대 한 방 사 선 의 학 회 지 1993 ; 29 (5) : 853~860 Journal of Korean Radiological Society, September, 1993

Iη Vivo lH MR Spectroscopy of Human Brain in Six Normal Volunteers*

Bo-Young Choe, Ph. D., Tae-Suk Suh, Ph. D., Yong-Whee Bahk, M.D. , Kyung-Sub Shinn, M.D.

DejJartment of R，αdiology， Kangnam 5t. M，α1')1’'s Hoφital， Catholic Universψ Medical College

- Abstract-

Iη vivo 'H MR spectroscopic studies were 'performe.d on the human brain in six normal volunteers. Some dis

tinct proton metabolites, such as N-acetylaspartate (NAA), creatinej phosphocreatine (Cr), cholinejphosphoch이ine

(Cho) , myo-inositol (Ins) and lipid (fat) were clearly identified in normal brain tissues. The signal intensity of

NAA resonance is strongest. The standard ratios of metabolites from the normal brain tissues in specific re­

gions were obtained for the references of further in vivo 'H MR spectroscopic studies. Our initial results sug­

gest the in vivo 'H MR spectroscopy may provide more precise diagnosis on the basis of the metabolic infor­

mations on brain tissues. The unique ability of in vivo 'H MR spectroscopy to offer noninvasive information

about tissue biocheIlÙstrγ in patients will stimulate its impact on clinical research and disease diagnosis.

Index Words: Magnetic resonance (MR) , Spectroscopy 40.1214

INTRODUCTION

The first , pioneering Nobel-prize-winning

nuclear magnetic resonance (NMR) experi­

ments were carried out in the 1940s by Purcell, Torey, and Pound (1) at Harvard University

and by Bloch, Hansen, and Packard (2) at Stan­

ford University. In 1950, Proctor (3) made a

critical observation that the specific resonance

frequency of a nucleus depended upon the na­

ture of its chemical and magnetic environment, leading to the definition of this phenomenon as

the chemical shift. 1’n medical field , NMR spec­

troscopy is just called MR spectroscopy or sim­

ply MRS since the word of “ nuclear" itself

made an undesirable impression to the patients

in general.

Over the last decade , in vitro MRS h as e­

volved into one of the most powerful methods

for deterrnining structure of biological macro­

molecules. This has opened a unique opportun­

ity for obtaining high- resolution three-dimen­

sional structures in aqueous solution under

physiological conditions, in contrast to the

well-established methods of x - ray crystallogra­

phy, which are applicable only to solids and in

particular, single crystals . 1:η vitro MRS has

been extensively applied in the structural analy­

sis of biological macromolecules (4-8). The de­

terrnination of three-dimensional conforma­

tions by iη vitro MRS represents and approach

to the understanding of the mechanisms of bio­

logical process in which biological macromole­

cules are involved.

Over the past few years, in vivo IH MRS has

* 본 논문은 가톨릭 중앙의료원 학술연구조성비로 이루어진 것임. 이 논문은 1993년 4월 6일 접수하여 1993년 6월 3일에 채택되었음.

Received April 6, Accepted July 3, 1993

@ …

Journal 01 Korean Radiological Society 1993; 29 (5) : 853~860

been successfully employed in living systems to

identify and quantitate the levels of biochemical

compounds, and to investigate the metabolism

and biochernistη of a variety of diseases and

disorders (9). Because in vivo lH MRS is a

rapid , sensitive, quantitative, noninvasive and

potentially risk-free method, it is a unique ana­

lytical method in clinical medicine that can ac­

cess to living cells and tissues directly without

any harm like magnetic resonance imaging

(MRI) (10 ,11). 1:η vivo 1 H MRS provides the

biochernical informations, such as the metabo­

lite levels between normal and neoplastic tissues

of brain, which can complement the results of

MRI exarninations in diagnostic radiology (1 2).

Studies with in vivo lH MRS become to be

possible in living organisms by the development

of pulse sequences that suppress the large pro­

ton signal from water and allow detection of

protons contained in compounds present at

lower concentrations. }η vivo lH MR spectra in

living systems are complex due to the narrow

spread of resonances . Unambiguous identifica­

tion of peaks is complicated by the presence of

signals from hydrogen nuclei with similar chem­

ical environments in different molecules.

Advantages of in vivo lH MRS include the abili­

ty for signal collection in a short time period

and the presence in the spectra of compounds

of biological importance that are affected by

early pathological process (13).

At starting stage with employing image­

guided water-suppressedη vivo IH MRS with

1.5 T MRlj MRS system, we have studied the

spectral patterns of a homogeneous group of

normal he허thy adults , and report the prelimi­

nary findings on the 1 H MR spectra of normal

brain tissues .

MATERIALS AND METHODS

During the period from December 1992 to

April 1993, six normal volunteers aged 19-41

years (median, 33 years) were examined with 10-

calizedη vivo lH MR spectroscopy by using

the PRESS (Pointing RESolved Spectroscopy)

and STEAM (STimulated Echo Acquisition

Method) CSI (Chemical Shift Iaging) pulse se­

quences (1 4). All of water- suppressed, localized

in vivo lH MR spectroscopic studies were per­

formed at 1.5 T whole body MRljMRS system

(Signa Advantage 4.7 Version, GE Medical

System, Milwaukee, Wisconsim, U.S.A.).

For three- dimensional representation, lH

,MR spectroscopic image (MRSI) of the human

brain was acquired from a 5 cm thick section

above the temple. The spectra were displayed

in their 2.5 x 2.5 cm voxels outlined by the pe­

ripherγ of the brain. The number of points in

axes was designed for 256 x 8 x 8. The spectral

grid was produced from CSI reconstruction

and auto-phased. Then, the spectral grid was

superposed on the corresponding MR image.

The localization was guided by T1-weighted, axial MR images obtained with 30 cm FOV

(field of view) and 5-mm thickenss as the first

step in the MR spectroscopic exarnination. T1-

weighted MR image was selected because of the

short time requirement. lH MR spectra were

obtained from nominal volumes of 8 cm3 (2 x 2

x 2 cm) localized in the brain tissue , such as

cerebral white matter, cerebral white and gray

matters, and thalamus. Spectral parameters

were as follows: 256 x 128 of acquisition matrix

number; 1 NEX (Number of EXcitation) of im­

aging time; 20-30 msec of echo time; 1.5-2

secs of repetition time; 128 of number of

averaging; 1000 Hz of spectral width; 1024 of

number of data points; 8 of phase cycle. The

total examination time per case was 30-60 min­

utes. All spectra were acquired with use of the

standard bird- cage quadrature head coil (GE

Medical Systems, Milwaukee, Wisconsin, U.S.

A.) that produces a uniform excitation frequen­

cy (63.86 MHz). All in vivo lH MRS data were

transferred to a Sun SPARC statÎon IPC (Sun

Microsystems, Mountain View, California, U.S.

A.) and processed by the SAGE data analysis

854 -

Bo-Young Choe, et al : In Vivo lH MR Spectroscopy of Human Brain in Six Normal Volunteers

package (GE Medical Systems, Milwaukee, Wis­

consin, U.S.A.).

The homogeneity of the magnetic field was

optirnized by shimrning procedure focused on

the water signal. In order to maxirnize the

water suppression, special attention was given

to l()cating the water signal exactly at the carri­

er frequency at the end of the shirnming proce­

dure. The raw data of free induction decay

(FID) were created from completion of scan

averages per examination. An exponential mul­

tiplication of line broadening 1-2 Hz was ap­

plied for apodization of suppressing the noise

level. After one-dimensional Fourier transfor­

mation, the spectra were phased manually by

zero and first order phase correction. AlI spec­

tra were plotted in the pure absorption mode.

Chemical shifts in the water-suppressed lH

spectra were referenced to the position of

water. The location of the water signal, which

was set to 4.77 ppm relative to tetramethylsi­

lane (TMS) at 0.0 ppm, was determined pre­

cisely from the water peak position in the un­

suppressed spectrum (1 5). Proton resonances in

the spectra obtained from normal brain tissues

were tentatively assigned on the basis of prior

assignments (1 6) .

RESULT

Fig. 1 is a representative of lH MR MRSI of

the normal brain with the 8 x ,8 grid overlaid

on 256 data points with using STEAM CSI

pulse sequence. There is a correspondence be­

tween the image and spectrum with some spuri­

ous peaks arising in outlying voxels. A few sig­

nals in outlying voxels are apparently artifactual

due to signal contarnination. The only water

and lipid peaks are predorninantly shown in

Fig. 1 because of relative intensity scale for

total 64 grids

Fig. 2. shows the T1-weighted axi때 MR

image of normal tissue defining the Volume Of

Interest (VOI) in the cerebral white matter of

Fig. 1. 'H MR spectroscopic image (MRSI) of the normal brain with the 8 x 8 grid overlaid on 256 data points with using STEAM CIS pulse sequence.

Fig. 2. Tl-weighted axi떠 MR image of the normal brain trssue defining the voxel (not angulated) in the white matter of the right parietal lobe selected for 10-calized in vivo 'H MRS

the right parietal lobe selected for localized iη

vivo lH MRS. The size of VOI located within

the cerebral white matter is 2 x 2 x 2 cm3 corre-

짜 …

Journal of Korean Radiological Society 1993; 29 (5) : 853~860

sponding to a volume of 8 ml. A typical water­

suppressedη vivo I H MR spectrum obtained

from the right cerebral white matter of the

brain of a normal volunteer is shown in Fig. 3.

Fig. 4 shows the T1-weighted axial MR image

of normal tissue defining the VOI in the left

thalamus. The size of VOI located within the

thalamus is 2 x 2 x 2 cm3• A typical water-sup­

pressed iη vivo IH MR spectrum obtained from

the left thalamus of the brain ofa normal vol­

unteer is shown in Fig. 5 . The predominant

components of human brain tissues consist of

NAA, Cr, Cho and lipid. Resonance line assign­

ments of m맹or metabolits are NAA, 2.02 ppm;

Cr, 3.05 ppm; Cho , 3.22 ppm; lns , 3.57 ppm.

A standard ratio of Crj Cho, NAAj Cho, NAAj

Cr for normal brain tissue in the various re­

gions is shown in Table 1. Values given in

Table 1 are mean :t standard deviation

ln all six normal volunteers , the consistent

MR peaks of the proton metabolites were dem­

onstrated . The spectral patterns were slightly

different on the basis of the regions and the in­

teresting VOls (17). ln Table 1, the minimal

standard deviations show that the reproducible

MRS results can be obtained from the specific locations .

NAA

Ins Cr ns Cho

ppm

Fig. 3. A typic외 water-suppressedη vivo 'H MR spectrum obtained from the white matter of the right parietal lobe of the normal brain tissue. Chemical shifts are indicated in parts per million (ppm).

DISCUSSION

Protons were initially selected because of

the highest natural abundance and the high rel­

ative receptivity in the biological systems. Due

to its increased sensitivity, localized in vivo I H MRS allows the examination of considerably

Fig. 4. Tl -weighted <Lxial MR imag eof normal tis­sue defining the voxel (not angulated) in the left thal­amus

NAA

까/\때μ씨

ppm

Fig. 5. A typic따 water-suppressed in vivo IH MR spectrum obtained from the left thalamus. Chemical shifts are indicated in parts per million (ppm)

856 -

Bo-Young Choe, et al : In Vivo lH MR Spectroscopy of Human Brain in Six Normal Volunteers

Table 1. }η Vivo lH MRS Signal Intensity Ratio of Major Proton Metabolites in Normal Brain Tissues of Adult.

Site of Number of Sex/ Mean Cr/Cho NAA/ Cho NAA/ Cr brain tissue volunteers Age(yr)

Cerebral white matter (parietallobe) 2 M/ 30.5 1.1 :t 0.2 2.2 :t 0.l 1.9 :t 0.l

Thalamus 2 M/ 40.5 2.0 :t 0.2 3.5 :t 0.5 1.8 :t 0.2

Cerebral white and gray matters* 2 M/ 27.5 2.9 :t 0.5 5.6:t 1.0 2.0 :t 0.l (posterior temporallobe)

* One of normal volunteers might be in motion during MR scans .

smaller volumes (up to 1 x 1 x 1 cm3 for l.5 T

system). In most of in vivo lH MRS studies,

MRS was used to investigate the ce l1ular pro­

cesses in isoltion or the influences of different

processes in isolation on the resonance of water

in intact ce l1s. However, in vivo lH MRS con­

fronted two major problems. First, lH MRS

produces many overlapping peaks and the verγ

complex spectra because of the large number

of metabolities. Coupling effect between the

spins of particular protons causes resonance to

occur as doublets , triplets, or more complicated

multiplets. Second, the application of in vivo lH

MRS to the study of living tissue has been dis­

turbed by the technical problems posed by the

presence of 110 molar concentration of the

water signal. The relative size of this signal can

now be reduced substantially by a variety of

water suppression pulse sequences, such as

PRESS ans STEAM pulse sequences. A large

number of proton-containing metabolites can

be detected when these methods are employed.

Unlike MRI, MRS requires the shimrning pro­

cedure for homogeneous magnetic field. The

spectral line width related with resolution or

quality of spectrum is critical1y dependent upon

the shimming procedure. Hence, the shimrning

procedure is quite important for the produc­

tion of best qu떠ity of MR spectrum.

We have demonstrated the ability of non-in­

vasive technique, localized in r,;ivo lH MRS to

monitor metabolic levels of human brain tissues

in normal volunteers for the first time in

Korea. A high degree of regional localization of

the iη νivo 1 H MR signal is achieved by PRESS

and STEAM pulse sequences. A related modali­

ty, lH MRSI is evolving and can contribute to

the understanding and management of diseases.

The technique of lH MRSI with STEAM CSI

pulse sequence needs to be more improved for

the prevention of signal contarnination of

adjacent grids. Since the absolute concentra­

tions and the relaxation times of brain metabo­

lite play a critical role in enhancing the signal

intensities, the relative ratios of each brain me­

tabolite became a protocol to analyze the in

vivo MR data set. In Figs. 3 and 5, the spectral

patterns and the relative ratios of brain metabo­

lites were different on the basis of the region of

tissues even in same normal volunteer. The rel­

ative proton metabolite ratios of the cerebral

white matter are in good agreement with Kugel

et al. (1 992) (1 8). NAA is located almost exclu­

sively in neurons (1 9), and believed to be a

neuronal marker (20). Cho is a precursor for

the biosynthesis of membrane lipids . The cho­

line-containing membrane phosph이ipids are

released during active myelin breakdown (21).

Besides NAA, Cho, Cr and Ins, Figs. 3 and 5

show the other proton metabolites , such as

GABA (y-aminobutyric acid; 2.25 ppm) , gluta­

mate (2.35 ppm) and some amrnino acids. In

addition to normal adult brain tissue, in vivo lH

MRS has been used for the investigation of

neonatal cerebral metabolism and function

(22).

It is clear that in vivo 1 H MRS offers the

new biochernical insights in vivo as wel1 as clini-

@ ”

Journal 01 Korean Radiological Society 1993; 29 (5) : 853~860

cal applications to various states of metabolic or

biochemical disorders and the best and possibly

the only hope for performing a noninvasive biopsy (23). The extra-dimension of in viνo lH

MRS has both genuine clincal value for diag­

nosing disease and evaluation therapy, and sci­

entific value as a new source of functional in­

formations about the nature of disease states.

The correlations between MRS and MR1 may

lead to the development of a set of

physiological, anatomical , and biochemical indi­

ces that will provide a valuable approach for in­

vestigating the underlying basis for many clini­

cal disease and disorders. The recent develop­

ment of spatially localized in vivo 1 H MRS

methods that sample the relative levels of mo­

bile metabolites from a volume of interest de­

fined from an MR image, has provided the val­

uable biochemical data base for integrating the

anatomical and pathological informations ob­

tained from MRI. The combination of anatomi­

cal informations by MR1 and biochemical meta­

bolic informations by in vivo 1 H MRS offers the

new means for understanding the origins and

the time course of progression in a variety of

disease and the bright prospect in the diagnos­

tic radiology (24).

The techniques of in vivo 1 H MRS have

been currently confronted many difficulties.

The signal-to-noise ratio is relatively poor be­

cause of the low concentrations (about 10 mM)

of proton metabolites in tissues. The signal-to­

noise ratio increases approximately linearly with

magnetic field strength. Therefore, the highest

available field should be desirable for optimum

sensitivity and resolution. Presently, whole body

magnets of up to 4 T are available although

magnets of 1.5 T to 2.0 T are more common.

1n addition to increasing of magnet field

strength to enhance the signal-to-noise ratio ,

two other available options are the expansion

of the voxel size and the increase of the num­

ber of scan averages. However, the tumor size

and interesting V01s are sometimes minimal ,

858

and the instrumental time is relatively expen­

sive. The instrumental time may be minimized

by upgrading the hardwares and the operating

system. Also, the coarse spatial resolution may

be improved by developing the efficient pulse

sequences. The magnet homogeneity is a criti­

cal part of spectroscopic protocal. 1t is impor­

tant that eddy currents generated in the mag­

net structure by the switching of the magnet

field gradient coils be kept to a minimum. The

procedures of data acquisitions and analysis re­

quire the sophisticated skill and techniques.

Moreover, the detailed interpretation of MRS

results requires the highly advanced knowledge

of biochemistπ and molecular pathophysiology.

The biochemical functions of proton meta­

bolities in brain tissue have not been fully un­

derstood.

The ratio of metabolites from the brain dis­

eases will be compared for the precise diagnosis

on the basis of the standard ratio of metabo­

lites from the normal healthy brain tissues in

specific regions , such as cerebral white matter, cerebral white and gray matter, and thalamus

With employing image-guided water-sup­

pressed iη vivo lH MRS , the further studies on

the variety of brain diseases including tumors

are in progress in our facility.

1n conclusion, in vivo lH MRS provides the

promising informations of brain metabolism

that cannot be obtained by any other modalities

in the human brain. Therefore, it is a useful

modality for accurate diagnosis , the evaluation

of the treatment and the biochemical and

physiological analysis. 1t is necessary to contin­

ue developing the in 띠vo 1 H MRS as a routine

method in the clinical area.

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인체 뇌의 국한성 생체내 양성자 자기공명분광법

가톨릭대학교 의과대학 방사선과학교실

최보영·서태석·박용휘·신경섭

뇌의 생화학적 대사성분과 함량을 토대로 정밀 진단법의 원안을 확립하여 진단 수준을 향상시키고저 6명의 자원자

정성 성인에 대해서 1. 5 T를 사용한 국한성 생체내 양성자 자기공명분광법을 이용한 연구를 시도하였다.

정상 뇌조직내 N - acetylaspartate (N AA), creatine/ phosphocreatine (Cr) , choline/ phosphocholine (Cho) ,

myo-inositol ( Ins)과 lipid ( fat) 는 양성자 자기공명분광 스팩트럼상에서 관측할 수 있었다. 정상인의 뇌조직상에서

는 NAA 자기공명신호가 양성자 물질대사 중 가장 큰 세기를 나타냈다. 자기공영분광 스팩트럼에 표출된 정상인의

뇌조직 대사성분들의 상대적 비율평균치를 뇌이상조직 환자의 것과 차후에 비교하기 위하여 산출하였다. 정상 성인

뇌조직내 Cr/ Cho , NNA/Cho , NNA/Cr의 상대적 비율치는 T able 1에서와 같이 두정엽백질에서 1.1:t O. 2, 2.

2 :t α 1, 1. 9:t O. 1, 시상에서 2. O:t o. 2, 3. 5:t O. 5, 1. 8:t O. 2, 후방측두엽 백회질에서 2. 9:t O. 5, 5. 6:t 1. 0, 2. O:t O. 1

로 각각 정량분석되었다.

저자들의 예비결과는 뇌조직의 생화학적 대사에 관한 비침습적 정보를 제공하는 국한성 생체내 양성자 자기공명분

광법이 보다 정확하고 민감한 방법으로 뇌조직내 양성자 대사성분의 종류와 함량을 정량분석할 수 있으므로， 앞으로

임상얀구와 뇌질병진단에 획기적인 기여를 할 것이며， 또 임상진단검사방법중 각광받을 첨단검사방법이 될 것으로

사료된다.

860 -