Skip to main content
Log in

Ultrasonic evaluation with second harmonic imaging and SonoVue in the assessment of cerebral perfusion in diabetic patients: a case-control study

  • Ultrasound
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

The purpose was to compare human brain tissue perfusion in diabetic patients and healthy subjects with second harmonic imaging ultrasound and SonoVue to test the hypothesis that brain tissue perfusion differences are present in these two groups of patients. In a prospective case-control study, second harmonic examinations performed in 20 patients with type II diabetes mellitus and in 20 matched control patients were compared. After administration of 2.5 ml of SonoVue, 60 time-triggered images were recorded. Time-intensity curves, including peak intensity and positive gradient normalized to the middle cerebral artery, were calculated to quantify ultrasound intensity in a region of interest. The Mann-Whitney U-test was used to reveal any differences between healthy and diabetic subjects. Mean peak intensity was 0.64±0.1 Au in healthy subjects and 0.53±0.09 Au in diabetic patients. Mean positive gradient was 0.04±0.007 Au/s in healthy subjects and 0.04±0.008 Au/s in diabetic patients. Peak intensity and positive gradient were significantly lower in diabetic patients than in healthy subjects (P<0.05). Ultrasound examination with second harmonic imaging and SonoVue administration is able to detect clinically silent, reduced cerebral perfusion in type II diabetic patients. Diabetic patients have reduced cerebral perfusion in comparison to healthy subjects.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Stegmayr B, Asplund K (1995) Diabetes as a risk factor for stroke: a popolation perspective. Diabetologia 38:1061–1068

    Article  CAS  PubMed  Google Scholar 

  2. Tuomilehto J, Rastenyte D, Jousilahti P, Sarti C, Vartiainen E (1996) Diabetes mellitus as a risk factor for death from stroke: prospective study of the middle-aged Finnish population. Stroke 2:210–215

    Google Scholar 

  3. Currie CJ, Morgan CL, Gill L, Stott NC, Peters JR (1997) Epidemiology and costs of acute hospital care for cerebrovascular disease in diabetic and non-diabetic populations. Stroke 28:1142–1146

    CAS  PubMed  Google Scholar 

  4. Reaven GM (1988) Role of insulin resistance in human disease. Diabetes 37:1595–1607

    CAS  PubMed  Google Scholar 

  5. Kaplan NM (1989) The deadly quartet: upper-body obesity, glucose intolerance, hypertriglyceridemia, and hypertension. Arch Intern Med 149:1514–1520

    Article  CAS  PubMed  Google Scholar 

  6. DeFronzo RA, Ferrannini E (1991) Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14:173–194

    CAS  PubMed  Google Scholar 

  7. Nagamachi S, Nishikawa T, Ono S et al (1994) Regional cerebral blood flow in diabetic patients: evaluation by N-isopropyl-123IMP with SPECT. Nucl Med Commun 15:455–460

    CAS  PubMed  Google Scholar 

  8. Jiménez-Bonilla JF, Carril JM, Quirce R, Gómez-Barquín R, Amado JA, Gutiérrez-Mendiguchía C (1996) Assessment of cerebral blood flow in diabetic patients with no clinical history of neurological disease. Nucl Med Commun 17:790–794

    PubMed  Google Scholar 

  9. Quirce R, Carril JM, Jiménez-Bonilla JF et al (1997) Semiquantitative assessment of cerebral blood flow with 99mTc-HMPAO SPECT in type I diabetic patients with no clinical history of cerebrovascular disease. Eur J Nucl Med 24:1507–1513

    Article  CAS  PubMed  Google Scholar 

  10. Biessels GJ, Braun KP, de Graaf RA, van Eijsden P, Gispen WH, Nicolay K (2001) Cerebral metabolism in streptozotocin-diabetic rats; an in vivo magnetic resonance spectroscopy study. Diabetologia 44:346–353

    Article  CAS  PubMed  Google Scholar 

  11. Chu K, Kang DW, Kim DE, Park SH, Roh JK (2002) Diffusion-weighted and gradient echo magnetic resonance findings of hemichorea–hemiballism associated with diabetic hyperglicemia: a hyperviscosity syndrome? Arch Neurol 59:448–452

    Article  PubMed  Google Scholar 

  12. Wakisaka M, Nagamachi S, Inoue K, Morotomi Y, Fujishima M (1990) Reduced regional cerebral blood flow in aged noninsulin-dependent diabetic patients with no history of cerebrovascular disease: evaluation by N-isopropil-123I-p-iodoamphetamine with single photon emission computed tomography. J Diabetes Complications 4:170–174

    Article  CAS  Google Scholar 

  13. Rodriguez G, Nobili F, Celestino MA et al (1993) Regional cerebral blood flow and cerebrovascular reactivity in IDDM. Diabetes Care 16:462–468

    CAS  PubMed  Google Scholar 

  14. Mortel KF, Meyer JS, Sims PA, McClintic K (1990) Diabetes mellitus as a risk factor for stroke. South Med J 83:904–911

    CAS  PubMed  Google Scholar 

  15. Grill V, Gutniak M, Bjorkman O et al (1990) Cerebral blood flow and substrates utilization in insulin-treated diabetic subjects. Am J Physiol 258:E813–E820

    CAS  PubMed  Google Scholar 

  16. Correas JM, Bridal L, Lesavre A, Mejean A, Claudon M, Helenon O (2001) Ultrasound contrast agents: properties, principles of action, tolerance, and artifacts. Eur Radiol 11:1316–1328

    Article  CAS  PubMed  Google Scholar 

  17. Bartolotta TV, Midiri M, Scialpi M, Sciarrino E, Galia M, Lagalla R (2004) Focal nodular hyperplasia in normal and fatty liver: a qualitative and quantitative evaluation with contrast-enhanced ultrasound. Eur Radiol 14:583–591

    Article  PubMed  Google Scholar 

  18. Quaia E, Bertolotto M, Dalla Palma L (2002) Characterization of liver hemangiomas with pulse inversion harmonic imaging. Eur Radiol 12:537–544

    PubMed  Google Scholar 

  19. Bertolotto M, Dalla Palma L, Quaia E, Locatelli M (2000) Characterization of unifocal liver lesions with pulse inversion harmonic imaging after Levovist injection: preliminary results. Eur Radiol 10:1369–1376

    Article  CAS  PubMed  Google Scholar 

  20. Albrecht T, Hoffmann CW, Schettler S, Overberg A, Ilg M, Wolf KJ (1999) Improved detection of liver metastases with phase inversion imaging during the liver-specific phase of the ultrasound contrast agent levovist. Eur Radiol 9[Suppl 3]:S388

  21. Albrecht T, Blomley MJ, Cosgrove DO et al (1999) Transit-time studies with levovist in patients with and without hepatic cirrhosis: a promising new diagnostic tool. Eur Radiol 9[Suppl 3]:S377–S3811

    Google Scholar 

  22. Sidhu PS, Shaw AS, Ellis SM, Karani JB, Ryan SM (2004) Microbubble ultrasound contrast in the assessment of hepatic artery patency following liver transplantation: role in reducing frequency of hepatic artery arteriography. Eur Radiol 14:21–30

    Google Scholar 

  23. Ascenti G, Zimbaro G, Mazziotti S, Gaeta M, Lamberto S, Scribano E (2001) Contrast-enhanced power Doppler US in the diagnosis of renal pseudotumors. Eur Radiol 11:2496–2499

    Google Scholar 

  24. Hohl C, Schmidt T, Haage P et al (2004) Phase-inversion tissue harmonic imaging compared with conventional B-mode ultrasound in the evaluation of pancreatic lesions. Eur Radiol 14:1109–1117

    PubMed  Google Scholar 

  25. Magarelli N, Guglielmi G, Di Matteo L, Tartaro A, Mattei PA, Bonomo L (2001) Diagnostic utility of an echo-contrast agent in patients with synovitis using power Doppler ultrasound: a preliminary study with comparison to contrast-enhanced MRI. Eur Radiol 11:1039–1046

    Google Scholar 

  26. Schroeder RJ, Bostanjoglo M, Rademaker J, Maeurer J, Felix R (2003) Role of power Doppler techniques and ultrasound contrast enhancement in the differential diagnosis of focal breast lesions. Eur Radiol 13:68–79

    Google Scholar 

  27. Postert T, Muhs A, Meves S, Federlein J, Przuntek H, Buttner T (1998) Transient response harmonic imaging. An ultrasound technique related to brain perfusion. Stroke 29:1901–1907

    CAS  PubMed  Google Scholar 

  28. Seidel G, Meyer K (2001) Harmonic imaging—a new method for the sonographic assessment of cerebral perfusion. Eur J Ultrasound 14:103–113

    Article  CAS  PubMed  Google Scholar 

  29. Seidel G, Greis C, Sonne J, Kaps M (1999) Harmonic grey scale imaging of the human brain. J Neuroimaging 9:171–174

    CAS  PubMed  Google Scholar 

  30. Seidel G, Algermissen C, Christoph A, Claassen L, Vidal-Langwasser M, Katzer T (2000) Harmonic imaging of the human brain. Visualization of brain perfusion with ultrasound. Stroke 31:151–154

    CAS  PubMed  Google Scholar 

  31. Seidel G, Algermissen C, Christoph A, Katzer T, Kaps M (2000) Visualization of brain perfusion with harmonic gray scale and power Doppler technology: an animal pilot study. Stroke 31:1728–1734

    CAS  PubMed  Google Scholar 

  32. Wiesmann M, Seidel G (2000) Ultrasound perfusion imaging of the human brain. Stroke 31:2421–2425

    CAS  PubMed  Google Scholar 

  33. Eyding J, Krogias C, Wilkening W, Meves S, Ermert H, Postert T (2003) Parameters of cerebral perfusion in phase-inversion harmonic imaging (PIHI) ultrasound examinations. Ultrasound Med Biol 29:1379–1385

    Article  PubMed  Google Scholar 

  34. van Wijk MC, Klaessens JH, Hopman JC, Liem KD, Thijssen JM (2003) Assessment of local changes of cerebral perfusion and blood concentration by ultrasound harmonic B-mode contrast measurement in piglet. Ultrasound Med Biol 29:1253–1260

    Article  PubMed  Google Scholar 

  35. Postert T, Federlein J, Weber S, Przuntek H, Buttner T (1999) Second harmonic imaging in acute middle cerebral artery infarction. Stroke 30:1702–1706

    CAS  PubMed  Google Scholar 

  36. Federlein J, Postert T, Meves S, Weber S, Przuntek H, Buttner T (2000) Ultrasonic evaluation of pathological brain perfusion in acute stroke using second harmonic imaging. J Neurol Neurosurg Psychiatry 69:616–622

    Google Scholar 

  37. Harrer JU, Mayfrank L, Mull M, Klotzsch C (2003) Second harmonic imaging: a new ultrasound technique to assess human brain tumour perfusion. J Neurol Neurosurg Psychiatry 74:333–338

    Google Scholar 

  38. Seidel G, Meyer-Wiethe K, Berdien G, Hollstein D, Toth D, Aach T (2004) Ultrasound perfusion imaging in acute middle cerebral artery infarction predicts outcome. Stroke 35:1107–1111

    Article  PubMed  Google Scholar 

  39. Bartels E, Bittermann HJ (2004) Transcranial contrast imaging of cerebral perfusion in stroke patients following decompressive craniectomy. Ultraschall Med 25:206–213

    Article  CAS  PubMed  Google Scholar 

  40. Harrer JU, Klotzsch C (2002) Second harmonic imaging of the human brain. The practicability of coronal insonation planes and alternative perfusion parameter. Stroke 33:1530–1535

    Article  PubMed  Google Scholar 

  41. Shen J, Xue Y, Zhang Y, Wang Q (2002) The application of transcranial Doppler in detecting diabetic cerebral macroangiopathy and microangiopathy. Zhonghua Nei Ke Za Zhi Mar 41:172–174

    Google Scholar 

  42. Lippera S, Gregorio F, Ceravolo MG, Lagalla G, Provinciali L (1997) Diabetic retinopathy and cerebral hemodynamic impairment in type II diabetes. Eur J Ophthalmol 7:156–162

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Giuseppe Caruso.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Caruso, G., Salvaggio, G., Ragusa, P. et al. Ultrasonic evaluation with second harmonic imaging and SonoVue in the assessment of cerebral perfusion in diabetic patients: a case-control study. Eur Radiol 15, 823–828 (2005). https://doi.org/10.1007/s00330-004-2474-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-004-2474-2

Keywords

Navigation