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01-07-2013 | Diagnostic Neuroradiology

Quantitative MRI shows cerebral microstructural damage in hemolytic–uremic syndrome patients with severe neurological symptoms but no changes in conventional MRI

Authors: Karin Weissenborn, Eva Bültmann, Frank Donnerstag, Anja M. Giesemann, Friedrich Götz, Hans Worthmann, Meike Heeren, Jan Kielstein, Anke Schwarz, Heinrich Lanfermann, Xiao-Qi Ding

Published in: Neuroradiology | Issue 7/2013

Abstract

Introduction

Severe neurological symptoms in Shiga toxin-producing Escherichia coli infection associated hemolytic–uremic syndrome (STEC–HUS) are often accompanied by none or only mild alterations of cerebral magnetic resonance imaging (MRI). This study aims to analyze if quantitative MRI is able to reveal cerebral pathological alterations invisible for conventional MRI.

Methods

In nine patients with STEC–HUS associated severe neurological symptoms but inconspicuous cerebral MRI findings maps of the parameters T2 relaxation time, relative proton density (PD), apparent diffusion coefficient (ADC), and fractional anisotropy (FA) were generated. Quantitative values of these parameters were measured at the basal ganglia, thalamus, and white matter of the frontal and parietal lobe and compared to those of nine age- and sex-matched controls.

Results

Significant T2 prolongation (p < 0.01) was found in the basal ganglia of all patients compared to controls. PD and ADC were not significantly altered. A significant reduction of FA in patients was seen at caput nuclei caudati (p < 0.01).

Conclusion

Prolonged T2 relaxation time indicates cerebral microstructural damages in these patients despite their inconspicuous MRI findings. T2 relaxometry could be used as a complementary tool for the assessment of metabolic–toxic brain syndromes.

Roche-Martinez A, Poo P, Maristany-Cucurella M, Jimenez-Llort A, Camacho JA, Campistol J (2008) Neurologic presentation in haemolytic–uraemic syndrome. Rev Neurol 47(4):191–196PubMed

Eriksson KJ, Boyd SG, Tasker RC (2001) Acute neurology and neurophysiology of haemolytic–uraemic syndrome. Arch Dis Child 84(5):434–435PubMedCrossRef

Gallo EG, Gianantonio CA (1995) Extrarenal involvement in diarrhoea-associated haemolytic–uraemic syndrome. Pediatr Nephrol 9(1):117–119PubMedCrossRef

Keir L, Coward RJ (2011) Advances in our understanding of the pathogenesis of glomerular thrombotic microangiopathy. Pediatrics 26(4):523–533, Epub 2010

Zoja C, Buelli S, Morigi M (2010) Shiga toxin-associated hemolytic uremic syndrome: pathophysiology of endothelial dysfunction. Pediatrics 25(11):2231–2240, Epub 2010 Apr 2228

Bale JF Jr, Brasher C, Siegler RL (1980) CNS manifestations of the hemolytic–uremic syndrome. Relationship to metabolic alterations and prognosis. Am J Dis Child 134(9):869–872PubMed

Obata F (2010) Influence of Escherichia coli shiga toxin on the mammalian central nervous system. Adv Appl Microbiol 71:1–19PubMedCrossRef

Magnus T, Röther J, Simova O, Meier-Cillien M, Repenthin J, Möller F, Gbadamosi J, Panzer U, Wengenroth M, Hagel C, Kluge S, Stahl RK, Wegscheider K, Urban P, Eckert B, Glatzel M, Fiehler J, Gerloff C (2012) The neurological syndrome in adults during the 2011 northern German E. coli serotype O104:H4 outbreak. Brain 135(Pt 6):1850–1859PubMedCrossRef

Weissenborn K, Donnerstag F, Kielstein JT, Heeren M, Worthmann H, Hecker H, Schmitt R, Schiffer M, Pasedag T, Schuppner R, Tryc AB, Raab P, Hartmann H, Ding XQ, Hafer C, Menne J, Schmidt BM, Bultmann E, Haller H, Dengler R, Lanfermann H, Giesemann AM (2012) Neurologic manifestations of E. coli infection-induced hemolytic–uremic syndrome in adults. Neurology 79(14):1466–1473PubMedCrossRef

10.

Upadhyaya K, Barwick K, Fishaut M, Kashgarian M, Siegel NJ (1980) The importance of nonrenal involvement in hemolytic–uremic syndrome. Pediatrics 65(1):115–120PubMed

11.

Steinborn M, Leiz S, Rudisser K, Griebel M, Harder T, Hahn H (2004) CT and MRI in haemolytic uraemic syndrome with central nervous system involvement: distribution of lesions and prognostic value of imaging findings. Pediatr Radiol 34(10):805–810PubMedCrossRef

12.

Ohlmann D, Hamann GF, Hassler M, Schimrigk K (1996) Involvement of the central nervous system in hemolytic uremic syndrome/thrombotic thrombocytopenic purpura. Nervenarzt 67(10):880–882PubMedCrossRef

13.

Ding XQ, Sun Y, Kruse B, Illies T, Zeumer H, Fiehler J, Lanfermann H (2009) Microstructural callosal abnormalities in normal-appearing brain of children with developmental delay detected with diffusion tensor imaging. Eur Radiol 19(6):1537–1543PubMedCrossRef

14.

Ding XQ, Fiehler J, Kohlschutter B, Wittkugel O, Grzyska U, Zeumer H, Ullrich K (2008) MRI abnormalities in normal-appearing brain tissue of treated adult PKU patients. J Magn Reson Imaging 27(5):998–1004PubMedCrossRef

15.

Ding XQ, Wittkugel O, Goebell E, Förster AF, Grzyska U, Zeumer H, Fiehler J (2008) Clinical applications of quantitative T2 determination: a complementary MRI tool for routine diagnosis of suspected myelination disorders. Eur J Paediatr Neurol 12(4):298–308, Epub 2007 OctPubMedCrossRef

16.

Leppert IR, Almli CR, McKinstry RC, Mulkern RV, Pierpaoli C, Rivkin MJ, Pike GB (2009) T(2) relaxometry of normal pediatric brain development. J Magn Reson Imaging 29(2):258–267PubMedCrossRef

17.

Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11(7):36–42

18.

Nathanson S, Kwon T, Elmaleh M, Charbit M, Launay EA, Harambat J, Brun M, Ranchin B, Bandin F, Cloarec S, Bourdat-Michel G, Piètrement C, Champion G, Ulinski T, Deschênes G (2010) Acute neurological involvement in diarrhea-associated hemolytic uremic syndrome. Clin J Am Soc Nephrol 5(7):1218–1228PubMedCrossRef

19.

Donnerstag F, Ding X, Pape L, Bültmann E, Lücke T, Zajaczek J, Hoy L, Das AM, Lanfermann H, Ehrich J, Hartmann H (2012) Patterns in early diffusion-weighted MRI in children with haemolytic uraemic syndrome and CNS involvement. Eur Radiol 22(3):506–513PubMedCrossRef

20.

Ono J, Kodaka R, Imai K, Itagaki Y, Tanaka J, Inui K, Nagai T, Sakurai K, Harada K, Okada S (1993) Evaluation of myelination by means of the T2 value on magnetic resonance imaging. Brain Dev 15(6):433–438PubMedCrossRef

21.

Ding XQ, Kucinski T, Wittkugel O, Goebell E, Grzyska U, Görg M, Kohlschütter A, Zeumer H (2004) Normal brain maturation characterized with age-related T2 relaxation times: an attempt to develop a quantitative imaging measure for clinical use. Invest Radiol 39(12):740–746PubMedCrossRef

22.

Bick U, Ullrich K, Stöber U, Möller H, Schuierer G, Ludolph AC, Oberwittler C, Weglage J, Wendel U (1993) White matter abnormalities in patients with treated hyperphenylalaninaemia: magnetic resonance relaxometry and proton spectroscopy findings. Eur J Pediatr 152(12):1012–1020PubMedCrossRef

23.

Larocque MP, Syme A, Yahya A, Wachowicz K, Allalunis-Turner J, Fallone BG (2010) Monitoring T2 and ADC at 9.4 T following fractionated external beam radiation therapy in a mouse model. Phys Med Biol 55(5):1381–1393PubMedCrossRef

24.

Cieszanowski A, Anysz-Grodzicka A, Szeszkowski W, Kaczynski B, Maj E, Gornicka B, Grodzicki M, Grudzinski IP, Stadnik A, Krawczyk M, Rowinski O (2012) Characterization of focal liver lesions using quantitative techniques: comparison of apparent diffusion coefficient values and T2 relaxation times. Eur Radiol 22(11):2514–2524PubMedCrossRef

25.

Madler B, Drabycz SA, Kolind SH, Whittall KP, MacKay AL (2008) Is diffusion anisotropy an accurate monitor of myelination? Correlation of multicomponent T2 relaxation and diffusion tensor anisotropy in human brain. Magn Reson Imaging 26(7):874–888PubMedCrossRef

26.

Bauwens A, Bielaszewska M, Kemper B, Langehanenberg P, von Bally G, Reichelt R, Mulac D, Humpf HU, Friedrich AW, Kim KS, Karch H, Müthing J (2011) Differential cytotoxic actions of Shiga toxin 1 and Shiga toxin 2 on microvascular and macrovascular endothelial cells. Thromb Haemost 105(3):515–528PubMedCrossRef

27.

Takahashi K, Funata N, Ikuta F, Sato S (2008) Neuronal apoptosis and inflammatory responses in the central nervous system of a rabbit treated with Shiga toxin-2. J Neuroinflammation 5:11PubMedCrossRef

28.

Goldstein J, Loidl CF, Creydt VP, Boccoli J, Ibarra C (2007) Intracerebroventricular administration of Shiga toxin type 2 induces striatal neuronal death and glial alterations: an ultrastructural study. Brain Res 1161:106–115PubMedCrossRef

29.

Tironi-Farinati C, Loidl CF, Boccoli J, Parma Y, Fernandez-Miyakawa ME, Goldstein J (2010) Intracerebroventricular Shiga toxin 2 increases the expression of its receptor globotriaosylceramide and causes dendritic abnormalities. J Neuroimmunol 222(1-2):48–61PubMedCrossRef

Title: Quantitative MRI shows cerebral microstructural damage in hemolytic–uremic syndrome patients with severe neurological symptoms but no changes in conventional MRI
Authors: Karin Weissenborn
Eva Bültmann
Frank Donnerstag
Anja M. Giesemann
Friedrich Götz
Hans Worthmann
Meike Heeren
Jan Kielstein
Anke Schwarz
Heinrich Lanfermann
Xiao-Qi Ding
Publication date: 01-07-2013
Publisher: Springer Berlin Heidelberg
Published in: Neuroradiology / Issue 7/2013
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI: https://doi.org/10.1007/s00234-013-1176-3

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Springer Medicine

Quantitative MRI shows cerebral microstructural damage in hemolytic–uremic syndrome patients with severe neurological symptoms but no changes in conventional MRI

Abstract

Introduction

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Introduction

Methods

Results

Conclusion

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