Skip to main content

Diffusion-weighted imaging of the kidneys in haemolytic uraemic syndrome

European Radiology volume 27, pages 4591–4601 (2017)Cite this article

Abstract

Objectives

To evaluate the kidneys of patients with haemolytic uraemic syndrome (HUS) using diffusion-weighted imaging (DWI) and Doppler ultrasound (US) compared with healthy controls.

Materials and Methods

Fifteen patients (mean age 33.3 years; three male; 12 female) with diarrhoea-positive HUS and 15 healthy volunteers were prospectively evaluated with DWI and Doppler US. A total apparent diffusion coefficient (ADCTOT), and ADCs predominantly reflecting microperfusion (ADCLOW) and diffusion (ADCHIGH) were calculated. Doppler US evaluated renal vascularity and flow.

Results

When compared with controls, kidneys affected by HUS showed reduced cortical ADC values (ADCTOT 1.79±0.22 vs. 2.04±0.1x10-3 mm2/s, P 0.001), resulting in either low corticomedullary differences (11/15 patients) or an inverted corticomedullary pattern (4/15 patients). Reduction of cortical ADC values was associated with a decrease of cortical vascularity on Doppler US (ADCTOT, P<0.001; ADCLOW, P 0.047). Kidneys with complete absence of the cortical vasculature on Doppler US (four patients) also demonstrated limited diffusion (ADCHIGH, P 0.002). Low glomerular filtration rate, requirement for haemodialysis during hospitalization, and longer duration of haemodialysis were associated with decreased cortical diffusivity (ADCTOT: P 0.04, 0.007, and <0.001, respectively).

Conclusion

DWI shows qualitative and quantitative abnormalities in kidneys affected by HUS, thereby extending the non-invasive assessment of renal parenchymal damage.

Key Points

• In HUS, DWI is feasible for functional characterization of kidney involvement.

• Kidneys affected by HUS showed reduced cortical diffusivity.

• Decreased cortical diffusivity was associated with lower kidney function.

• Requirement and duration of haemodialysis was linked to degree of cortical alterations.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Karpac CA, Li X, Terrell DR et al (2008) Sporadic bloody diarrhoea-associated thrombotic thrombocytopenic purpura-haemolytic uraemic syndrome: an adult and paediatric comparison. Br J Haematol 141:696–707

    Article  Google Scholar 

  2. Tostivint I, Mougenot B, Flahault A et al (2002) Adult haemolytic and uraemic syndrome: causes and prognostic factors in the last decade. Nephrol Dial Transplant 17:1228–1234

    Article  Google Scholar 

  3. Zimmerhackl LB, Besbas N, Jungraithmayr T et al (2006) Epidemiology, clinical presentation, and pathophysiology of atypical and recurrent hemolytic uremic syndrome. Semin Thromb Hemost 32:113–120

    Article  Google Scholar 

  4. Loos S, Ahlenstiel T, Kranz B et al (2012) An outbreak of Shiga toxin-producing Escherichia coli O104:H4 hemolytic uremic syndrome in Germany: presentation and short-term outcome in children. Clin Infect Dis 55:753–759

    CAS  Article  Google Scholar 

  5. Buchholz U, Bernard H, Werber D et al (2011) German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 365:1763–1770

    CAS  Article  Google Scholar 

  6. Ducker C, Dautel P, Wagner K et al (2011) Clinical symptoms, treatment and outcome of EHEC and EHEC-HUS patients treated as in-patients. Dtsch Med Wochenschr 136:1770–1776

    CAS  Article  Google Scholar 

  7. Garg AX, Suri RS, Barrowman N et al (2003) Long-term renal prognosis of diarrhea-associated hemolytic uremic syndrome: a systematic review, meta-analysis, and meta-regression. JAMA 290:1360–1370

    CAS  Article  Google Scholar 

  8. Colic E, Dieperink H, Titlestad K, Tepel M (2011) Management of an acute outbreak of diarrhoea-associated haemolytic uraemic syndrome with early plasma exchange in adults from southern Denmark: an observational study. Lancet 378:1089–1093

    Article  Google Scholar 

  9. Lapeyraque AL, Malina M, Fremeaux-Bacchi V et al (2011) Complement Blockade in Severe Shiga-Toxin-Associated HUS. N Engl J Med. doi:10.1056/NEJMc1100859

    Article  PubMed  Google Scholar 

  10. Laszik ZGS, Fred G (2007) Hepinstall's Pathology of the Kidney, 6th Edition, 6th Edition edn. Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  11. Lemmer A, Bergmann K, Walch R, Endert G (1995) Doppler ultrasound studies of long-term follow-up of children with hemolytic-uremic syndrome. Ultraschall Med 16:127–131

    CAS  Article  Google Scholar 

  12. O'Brien JA, Van Why SK, Keller MS, Gaudio KM, Kennedy TL, Siegel NJ (1994) Altered renovascular resistance after spontaneous recovery from hemolytic uremic syndrome. Yale J Biol Med 67:1–14

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Gleeson FV, Fitzpatrick MM, Somers J, Kennedy C, De Bruyn R, Barratt TM (1992) Duplex Doppler ultrasound in the investigation of occult nephropathy following haemolytic uraemic syndrome. Br J Radiol 65:137–139

    CAS  Article  Google Scholar 

  14. Scholbach TM (2001) Changes of renal flow volume in the hemolytic-uremic syndrome--color Doppler sonographic investigations. Pediatr Nephrol 16:644–647

    CAS  Article  Google Scholar 

  15. Glatstein M, Miller E, Garcia-Bournissen F, Scolnik D (2010) Timing and utility of ultrasound in diarrhea-associated hemolytic uremic syndrome: 7-year experience of a large tertiary care hospital. Clin Pediatr (Phila) 49:418–421

    Article  Google Scholar 

  16. Patriquin HB, O'Regan S, Robitaille P, Paltiel H (1989) Hemolytic-uremic syndrome: intrarenal arterial Doppler patterns as a useful guide to therapy. Radiology 172:625–628

    CAS  Article  Google Scholar 

  17. Reising A, Hafer C, Hiss M et al (2016) Ultrasound findings in EHEC-associated hemolytic-uremic syndrome and their clinical relevance. Int Urol Nephrol 48:561–570

    Article  Google Scholar 

  18. Naesens M, Heylen L, Lerut E et al (2013) Intrarenal resistive index after renal transplantation. N Engl J Med 369:1797–1806

    CAS  Article  Google Scholar 

  19. Boddi M, Natucci F, Ciani E (2015) The internist and the renal resistive index: truths and doubts. Intern Emerg Med 10:893–905

    Article  Google Scholar 

  20. Thoeny HC, De Keyzer F, Oyen RH, Peeters RR (2005) Diffusion-weighted MR imaging of kidneys in healthy volunteers and patients with parenchymal diseases: initial experience. Radiology 235:911–917

    Article  Google Scholar 

  21. Thoeny HC, De Keyzer F (2011) Diffusion-weighted MR imaging of native and transplanted kidneys. Radiology 259:25–38

    Article  Google Scholar 

  22. Thoeny HC, Zumstein D, Simon-Zoula S et al (2006) Functional evaluation of transplanted kidneys with diffusion-weighted and BOLD MR imaging: initial experience. Radiology 241:812–821

    Article  Google Scholar 

  23. Vermoolen MA, Kwee TC, Nievelstein RA (2012) Apparent diffusion coefficient measurements in the differentiation between benign and malignant lesions: a systematic review. Insights Imaging 3:395–409

    CAS  Article  Google Scholar 

  24. Lassel EA, Rao R, Schwenke C, Schoenberg SO, Michaely HJ (2014) Diffusion-weighted imaging of focal renal lesions: a meta-analysis. Eur Radiol 24:241–249

    CAS  Article  Google Scholar 

  25. Dale BM, Braithwaite AC, Boll DT, Merkle EM Field strength and diffusion encoding technique affect the apparent diffusion coefficient measurements in diffusion-weighted imaging of the abdomen. Invest Radiol 45: 104-108

    Article  Google Scholar 

  26. Yildirim E, Kirbas I, Teksam M, Karadeli E, Gullu H, Ozer I (2008) Diffusion-weighted MR imaging of kidneys in renal artery stenosis. Eur J Radiol 65:148–153

    Article  Google Scholar 

  27. Xu Y, Wang X, Jiang X (2007) Relationship between the renal apparent diffusion coefficient and glomerular filtration rate: preliminary experience. J Magn Reson Imaging 26:678–681

    Article  Google Scholar 

  28. Namimoto T, Yamashita Y, Mitsuzaki K, Nakayama Y, Tang Y, Takahashi M (1999) Measurement of the apparent diffusion coefficient in diffuse renal disease by diffusion-weighted echo-planar MR imaging. J Magn Reson Imaging 9:832–837

    CAS  Article  Google Scholar 

  29. Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505

    Article  Google Scholar 

  30. Kettritz U, Semelka RC, Brown ED, Sharp TJ, Lawing WL, Colindres RE (1996) MR findings in diffuse renal parenchymal disease. J Magn Reson Imaging 6:136–144

    CAS  Article  Google Scholar 

  31. Cheong B, Muthupillai R, Rubin MF, Flamm SD (2007) Normal values for renal length and volume as measured by magnetic resonance imaging. Clin J Am Soc Nephrol 2:38–45

    Article  Google Scholar 

  32. Helenon O, el Rody F, Correas JM et al (1995) Color Doppler US of renovascular disease in native kidneys. Radiographics 15:833–854, discussion 854-865

    CAS  Article  Google Scholar 

  33. Trillaud H, Merville P, Tran Le Linh P, Palussiere J, Potaux L, Grenier N (1998) Color Doppler sonography in early renal transplantation follow-up: resistive index measurements versus power Doppler sonography. AJR Am J Roentgenol 171:1611–1615

    CAS  Article  Google Scholar 

  34. Martinoli C, Crespi G, Bertolotto M et al (1996) Interlobular vasculature in renal transplants: a power Doppler US study with MR correlation. Radiology 200:111–117

    CAS  Article  Google Scholar 

  35. Noris M, Remuzzi G (2005) Hemolytic uremic syndrome. J Am Soc Nephrol 16:1035–1050

    CAS  Article  Google Scholar 

  36. Tublin ME, Bude RO, Platt JF (2003) Review. The resistive index in renal Doppler sonography: where do we stand? AJR Am J Roentgenol 180:885–892

    Article  Google Scholar 

  37. Argyle JC, Hogg RJ, Pysher TJ, Silva FG, Siegler RL (1990) A clinicopathological study of 24 children with hemolytic uremic syndrome. A report of the Southwest Pediatric Nephrology Study Group. Pediatr Nephrol 4:52–58

    CAS  Article  Google Scholar 

  38. Keir L, Coward RJ (2011) Advances in our understanding of the pathogenesis of glomerular thrombotic microangiopathy. Pediatr Nephrol 26:523–533

    Article  Google Scholar 

  39. Sigmund EE, Vivier PH, Sui D et al (2012) Intravoxel Incoherent Motion and Diffusion-Tensor Imaging in Renal Tissue under Hydration and Furosemide Flow Challenges. Radiology 263:758–769

    Article  Google Scholar 

  40. Emre T, Kilickesmez O, Buker A, Inal BB, Dogan H, Ecder T (2016) Renal function and diffusion-weighted imaging: a new method to diagnose kidney failure before losing half function. Radiol Med 121:163–172

    Article  Google Scholar 

  41. Xu X, Fang W, Ling H, Chai W, Chen K (2009) Diffusion-weighted MR imaging of kidneys in patients with chronic kidney disease: initial study. Eur Radiol 20:978–983

    Article  Google Scholar 

  42. Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407

    Article  Google Scholar 

  43. Koh DM, Collins DJ (2007) Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 188:1622–1635

    Article  Google Scholar 

  44. Liang L, Chen WB, Chan KW et al (2016) Using intravoxel incoherent motion MR imaging to study the renal pathophysiological process of contrast-induced acute kidney injury in rats: Comparison with conventional DWI and arterial spin labelling. Eur Radiol 26:1597–1605

    Article  Google Scholar 

  45. Levey AS, Coresh J, Greene T et al (2006) Using standardized serum creatinine values in the modification of diet in renal disease study equation for estimating glomerular filtration rate. Ann Intern Med 145:247–254

    CAS  Article  Google Scholar 

  46. Levey AS, Coresh J, Greene T et al (2007) Expressing the Modification of Diet in Renal Disease Study equation for estimating glomerular filtration rate with standardized serum creatinine values. Clin Chem 53:766–772

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Diagnostic and Interventional Radiology and Nuclear Medicine, University Medical Center Hamburg-Eppendorf, Martinistrasse 52, 20246, Hamburg, Germany

    Jochen Herrmann, Stephanie Galler, Bjoern P. Schoennagel, Peter Bannas, Jin Yamamura, Michael Groth & Gerhard Adam

  2. Department of Diagnostic and Interventional Radiology and Nuclear Medicine, Section of Pediatric Radiology, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany

    Jochen Herrmann, Jasmin D. Busch & Magdalini Tozakidou

  3. III. Department of Internal Medicine, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany

    Ulrich Wenzel

  4. Department for Psychiatry and Psychotherapy, Section for Addiction Research and Therapy, University Hospital of Tübingen, 72076, Tübingen, Germany

    Kay U. Petersen

  5. Siemens AG Healthcare, 20099, Hamburg, Germany

    Michaela Joekel

  6. Katholisches Marienkrankenhaus Hamburg Department of Diagnostic and Interventional Radiology, Alfredstr. 9, 22087, Hamburg, Germany

    Christian R. Habermann

Authors
  1. Jochen Herrmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulrich Wenzel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephanie Galler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bjoern P. Schoennagel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jasmin D. Busch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Magdalini Tozakidou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kay U. Petersen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michaela Joekel
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peter Bannas
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jin Yamamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Michael Groth
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Gerhard Adam
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Christian R. Habermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jochen Herrmann.

Ethics declarations

Guarantor

The scientific guarantor of this publication is PD Dr. J. Herrmann.

Conflict of interest

The authors of this manuscript declare relationships with the following companies: Michaela Joekel, Siemens AG Healthcare, Hamburg, Germany.

Funding

The authors state that this work has not received any funding.

Statistics and biometry

Two of the authors (Kay U. Petersen and Michael Groth) have significant statistical expertise.

Ethical approval

Institutional Review Board approval was obtained.

Informed consent

Written informed consent was obtained from all subjects (patients and controls) in this study.

Study subjects or cohorts overlap

No study subjects or cohorts have been previously reported.

Methodology

•prospective

•case-control study

•performed at one institution

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Material Fig. 6

(DOC 25 kb)

Supplemental Material Fig. 7

(DOC 25 kb)

Supplemental Material Fig. 8

(DOC 25 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Herrmann, J., Wenzel, U., Galler, S. et al. Diffusion-weighted imaging of the kidneys in haemolytic uraemic syndrome. Eur Radiol 27, 4591–4601 (2017). https://doi.org/10.1007/s00330-017-4848-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-4848-2

Keywords

  • ADC
  • Diffusion-weighted imaging
  • Haemolytic-uraemic syndrome
  • Kidney
  • MRI
  • STEC