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Rev Esp Med Nucl Imagen Mol.

2015;34(2):8994

Original article

A novel, fully automated, observer-independent program for


semiquantifying striatal 123 I-FP-CIT uptake
P. Tamayo a,c,,1 , C. Montes b,c,1 , M.E. Perez b , E. Martin a , J.R. Garca-Talavera a
a
Nuclear Medicine Department, University Hospital of Salamanca, Spain
b
Medical Physics Department, University Hospital of Salamanca, Spain
c
Institute of Biomedical Research of Salamanca, Spain

a r t i c l e i n f o a b s t r a c t

Article history: Objective: To describe and validate a novel, fully automated program specically designed for the semi-
Received 11 April 2014 quantication of striatal 123 I-FP-CIT uptake using volumes of interest (VOI) analysis.
Accepted 20 August 2014 Material and methods: The proposed algorithm is based on a template that mimics the striatal 123 I-FP-CIT
Available online 8 October 2014
uptake in a healthy subjects, derived from dened anatomical VOIs available from WFU PickAtlas. Four
SPECT studies of the anthropomorphic Alderson phantom lled with variable radioactive concentrations
Keywords: were acquired for the experimental validation. Experimental SPECT images were spatially normalized
123
I-FP-CIT SPECT
with respect to the previously created template. The binary VOIs corresponding to left caudate and puta-
VOI analysis
SPM
men and right caudate and putamen, which were used to construct the template, were projected onto
Alderson RSD phantom the experimental images to obtain the counts for these regions. To minimize the partial volume effect, a
Striatal uptake semiquantication percentage of the voxels in these regions (threshold), rather than all of them, was used. A binary occipital
VOI was used to quantify the non-specic uptake. Experimental binding potentials (BPs) were calculated
from the counts in these regions. True BPs were calculated from aliquots taken from the solutions used
to ll the phantom.
Results: There were statistically signicant differences in the experimental BP values (p < 0.002) accord-
ing to the percentage of voxels used. A highly signicant correlation was achieved between true and
experimental BP values, regardless of the percentage of voxels included for quantication.
Conclusions: Our novel, observer-independent program automatically performs the semiquantication
of striatal 123 I-FP-CIT uptake in experimental studies.
2014 Elsevier Espaa, S.L.U. and SEMNIM. All rights reserved.

Un nuevo programa, totalmente automtico e independiente del observador


para semi-cuanticar la captacin estriatal de 123 I-FP-CIT

r e s u m e n

Palabras clave: Objetivos: Describir y validar un nuevo software, totalmente automtico, especcamente disenado para
123
I-FP-CIT SPECT semi-cuanticar la captacin estriatal de 123 I-FP-CIT usando volmenes de inters (VOIs).
Anlisis de VOIs Material y mtodos: El algoritmo propuesto se basa en una plantilla que remeda la captacin estriatal
SPM
de 123 I-FP-CIT en un sujeto sano, obtenida a partir de VOIs anatmicos denidos en WFU PickAtlas. Para
Maniqu RDS Alderson
la validacin experimental de este algoritmo se adquirieron 4 estudios SPECT del maniqu antropomr-
Semicuanticacin de la captacin estriatal
co Alderson llenado con concentraciones radioactivas variables. Las imgenes SPECT experimentales se
normalizaron espacialmente respecto a la plantilla creada. Los VOIs binarios correspondientes a ncleo
caudado y putmen derechos e izquierdos, utilizados para disenar la plantilla, se proyectaron sobre las
imgenes experimentales para obtener las cuentas en estas regiones. Para minimizar los efectos de vol-
umen parcial se utiliz un porcentaje de vxeles, en vez de utilizar todos los vxeles contenidos en estos
VOIs. Se ha utilizado un VOI binario situado en regin occipital para cuanticar la unin no especca.
Los potenciales de unin (BPs) experimentales se calcularon a partir de las cuentas obtenidas en estas
regiones. Los BPs reales se calcularon a partir de alcuotas tomadas de las soluciones utilizadas para llenar
el maniqu.
Resultados: Hubo diferencias estadsticamente signicativas en los BPs experimentales en funcin del
porcentaje de vxeles utilizados para la cuanticacin (p < 0.002). Se alcanz una alta correlacin entre
los BPs reales y los experimentales, independientemente del porcentaje de vxeles utilizados para la
cuanticacin.

Corresponding author.
E-mail address: ptamayo@usal.es (P. Tamayo).
1
Both authors contributed equally to this work.

http://dx.doi.org/10.1016/j.remn.2014.08.004
2253-8089/ 2014 Elsevier Espaa, S.L.U. and SEMNIM. All rights reserved.
2253-654X/
90 P. Tamayo et al. / Rev Esp Med Nucl Imagen Mol. 2015;34(2):8994

Conclusiones: Este nuevo programa automtico e independiente del observador realiza la semicuanti-
cacin de la captacin estriatal de 123 I-FP-CIT en estudios experimentales.
2014 Elsevier Espaa, S.L.U. y SEMNIM. Todos los derechos reservados.

Introduction (available from Radiology Support Devices Inc. and provided by


GE-Healthcare), which reproduces the striatal morphology. VOIs
Parkinsons disease (PD) is a progressive neurodegenerative corresponding to left and right caudate and putamen and to a
disorder characterized by the motor triad of tremor, rigidity and reference area (occipital area) were then applied to spatially nor-
bradykinesia. These symptoms are associated with the loss of malized phantom images to obtain the count statistics for these
dopaminergic neurons in the substance nigra pars compacta, the regions and thereby to calculate the binding potentials (BP). These
presence of ubiquinated protein deposits in the cytoplasm of neu- procedures were performed with Statistical Parametrical Mapping
rons, and a subsequent decline in dopamine levels in the striatum, software (SPM8).10 The details of the process are described in the
which is required to control movement.1 following sections.
123 I-FP-CIT, a radioiodinated cocaine analog, is a radiophar-

maceutical that binds specically, though not selectively, to Construction of the template
presynaptic dopamine transporters (DATs) in vivo. This enables
the study of nigrostriatal dopaminergic system integrity, which is As SPM does not have a specic template for the striatal
altered in PD and preserved in essential tremor and drug-induced uptake of 123 I-FP-CIT, it is necessary to create one that resem-
parkinsonism, by means of the Single Photon Emission Com- bles this uptake.13 SPM contains the WFU PickAtlas toolbox,11,12
puted Tomography (SPECT) imaging technique.2 In routine clinical which enables anatomical VOIs as binary masks to be dened. The
practice, results of 123 I-FP-CIT SPECT are qualitatively evaluated,2,3 Anatomical Automatical Labelling atlas14 was selected in the soft-
although this involves a degree of subjectivity and some uncer- ware WFU PickAtlas and four binary VOIs, left and right caudate
tainty about incipient parkinsonism. The results are categorical, and putamen, representing striatal structures, were used. The vol-
and so cannot fully reect the continuous characteristics of clinical ume of these VOIs was 4.95, 4.96, 9.35 and 9.24 ml for left and right
variability and disease progression. However, accurate semiquan- caudate and putamen, respectively. These regions are dened in
tication of DAT binding could be helpful in the early stages of PD the standard space of the Montreal Neurological Institute (MNI). To
to detect subtle changes in DAT binding,4 and in sequential stud- reproduce the background uptake in 123 I-FP-CIT patient studies, the
ies to monitor disease progression57 and the benecial effects of a priori maps of gray and white matter included in SPM were added.
putative neuroprotective drugs.8 These maps were also dened in the MNI space. The template
DAT binding is usually quantied as the ratio of specic bind- was built adding the following binary VOIs: left and right caudate
ing in striatal regions to nonspecic binding in a reference region nucleus, with a weighting factor of 4; left and right putamen, with
devoid of DAT. There are several methods for quantifying DAT den- a weighting factor of 2; and a background region with a weight-
sity using regions of interest (ROI) in which striatal regions are ing factor of 1. These weighting factors were selected to mimic the
usually manually delineated in the reconstructed SPECT images. 123 I-FP-CIT uptake of a subject who had involvement of striatal
The results obtained are expressed as a continuous rather than uptake in a moderate degree. This template is used to spatially
a categorical variable, thereby reecting the great clinical vari- normalize all the studies in the same space, both healthy and patho-
ability more fully. However, such techniques based on manual or logical subjects. If similar weighting factors would had been applied
semiautomatic ROIs are operator-dependent and so are prone to a for putamen as for caudate a good normalization would be achieved
considerable inter- and intraobserver variability that is no longer in healthy subjects but not in pathological ones. On the contrary, if
considered acceptable in clinical practice or research studies.9 the weighting factors applied were much higher for caudate than
Therefore, automated observer-independent systems are required for putamen, a good normalization would be achieved in patholog-
for several reasons: to overcome observer dependency and min- ical subjects but not in healthy ones. The template obtained in this
imize variability, to provide 3D information that reects the way is of high resolution.
structure of the entire striatum, and to standardize the semiquan- The 123 I-FP-CIT SPECT images of patient studies are affected by
tication process, so enabling the comparison of data from different the characteristic low resolution of images obtained with gam-
centers. macameras and thus differ from the high-resolution template
Here we propose a novel fully automated observer-independent built here. To transform the high-resolution template to a low-
program specically designed for processing and quantifying 123 I- resolution one an 8 mm 8 mm 8 mm full width at half maximum
FP-CIT SPECT images using volumes of interest (VOI) analysis. The (FWHM) 3D Gaussian lter was applied. The low-resolution tem-
method is based on a specic low-resolution template that rep- plate obtained is shown in Fig. 1.
resents a realistic simulation of the activity distribution from the
basal ganglia of a healthy subject. Experimental validation of this
Experimental studies
method with an anthropomorphic striatal phantom (Alderson RSD
phantom) is presented.
Four SPECT studies of the anthropomorphic Alderson phantom
were acquired to validate the proposed quantication method.
Material and methods With the rst acquisition, referred to as the reference acquisi-
tion, both caudate and putamen contained the same radioactive
The proposed algorithm is based on a template that mimics stri- concentration of approximately 150 kBq/ml of 123 I-NaI. The back-
atal 123 I-FP-CIT uptake in a healthy subject. The aim of creating this ground chamber, mimicking the cerebral cortex, was lled with a
template was to have a common stereotactic space to t 123 I-FP-CIT radioactive concentration of 19.0 kBq/ml solution. After this ref-
SPECT images of patients so that comparisons can be made. Patient erence SPECT acquisition, three acquisitions were performed by
studies have not been used in this work. Instead, experimental reducing sequentially the radioactive concentration of striatum.
studies were made with the anthropomorphic Alderson phantom The rst was acquired by reducing the concentration of the right
P. Tamayo et al. / Rev Esp Med Nucl Imagen Mol. 2015;34(2):8994 91

Figure 1. Low-resolution template designed with 3D binary regions that mimics 123 I-FP-CIT striatal uptake in a healthy subject.

putamen (lled with a solution of 110 kBq/ml), the second by reduc- to account for global shape differences (which is not done by the
ing of the left putamen (lled with a solution of 54.8 kBq/ml) and afne registration) between the studies and the template. This
the third by reducing the concentration of left caudate (lled with spatial normalization allowed us to have all the experimental
a solution of 87.7 kBq/ml). images and the template in the same anatomical space, enabling us
The four experimental SPECT studies were acquired with a to assume voxel-to-voxel correspondence. These co-registrations
dual-head rotating gamma camera (Axis, Picker) tted with an were visually validated.
ultra-high-resolution fan-beam collimator. SPECT data were col-
lected in a 128 128 matrix, for 35 min, in step-and-shoot mode VOI analyses and experimental BP calculations
(120 steps, 3 , 35 s per step) with a symmetrical window of 20%
centered on a 159 keV 123 I photopeak. Images were reconstructed VOIs that t the 3D shape of striatal structures are needed to
using an OSEM algorithm (4 iterative steps). The postltering used semiquantify the striatal uptake of 123 I-FP-CIT. To do this, pre-
in this study was a low-frequency lter (Low-Pass, order 5 and viously used high-resolution binary VOIs corresponding to left
cut-off 0.40/cm). The images were corrected for attenuation by the caudate and putamen and right caudate and putamen were used to
Chang method using an attenuation coefcient of 0.04/cm, obtained construct the template. As these regions were in the same space as
experimentally for this equipment with a uniform phantom lled in normalized studies, they were projected onto the experimental
with 123 I. The isotropic voxel size of the reconstructed studies was images to obtain the counts in these regions (Fig. 2).
2.6 mm. The spatial resolution (FWHM) of the camera tted with The log roi batch function16 allows mean counts to be made in
ultra-high-resolution fan-beam collimators, at 15 cm from the col- a VOI. However, in small volumes, such as striatal structures, there
limator surface, is 8.6 mm. is a count loss due to the partial volume effect (PVE) and the mean
Aliquots of 0.1 ml of each solution used to ll the four striatal count of all the voxels contained in a VOI is not a good estimator
regions and the background chamber were taken to obtain accurate of the activity concentration in that VOI. To minimize the effect,
radioactive counts in each region. These aliquots were measured in it is necessary to establish a threshold as a percentage of voxels
a NaI well counter 20 h after SPECT images were acquired to mini- with the higher counts. For this purpose the log roi batch function
mize count loss due to dead time. The dead time of the system was was modied in such way that the counts in the VOI were ranked in
always less than 1%. In any case the system automatically corrects decreasing order and then a range of percentages of voxels with the
for dead time providing both the real time and the live time. True BP higher counts (550%) were selected. The mean count of selected
values were calculated as BPtrues = (aliquot counts background voxels was calculated for each threshold.
counts)/background counts. A binary occipital VOI was dened in the reference phantom
image using MRICro software. The original log roi batch func-
Spatial normalization tion was used to obtain the mean counts in this background
region in order to quantify the non-specic radiotracer uptake.
Once SPECT studies had been acquired and reconstructed, they Experimental BP were calculated as BPexperimentals = (striatal
were transferred via DICOM to a PC and converted to Nifti format by activity occipital activity)/occipital activity.
means of the free MRICro software.15 Then, by SPM8, experimental
images were spatially normalized to the previously created tem- Statistics
plate. This spatial normalization consisted of 12-parameter afne
transformations composed of 3 translations, 3 rotations (rigid- Pearson correlation coefcients (r) between true and exper-
body), 3 shears and 3 zooms. Nonlinear warps were then performed imental BP values were calculated and considered statistically

Figure 2. 3D binary regions projected onto the reference phantom acquisition used to calculate experimental BP values.
92 P. Tamayo et al. / Rev Esp Med Nucl Imagen Mol. 2015;34(2):8994

Table 1 0.976
True and experimental BP values in striatal structures obtained with different voxel
thresholds for the four acquisition performed with phantom.

Pearson correlation coefficient (r)


True BP Experimental BP
0.974
Threshold

5% 15% 25% 35% 50%

Reference acquisition 0.972


Right C 6.57 3.42 3.12 2.91 2.73 2.48
Left C 6.57 3.25 3.00 2.80 2.62 2.37
Right P 6.57 3.32 3.00 2.75 2.54 2.28
Left P 6.57 3.47 3.09 2.83 2.63 2.36 0.97
2nd acquisition
Right C 6.57 3.34 3.01 2.78 2.59 2.33
Left C 6.57 3.34 3.02 2.80 2.60 2.35
Right P 5.03 2.76 2.47 2.26 2.09 1.86 0.968
0 10 20 30 40 50
Left P 6.57 3.56 3.22 2.95 2.73 2.45
Threshold (%)
3rd acquisition
Right C 6.57 3.26 2.96 2.75 2.55 2.28
Figure 3. Pearson correlation coefcients between true and experimental BP values
Left C 6.57 3.25 2.87 2.59 2.38 2.11
for different percentages of voxels (thresholds).
Right P 5.03 2.68 2.40 2.18 2.01 1.78
Left P 2.28 1.58 1.41 1.28 1.18 1.03
3
4th acquisition
Right C 6.57 2.95 2.68 2.45 2.20 1.83
Left C 3.92 1.91 1.72 1.55 1.37 1.10
Right P 5.03 2.51 2.27 2.09 1.92 1.68
Left P 2.28 1.45 1.23 1.05 0.91 0.74

C = Caudate nucleus, P = Putamen. 2


Experimental BP

signicant at an -level of <0.05. One-way ANOVA was used to


test whether the range of percentages of used voxels resulted in
statistically signicant differences in experimental BP values. 1

Results

The experimental BP values of right caudate and putamen and


left caudate and putamen regions, obtained by the quantication 0
1 2 3 4 5 6 7
method presented here and using different percentages of voxels,
Trues BP
are shown in Table 1. True BPs are also displayed in this table. It
can be seen that the lower the percentage of voxels included in Figure 4. Scatter plot of the true and measured BP values for the 25% threshold in
the quantication the higher the experimental BP values obtained, the right and left caudate and putamen regions.
probably due to the weaker inuence of the partial volume effect.
There were statistically signicant differences between the caudate and putamen and occipital regions to measure radiotracer
experimental BP values for all the thresholds analyzed (p < 0.002). uptake in these regions and thereby to calculate the BP values.
Specically, signicant differences were observed between the 5 The availability of an automated image-analysis program would
and 50% (p < 0.005) thresholds but not between the others (15%, be desirable for diagnosing PD in its early stages, so that subtle
25% and 35%). This means that either of the later thresholds might changes in DAT binding can be detected, and for monitoring disease
be used to quantify striatal 123 I-FP-CIT uptake. progression and the benecial effects of putative neuroprotective
A highly signicant correlation was noted between true and drugs. This novel program is fully automated once transverse slices,
experimental BP values, regardless of the percentage of voxels which have already been reconstructed and attenuation-corrected
included for the quantication, with the highest Pearson correla- on the departments workstation, have been transferred to the PC
tion coefcient recorded for the 25% threshold (r = 0.975, p < 0.0001; via the DICOM protocol. All subsequent processing is accomplished
Fig. 3). The scatter plot of the true and measured BP values for the rapidly (within 15 min) and without any manual intervention. Thus,
25% threshold in the right and left caudate and putamen regions the process is not too time-consuming for the operator and is
(R2 = 0.950, p < 0.0001) is displayed in Fig. 4. We therefore used observer-independent.
the 25% threshold to calculate the experimental BP values, which Several automated quantication programs have been pro-
proved to be approximately 43% of the true values. posed, but none have been universally accepted as a standard
method of quantication.17 In 2007, Calvini and coworkers
Discussion designed an algorithm named BasGan (the acronym derived from
basal ganglia),18 based on a high-denition (3D) striatal tem-
Our results show that a novel, fully automated, observer- plate derived from the Talairach atlas, which is converted to a
independent program, specically designed for processing and low-resolution template by applying a 3D Gaussian lter. This low-
quantifying 123 I-FP-CIT SPECT images using VOI analysis, works resolution template is meant to represent the striatal radiotracer
under experimental conditions and may be of great value for quan- uptake of a healthy subject. The algorithm automatically makes
tifying striatal uptake in clinical practice. This program is based on the transformation necessary to achieve optimal positioning of the
a specic low-resolution template that realistically simulates the 3D striatal template on the 123 I-FP-CIT SPECT images of the patient.
distribution of activity from the basal ganglia of a healthy subject, However, these SPECT images of patient previously need to be man-
and on the use of VOIs representing left caudate and putamen, right ually oriented so that they lie parallel to the bicommissural line
P. Tamayo et al. / Rev Esp Med Nucl Imagen Mol. 2015;34(2):8994 93

(AC-PC position), which requires operator intervention, whereas semiquantication of striatal uptake of 123 I-FP-CIT reveals a close
our method is fully automatic and independent of operator. With correlation between true and experimental BP values.
the BasGan program, which includes PVE correction, the authors In general, the BPs values obtained depend on the equipment
found a highly signicant correlation between true and experi- and the methodology used to acquire the images as well as the
mental BP values (r = 0.97) in the phantom images (as we found in method used for the semiquantication. The algorithm proposed
ours), and more accurate semiquantitative results following PVE by us aims to control the variability due to the semiquantica-
correction. Despite the very close correlation between true and tion since it is a fully automated observer-independent program. To
experimental BP values in the phantom studies, the BP obtained control the variability due to both the equipment and the method-
in the regions with the lowest radiotracer concentrations led to an ology used it would require to acquire experimental studies with
overestimation of the counts, which might have been due to an phantoms for correction factors then applied to clinical studies with
overcorrection of PVE. We did not perform PVE correction, which patients.27
may explain why our experimental BP values were lower (43%) than The software proposed by us is neither freely downloadable
the true BP values. from the web nor offered commercially, but rather is designed to
Tossici-Bolt et al.19 proposed the Southampton method as be developed in individual centers, where the VOIs and thereby
another automated DAT quantication method. It uses geometri- the template for standardizing clinical studies must be created and
cal VOIs for the striatum, which are large enough to ensure the the 123 I-FP-CIT uptake in the VOIs quantied. These steps may seem
inclusion of all the counts detected outside the physical volume somewhat complex, but detailed information about how to perform
of the structures due to the PVE, and a reference VOI for measur- each of the steps is provided in the materials and methods sec-
ing the specic to non-specic ratio. Thus, this technique accounts tion of this paper. Furthermore, todays Nuclear Medicine Services
for the PVE by measuring total striatal uptake. However, measure- include other professionals such as engineers or medical physicist,
ment of total striatal uptake is a limitation of this method because who are familiarized with Matlab and SPM platforms for processing
it obviates subdivision into striatal subregions such as the head and quantication of medical images, and therefore are capable to
of the caudate and the putamen tail. Intra-striatal quantication implement this method without much difculty.
might improve discrimination between normality and disease as
well as providing futher information about disease severity and
Conclusion
progression.2022 The VOIs are manually positioned, which results
in intra- and inter-observer variability of 3% and 4%, respectively,
The algorithm described here is novel, fully automated, and
for experienced operators. The method we propose resolves these
observer-independent. The program has been specically designed
constraints since it is completely automatic and uses subregions
for processing and quantifying 123 I-FP-CIT SPECT images using VOI
within the striatum, which yields more information about disease
analysis. It has been shown to work effectively in phantom studies.
severity and progression.
BRASS23 is a commercial program running on the Hermes work-
station (Nuclear Diagnostics, Stockholm, Sweden). It uses a map of Conicts of interest
anatomical VOIs obtained from the MRI of a control patient. Clinical
studies are registered on the 123 I-FP-CIT template, obtained from The authors have no conicts of interest to declare.
healthy subjects. A VOI map is used to adjust the patient striatal
VOIs to compensate for individual anatomic variations in order to
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