–221.
   PubMedGoogle Scholar
• Strunk J, Müller-Ladner U. Rheumatoid arthritis: Doppler ultrasonography for assessment: Doppler ultrasonography. Available from: http://www.medscape.org/viewarticle/736708_8.
   Google Scholar
• Knobloch K, Grasemann R, Spies M, et al. Midportion Achilles tendon microcirculation after intermittent combined cryotherapy and compression compared with cryotherapy alone a randomized trial. Am J Sports Med. 2008;36:2128–2138.
   PubMed Web of Science ®Google Scholar
• Kubo K, Ikebukuro T. Blood circulation of patellar and Achilles tendons during contractions and heating. Med Sci Sports Exer. 2012;44:2111–2117.
   PubMed Web of Science ®Google Scholar
• Kubo K, Yajima H, Takayama M, et al. Effects of acupuncture and heating on blood volume and oxygen saturation of human Achilles tendon in vivo. Eur J Appl Physiol. 2010;109:545–550.
   PubMed Web of Science ®Google Scholar
• Kubo K, Yajima H, Takayama M, et al. Changes in blood circulation of the contralateral Achilles tendon during and after acupuncture and heating. Int J Sports Med. 2011;32:807–813.
   PubMed Web of Science ®Google Scholar
• Chang K, Wu C, Ding Y, et al. Application of contrast-enhanced sonography with time-intensity curve analysis to explore hypervascularity in achilles tendinopathy by using a rabbit model. J Ultras Med. 2012;31:737–746.
   PubMed Web of Science ®Google Scholar
• Notarnicola A, Fischetti F, Gallone D, et al. Overload and neovascularization of shoulder tendons in volleyball players. BMC Res Notes. 2012;5:397.
   PubMedGoogle Scholar
• Shen H, Chen S, Wu C, et al. Contrast-enhanced sonography for the evaluation of neovascularization in tendinopathic tissues. J Med Ultrasound. 2012;20:109–114.
   Google Scholar
• Boesen A, Boesen M, Koenig M, et al. Evidence of accumulated stress in Achilles and anterior knee tendons in elite badminton players. Knee Surg Sports Traumatol Arthrosc. 2011;19:30–37.
   PubMed Web of Science ®Google Scholar
• Knobloch K, Kraemer R, Jagodzinski M, et al. Eccentric training decreases paratendon capillary blood flow and preserves paratendon oxygen saturation in chronic Achilles tendinopathy. J Orthop Sports Phys Ther. 2007;37:269–276.
   PubMed Web of Science ®Google Scholar
• Knobloch K. The role of tendon microcirculation in Achilles and patellar tendinopathy. J Orthop Surg Res. 2008;18:106–108.
   Google Scholar
• Hirschmuller A, Frey V, Deibert P, et al. Achilles tendon power Doppler sonography in 953 long distance runners-a cross sectional study. Ultraschall Med. 2010;31:387.
   PubMed Web of Science ®Google Scholar
• Hirschmuller A, Frey V, Deibert P, et al. Prognostic value of Achilles tendon Doppler sonography in asymptomatic runners. Am J Sports Med. 2012;44:199–205.
   Google Scholar
• Astrom M, Westlin N. Blood flow in the human Achilles tendon assessed by laser Doppler flowmetry. J Orthop Res. 1994;12:246–252.
   PubMed Web of Science ®Google Scholar
• Knobloch K, Schreibmueller L, Meller R, et al. Superior Achilles tendon microcirculation in tendinopathy among symptomatic female versus male patients. Am J Sports Med. 2008;36:509–514.
   PubMed Web of Science ®Google Scholar
• Davies M, Bland J, Hangartner J, et al. Factors influencing the presence or absence of acute coronary artery thrombi in sudden ischaemic death. Eur Heart J. 1989;10:203–208.
   PubMed Web of Science ®Google Scholar
• Zhang J, Ying X, Lu Q, et al. A single high dose of vitamin C counteracts the acute negative effect on microcirculation induced by smoking a cigarette. Microvasc Res. 1999;58:305–311.
   PubMed Web of Science ®Google Scholar
• Song E, Rowe S, Chung J, et al. Failure of osteointegration of hamstring tendon autograft after anterior cruciate ligament reconstruction. Arthroscopy 2004;20:424–428.
   PubMed Web of Science ®Google Scholar
• Moller A, Pedersen T, Villebro N, et al. Effect of smoking on early complications after elective orthopaedic surgery. J Bone Joint Surg Br. 2003;85-B:178–181.
   Google Scholar
• Siafaka A, Angelopoulos E, Kritikos K, et al. Acute effects of smoking on skeletal muscle microcirculation monitored by near-infrared spectroscopy. Chest 2007;131:1479–1485.
   PubMed Web of Science ®Google Scholar
• Neunteufl T, Priglinger U, Heher S, et al. Effects of vitamin E on chronic and acute endothelial dysfunction in smokers. J Am Coll Cardiol. 2000;35:277–283.
   PubMed Web of Science ®Google Scholar
• Richardson RS, Donato AJ, Uberoi, et al. Exercise induced brachial artery vasodilation: role of free radicals. Am J Physiol. 2007;292:H1516–H1522.
   Google Scholar
• Vogel RA, Corretti MC, Plotnick GD, et al. Effect of a single high fat meal on endothelial function in healthy subjects. Am J Cardiol. 1997;79:350–354.
   PubMed Web of Science ®Google Scholar
• Tsutsui M, Noguchi K, Matsuzaki T, et al. Caffeine contained in a cup of coffee ameliorates microvascular endothelial function in healthy subjects. In: American Heart Association Scientific Sessions 2013, Session APS.714.01 Peripheral Vascular Disease: Metabolic Disorders; 2013 November 16–17; Dallas: American Heart Association; 2013.
   Google Scholar
• Neukam K, Stahl W, Tronnier H, et al. Consumption of flavanol-rich cocoa acutely increases microcirculation in human skin. Eur J Nutr. 2007;46:53–56.
   PubMed Web of Science ®Google Scholar
• Weis M, Heeschen C, Glassford A, et al. Statins have biphasic effects on angiogenesis. Circulation. 2002;105:739–745.
   PubMed Web of Science ®Google Scholar
• Tol J, Spiezia F, Maffulli N. Neovascularization in Achilles tendinopathy: have we been chasing a red herring? Knee Surg Sports Traumatol Arthrosc. 2012;20:1891–1894.
   PubMedGoogle Scholar
• Abboud J, Beason D, Soslowsky L. Emerging ideas: the effect of hypercholesterolemia on tendons. Clin Orthop Relat Res. 2012;470:317–320.
   PubMed Web of Science ®Google Scholar
• Ozgurtas T, Yildiz C, Serdar M, et al. Is high concentration of serum lipids a risk factor for Achilles tendon rupture? Clinica Chimica Acta. 2003;331:25–28.
   PubMed Web of Science ®Google Scholar
• Kim JM, Kim MW, Do HJ. Influence of hyperlipidemia on the treatment of supraspinatus tendinopathy with or without tear. Ann Rehabil Med. 2016;40:463–469.
   PubMedGoogle Scholar
• Esenkaya I, Unay K. Tendon, tendon healing, hyperlipidemia and statins. Muscles, Ligaments Tendons J. 2011;1:169–171.
   PubMedGoogle Scholar
• Abate M, Schiavone C, Salini S. Neoangiogenesis is reduced in chronic tendinopathies of type 2 diabetic patients. Int J Immunopathol Pharmacol. 2012;25:757–761.
   PubMed Web of Science ®Google Scholar
• Parson HK, Bundy MA, Dublin CB, et al. Pleiotropic effects of rosuvastatin on microvascular function in type 2 diabetes. Diabetes Metab Syndr Obes. 2010;3:19.
   PubMedGoogle Scholar
• Rees J, Stride M, Scott A. Tendons - time to revisit inflammation. Br J Sports Med. 2014;48:1553–1557.
   PubMed Web of Science ®Google Scholar
• Al-Asfar S, Attar M, Shacfeh H. Infliximab treatment for resistant Achilles tendonitis. Saudi Med J. 2009;30:1228–1230.
   PubMed Web of Science ®Google Scholar
• Fredberg U, Ostgaard R. Effect of ultrasound-guided, peritendinous injections of adalimumab and anakinra in chronic Achilles tendinopathy: a pilot study. Scand J Med Sci Sports. 2009;19:338–344.
   PubMed Web of Science ®Google Scholar
• Richards P, Dheer A, McCall I. Achilles tendon (TA) size and power Doppler ultrasound (PD) changes compared to MRI: a preliminary observational study. Clin Radiol. 2001;56:843–850.
   PubMed Web of Science ®Google Scholar
• Jonge S, de Warnaars J, de Vos R, et al. Relationship between neovascularization and clinical severity in Achilles tendinopathy in 556 paired measurements. Scand J Med Sci Sports. 2013;24:773–778.
   PubMed Web of Science ®Google Scholar
• Risch L, Cassel J, Messerschmidt K, et al. Is sonographic assessment of intratendinous blood flow in Achilles tendinopathy patients reliable? Ultrasound Int Open. 2016;2:E13–18.
   PubMed Web of Science ®Google Scholar
• Koenig M, Torp-Pedersen S, Qvistgaard E, et al. Preliminary results of colour Doppler-guided intratendinous glucocorticoid injection for Achilles tendonitis in five patients. Scand J Med Sci Sports. 2004;14:100–106.
   PubMed Web of Science ®Google Scholar
• Cook J, Ptazsnik R, Kiss Z, et al. High reproducibility of patellar tendon vascularity assessed by colour Doppler ultrasonography: a reliable measurement tool for quantifying tendon pathology. Br J Sports Med. 2005;39:700–703.
   PubMed Web of Science ®Google Scholar
• Yang X, Coleman D, Pugh N, et al. Quantitative assessment of intra-vascular volume in human Achilles tendinopathy. J Med Eng Technol. 2011;35:172–178.
   PubMedGoogle Scholar
• Yang X, Coleman D, Pugh N, et al. A novel 3-D power Doppler ultrasound approach to the quantification of Achilles tendon neovascularity. Ultrasound Med Biol. 2011;37:1046–1055.
   PubMed Web of Science ®Google Scholar
• Huang Y, Chen J, Chang YC, et al. Diagnosis of solid breast tumors using vessel analysis in three-dimensional power Doppler ultrasound images. J Digit Imaging. 2013;26:731–739.
   PubMed Web of Science ®Google Scholar
• van Der Ven M, Luime JJ, Levinia L, et al. High-frame-rate power Doppler ultrasound is more sensitive than conventional power Doppler in detecting rheumatic vascularisation. Ultrasound Med Biol. 2017;43:1868–1879.
   PubMed Web of Science ®Google Scholar