Skip to main content
Top
Published in: European Radiology 10/2016

01-10-2016 | Paediatric

Amide Proton Transfer (APT) MR imaging and Magnetization Transfer (MT) MR imaging of pediatric brain development

Authors: Hong Zhang, Huiying Kang, Xuna Zhao, Shanshan Jiang, Yi Zhang, Jinyuan Zhou, Yun Peng

Published in: European Radiology | Issue 10/2016

Login to get access

Abstract

Objectives

To quantify the brain maturation process during childhood using combined amide proton transfer (APT) and conventional magnetization transfer (MT) imaging at 3 Tesla.

Methods

Eighty-two neurodevelopmentally normal children (44 males and 38 females; age range, 2−190 months) were imaged using an APT/MT imaging protocol with multiple saturation frequency offsets. The APT-weighted (APTW) and MT ratio (MTR) signals were quantitatively analyzed in multiple brain areas. Age-related changes in MTR and APTW were evaluated with a non-linear regression analysis.

Results

The APTW signals followed a decreasing exponential curve with age in all brain regions measured (R2 = 0.7−0.8 for the corpus callosum, frontal and occipital white matter, and centrum semiovale). The most significant changes appeared within the first year. At maturation, larger decreases in APTW and lower APTW values were found in the white matter. On the contrary, the MTR signals followed an increasing exponential curve with age in the same brain regions measured, with the most significant changes appearing within the initial 2 years. There was an inverse correlation between the MTR and APTW signal intensities during brain maturation.

Conclusions

Together with MT imaging, protein-based APT imaging can provide additional information in assessing brain myelination in the paediatric population.

Key Points

APTW signals followed a decreasing exponential curve with age.
The most significant APTW changes appeared within the first year
At maturation, larger APTW decreases and lower APTW appeared in white matter
MTR signals followed an increasing exponential curve with age
Appendix
Available only for authorised users
Literature
1.
go back to reference Brody BA, Kinney HC, Kloman AS, Gilles FH (1987) Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301CrossRefPubMed Brody BA, Kinney HC, Kloman AS, Gilles FH (1987) Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301CrossRefPubMed
2.
3.
4.
go back to reference Dietrich RB, Bradley WG, Zaragoza EJ et al (1988) MR evaluation of early myelination patterns in normal and developmentally delayed infants. AJR Am J Roentgenol 150:889–896CrossRefPubMed Dietrich RB, Bradley WG, Zaragoza EJ et al (1988) MR evaluation of early myelination patterns in normal and developmentally delayed infants. AJR Am J Roentgenol 150:889–896CrossRefPubMed
5.
go back to reference Bird CR, Hedberg M, Drayer BP, Keller PJ, Flom RA, Hodak JA (1989) MR assessment of myelination in infants and children: usefulness of marker sites. AJNR Am J Neuroradiol 10:731–740PubMed Bird CR, Hedberg M, Drayer BP, Keller PJ, Flom RA, Hodak JA (1989) MR assessment of myelination in infants and children: usefulness of marker sites. AJNR Am J Neuroradiol 10:731–740PubMed
6.
go back to reference Barkovich AJ, Kjos BO, Jackson DE Jr, Norman D (1988) Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 166:173–180CrossRefPubMed Barkovich AJ, Kjos BO, Jackson DE Jr, Norman D (1988) Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology 166:173–180CrossRefPubMed
7.
go back to reference Ballesteros MC, Hansen PE, Soila K (1993) MR imaging of the developing human brain. Part 2. Postnatal development. Radiographics 13:611–622CrossRefPubMed Ballesteros MC, Hansen PE, Soila K (1993) MR imaging of the developing human brain. Part 2. Postnatal development. Radiographics 13:611–622CrossRefPubMed
8.
go back to reference Ding XQ, Kucinski T, Wittkugel O et al (2004) Normal brain maturation characterized with age-related T2 relaxation times: an attempt to develop a quantitative imaging measure for clinical use. Investig Radiol 39:740–746CrossRef Ding XQ, Kucinski T, Wittkugel O et al (2004) Normal brain maturation characterized with age-related T2 relaxation times: an attempt to develop a quantitative imaging measure for clinical use. Investig Radiol 39:740–746CrossRef
9.
go back to reference Forbes KP, Pipe JG, Bird CR (2002) Changes in brain water diffusion during the 1st year of life. Radiology 222:405–409CrossRefPubMed Forbes KP, Pipe JG, Bird CR (2002) Changes in brain water diffusion during the 1st year of life. Radiology 222:405–409CrossRefPubMed
10.
go back to reference Laule C, Vavasour IM, Kolind SH et al (2007) Magnetic resonance imaging of myelin. Neurotherapeutics 4:460–484CrossRefPubMed Laule C, Vavasour IM, Kolind SH et al (2007) Magnetic resonance imaging of myelin. Neurotherapeutics 4:460–484CrossRefPubMed
11.
go back to reference Welker KM, Patton A (2012) Assessment of normal myelination with magnetic resonance imaging. Semin Neurol 32:15–28CrossRefPubMed Welker KM, Patton A (2012) Assessment of normal myelination with magnetic resonance imaging. Semin Neurol 32:15–28CrossRefPubMed
12.
go back to reference Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315CrossRefPubMed Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315CrossRefPubMed
13.
go back to reference Deoni SC, Mercure E, Blasi A et al (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784–791CrossRefPubMed Deoni SC, Mercure E, Blasi A et al (2011) Mapping infant brain myelination with magnetic resonance imaging. J Neurosci 31:784–791CrossRefPubMed
15.
go back to reference Henkelman RM, Stanisz GJ, Graham SJ (2001) Magnetization transfer in MRI: a review. NMR Biomed 14:57–64CrossRefPubMed Henkelman RM, Stanisz GJ, Graham SJ (2001) Magnetization transfer in MRI: a review. NMR Biomed 14:57–64CrossRefPubMed
16.
go back to reference Kucharczyk W, Macdonald PM, Stanisz GJ, Henkelman RM (1994) Relaxation and magnetization transfer of white matter lipids at MR imaging: importance of cerebtosides and pH. Radiology 192:521–529CrossRefPubMed Kucharczyk W, Macdonald PM, Stanisz GJ, Henkelman RM (1994) Relaxation and magnetization transfer of white matter lipids at MR imaging: importance of cerebtosides and pH. Radiology 192:521–529CrossRefPubMed
17.
go back to reference Engelbrecht V, Rassek M, Preiss S, Wald C, Modder U (1998) Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. AJNR Am J Neuroradiol 19:1923–1929PubMed Engelbrecht V, Rassek M, Preiss S, Wald C, Modder U (1998) Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. AJNR Am J Neuroradiol 19:1923–1929PubMed
18.
go back to reference van Buchem MA, Steens SC, Vrooman HA et al (2001) Global estimation of myelination in the developing brain on the basis of magnetization transfer imaging: a preliminary study. AJNR Am J Neuroradiol 22:762–766PubMed van Buchem MA, Steens SC, Vrooman HA et al (2001) Global estimation of myelination in the developing brain on the basis of magnetization transfer imaging: a preliminary study. AJNR Am J Neuroradiol 22:762–766PubMed
19.
go back to reference Zhou J, Payen J, Wilson DA, Traystman RJ, van Zijl PCM (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090CrossRefPubMed Zhou J, Payen J, Wilson DA, Traystman RJ, van Zijl PCM (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090CrossRefPubMed
20.
go back to reference Zhou J, van Zijl PC (2006) Chemical exchange saturation transfer imaging and spectroscopy. Prog NMR Spectrosc 48:109–136CrossRef Zhou J, van Zijl PC (2006) Chemical exchange saturation transfer imaging and spectroscopy. Prog NMR Spectrosc 48:109–136CrossRef
21.
23.
go back to reference Zhou J, Zhu H, Lim M et al (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128CrossRefPubMed Zhou J, Zhu H, Lim M et al (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128CrossRefPubMed
24.
go back to reference Jiang S, Yu H, Wang X et al (2015) Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla. Eur Radiol. doi:10.1007/s00330-00015-03805-00331 Jiang S, Yu H, Wang X et al (2015) Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla. Eur Radiol. doi:10.​1007/​s00330-00015-03805-00331
25.
go back to reference Harston GW, Tee YK, Blockley N et al (2015) Identifying the ischaemic penumbra using pH-weighted magnetic resonance imaging. Brain 138:36–42CrossRefPubMed Harston GW, Tee YK, Blockley N et al (2015) Identifying the ischaemic penumbra using pH-weighted magnetic resonance imaging. Brain 138:36–42CrossRefPubMed
27.
go back to reference Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173CrossRefPubMed Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29:162–173CrossRefPubMed
28.
29.
go back to reference Barkovich AJ (2000) Concepts of myelin and myelination in neuroradiology. AJNR Am J Neuroradiol 21:1099–1109PubMed Barkovich AJ (2000) Concepts of myelin and myelination in neuroradiology. AJNR Am J Neuroradiol 21:1099–1109PubMed
30.
go back to reference Rispoli P, Carzino R, Svaldo-Lanero T et al (2007) A thermodynamic and structural study of myelin basic protein in lipid membrane models. Biophys J 93:1999–2010CrossRefPubMedPubMedCentral Rispoli P, Carzino R, Svaldo-Lanero T et al (2007) A thermodynamic and structural study of myelin basic protein in lipid membrane models. Biophys J 93:1999–2010CrossRefPubMedPubMedCentral
31.
go back to reference Sternberger NH, Itoyama Y, Kies MW, Webster HD (1978) Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat C.N.S. J Neurocytol 7:251–263CrossRefPubMed Sternberger NH, Itoyama Y, Kies MW, Webster HD (1978) Immunocytochemical method to identify basic protein in myelin-forming oligodendrocytes of newborn rat C.N.S. J Neurocytol 7:251–263CrossRefPubMed
32.
go back to reference Hartman BK, Agrawal HC, Kalmbach S, Shearer WT (1979) A comparative study of the immunohistochemical localization of basic protein to myelin and oligodendrocytes in rat and chicken brain. J Comp Neurol 188:273–290CrossRefPubMed Hartman BK, Agrawal HC, Kalmbach S, Shearer WT (1979) A comparative study of the immunohistochemical localization of basic protein to myelin and oligodendrocytes in rat and chicken brain. J Comp Neurol 188:273–290CrossRefPubMed
33.
go back to reference Keupp J, Baltes C, Harvey PR, van den Brink J (2011) Parallel RF transmission based MRI technique for highly sensitive detection of amide proton transfer in the human brainProc 19th Annual Meeting ISMRM, Montreal, Quebec, pp 710 Keupp J, Baltes C, Harvey PR, van den Brink J (2011) Parallel RF transmission based MRI technique for highly sensitive detection of amide proton transfer in the human brainProc 19th Annual Meeting ISMRM, Montreal, Quebec, pp 710
34.
go back to reference Zu Z, Janve VA, Xu J, Does MD, Gore JC, Gochberg DF (2013) A new method for detecting exchanging amide protons using chemical exchange rotation transfer. Magn Reson Med 69:637–647CrossRefPubMed Zu Z, Janve VA, Xu J, Does MD, Gore JC, Gochberg DF (2013) A new method for detecting exchanging amide protons using chemical exchange rotation transfer. Magn Reson Med 69:637–647CrossRefPubMed
35.
go back to reference Lee JS, Xia D, Ge Y, Jerschow A, Regatte RR (2014) Concurrent saturation transfer contrast in in vivo brain by a uniform magnetization transfer MRI. Neuroimage 95:22–28CrossRefPubMedPubMedCentral Lee JS, Xia D, Ge Y, Jerschow A, Regatte RR (2014) Concurrent saturation transfer contrast in in vivo brain by a uniform magnetization transfer MRI. Neuroimage 95:22–28CrossRefPubMedPubMedCentral
36.
go back to reference Desmond KL, Moosvi F, Stanisz GJ (2014) Mapping of amide, amine, and aliphatic peaks in the CEST spectra of murine xenografts at 7 T. Magn Reson Med 71:1841–1853CrossRefPubMed Desmond KL, Moosvi F, Stanisz GJ (2014) Mapping of amide, amine, and aliphatic peaks in the CEST spectra of murine xenografts at 7 T. Magn Reson Med 71:1841–1853CrossRefPubMed
37.
go back to reference Cai K, Singh A, Poptani H et al (2015) CEST signal at 2 ppm (CEST@2ppm) from Z-spectral fitting correlates with creatine distribution in brain tumor. NMR Biomed 28:1–8PubMed Cai K, Singh A, Poptani H et al (2015) CEST signal at 2 ppm (CEST@2ppm) from Z-spectral fitting correlates with creatine distribution in brain tumor. NMR Biomed 28:1–8PubMed
38.
go back to reference Heo H-Y, Zhang Y, Jiang S, Lee D-H, Zhou J (2015) Quantitative assessment of amide proton transfer (APT) and nuclear Overhauser enhancement (NOE) imaging with extrapolated semi-solid magnetization transfer reference (EMR) signals: II. Comparison of three EMR models and application to human brain glioma at 3 T. Magn Reson Med. doi:10.1002/mrm.25795 Heo H-Y, Zhang Y, Jiang S, Lee D-H, Zhou J (2015) Quantitative assessment of amide proton transfer (APT) and nuclear Overhauser enhancement (NOE) imaging with extrapolated semi-solid magnetization transfer reference (EMR) signals: II. Comparison of three EMR models and application to human brain glioma at 3 T. Magn Reson Med. doi:10.​1002/​mrm.​25795
Metadata
Title
Amide Proton Transfer (APT) MR imaging and Magnetization Transfer (MT) MR imaging of pediatric brain development
Authors
Hong Zhang
Huiying Kang
Xuna Zhao
Shanshan Jiang
Yi Zhang
Jinyuan Zhou
Yun Peng
Publication date
01-10-2016
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 10/2016
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-015-4188-z

Other articles of this Issue 10/2016

European Radiology 10/2016 Go to the issue