Original article

Usefulness of a deep-inspiration breath-hold 18F-FDG
PET/CT technique in diagnosing liver, bile duct,
and pancreas tumors
Shigeki Nagamachia, Hideyuki Wakamatsua, Shogo Kiyoharaa, Seigo Fujitaa,
Shigemi Futamia, Hideo Aritaa, Ryuichi Nishiia, Shozo Tamuraa
and Keiichi Kawaib
Background The deep-inspiration breath-hold18
F-fluorodeoxyglucose PET/computed tomography (DIBH
18
F-FDG PET/CT) technique improves the limitations ofdiagnosing a lesion located in an area influenced byrespiratory motion that brings about spatial misregistration
caused by respiration between PET and CT. However, its
clinical effectiveness with regard to abdominal lesions
has not been elucidated. The influence of respiratory
motion for calculating the maximal standardized uptake
value (SUVmax) and metabolic volume (MV) in DIBH
18
F-FDG PET/CT has not been investigated either.
Objective The purpose of this study was to investigate
the usefulness of the DIBH 18F-FDG PET/CT technique indiagnosing liver tumors, bile duct cancers, and pancreas
tumors. In addition, we compared the values of SUVmax and
MV between DIBH and nonbreath-hold (NBH).

organ, by the DIBH technique. In 22 lesions (46.8%),
we corrected the tumor location within the organ.
Consequently, tumor staging also changed in 11 patients(23.4%) after correction by the DIBH technique. Regarding
the SUVmax value by DIBH, it showed an increase of
approximately 15.0–58.6% compared with that measured
by NBH. In contrast, the value of MV by DIBH showed adecrease of 20% compared with that measured by NBH.
Conclusion The DIBH 18F-FDG PET/CT technique isfeasible for accurate localization when diagnosingof liver tumors, bile duct cancers, and pancreas cancers.
The DIBH technique also improves the inaccuratequantification of both SUVmax and MV. Nucl Med Commun
c 2009 Wolters Kluwer Health | Lippincott
30:326–332 Williams & Wilkins.
Nuclear Medicine Communications 2009, 30:326–332

Methods Forty patients with various abdominal
malignancies including liver tumors, bile duct cancers, andpancreas tumors were enrolled. In total, the patients had
47 abdominal lesions. All patients showed a misregisteredimage in the early whole-body image taken 50 min after
intravenous 18F-FDG infusions. We added the delayed
images 40 min after the first image. On the delayed image,
we carried out both conventional techniques with normal
respiration (NBH) and the DIBH technique. Finally, we
compared two kinds of images in each patient. At the sametime, we compared both SUVmax and MV of cancer obtainedby the two kinds of imaging methods.

Keywords: 18F-fluorodeoxyglucose PET/computed tomography,
bile duct cancer, deep-inspiration breath-hold, liver tumor, pancreas tumoraDepartment of Radiology, School of Medicine, Miyazaki University, Kihara,
Kiyotake, Miyazaki-gun, Miyazaki Prefecture and bFaculty of Health Science,
School of Medicine, Kanazawa University, Ishikawa Prefecture, Japan

Correspondence to Associate Professor Shigeki Nagamachi, MD, Departmentof Radiology, School of Medicine, Miyazaki University, 5200 Kihara, Kiyotake,Miyazaki-gun, Miyazaki Prefecture 889-1692, Japan
Tel: + 11 81 985 85 1510 x2244; fax: + 11 81 985 85 7172;
e-mail: snagama@med.miyazaki-u.ac.jp
Received 27 September 2008 Revised 10 November 2008
Accepted 6 December 2008

Results In 14 lesions (29.8%), we corrected theanatomical tumor location, from the incorrect to the correct

Introduction
The development of combined PET/computed tomography (CT) imaging yields an increased sensitivity andspecificity beyond that which either of the two modalities
possesses separately and, therefore, provides improved
diagnostic accuracy for various cancers [1–4]. As attenuation correction in PET is performed with the use of
CT data, accurate spatial registration of PET and CT
images sets is required. Therefore, in the interpretation
c 2009 Wolters Kluwer Health | Lippincott Williams & Wilkins
0143-3636 

of PET/CT imaging, the misalignment of structures andlesions owing to respiratory motion is a significant
problem [5–7]. It causes not only the misdiagnosis oftumor location but also errors of quantification [6–8]. To
overcome this drawback, respiratory gating of PET and
CT is available using specific equipment for gating dataacquisition [9–12]. However, such equipment requires
a long acquisition time for processing the examinationand tends to contain a higher degree of noise [9–11].
DOI: 10.1097/MNM.0b013e3283298f78

DIBH 18F-FDG PET/CT is feasible technique Nagamachi et al. 327

Recently, the deep-inspiration breath-hold (DIBH)
technique has been reported to be likely to overcome
these problems. Particularly, it has been validated as a
useful technique in the diagnosis of thoracic lesions, suchas lung cancer [13–15].
Regarding abdominal lesions, such as liver tumors, theclinical effectiveness of this technique has not beenreported despite the possible usefulness of image registration in PET/CT [7]. As the liver has a complicatedarchitecture, such as portal veins or a bile duct system,
the correct diagnosis of lesion location is important for
determining therapeutic indications.
The effectiveness of DIBH is related to identifying
anatomical localizations as well as providing correct
quantification. According to a previous report, the maximal
standardized uptake values (SUVmax) by DIBH PET
were significantly higher than those by conventional
nonbreath-hold (NBH) PET [13,14]. Therefore, by using
the DIBH PET/CT technique, we can accurately
evaluate lesions close to the diaphragm in quantitative
analysis. To the best our knowledge, the indication of
the DIBH technique in the abdominal region has notbeen confirmed either. Furthermore, a comparative study
between NBH and DIBH in the quantification of SUVmax
or metabolic volume (MV) has not been conductedpreviously. The purpose of this study was to investigate
the usefulness of the DIBH 18F-fluorodeoxyglucose
PET/CT (DIBH 18F-FDG PET/CT) technique in diagnosing liver, pancreas or bile duct malignant tumors, andin quantitative analysis.

Materials and methods
Patients

Forty patients (27 male, 13 female; average age, 59.2
years; age range, 35–69) with a biopsy-proven diagnosisof cancer confirmed by staff pathologists at the Schoolof Medicine, Miyazaki University, were included. All
patients were selected according to the findings of awhole-body image, which showed several misregistrations
under NBH conditions. All analyzed lesions comprised
28 liver tumors, 10 bile duct cancers including gall
bladder cancer and lymph node metastasis, and ninepancreas cancers. All lesions were solid tumors diagnosed
by radiography, CT, and ultrasound. All patients were freefrom diabetes or chronic obstructive pulmonary disease.
They had normal respiratory function. With regard to
the tumor maximal diameter, there were no significant
differences among abdominal lesions (Table 1).
Data acquisition and image reconstruction

All PET/CT studies were carried out using an LSO-based
whole-body PET/CT scanner (Biograph 16; Siemens
Medical Solutions, Knoxville, USA) . The CT componentof PET/CT corresponds to a 16-slice multidetector-row
spiral CT scanner (Sensation 16; Siemens A.G., Forcheim,

Table 1

Patients’ clinical characteristics

Age (years)
Sex (male/female)
Respiratory function
%FEV1
%VC
Maximal diameter (mm)a
COPD
Diabetes mellitus

Liver

Bile duct

Pancreas(n = 22)(n = 9)(n = 9)68.4 ± 13.5
16/6

61.3 ± 10.2
5/4

61.3 ± 10.2
6/3

89.3 ± 7.5
92.6 ± 9.2
25.9 ± 6.9
None
None

88.2 ± 8.9
90.1 ± 8.2
15.7 ± 7.5
None
None

78.2 ± 8.9
89.6 ± 9.2
11.7 ± 8.5
None
None

%FEV1, forced expiratory volume in 1 second; %VC, vital capacity; COPD,
chronic obstructive pulmonary disease.
aThe maximal diameter was calculated as the mean value of lesions.

Germany) with a transverse field of view (FOV) of
500 mm and a spatial resolution greater than 1 mm.
The PET component of PET/CT allows only threedimensional acquisition with a FOV of 700 mm in thetransaxial direction and 170 mm in the axial direction.
The intrinsic resolution is 4.2-mm full-width-at-halfmaximum.
CT images were used for anatomical landmarks. CTbased attenuation correction used 700-mm extended
FOV technology. The same clinical reconstruction parameters were used for both NBH PET and DIBH PET
images. All PET images were reconstructed using iterativealgorithms (Fourier rebinning plus attenuation-weighted
ordered-subset expectation maximization, 4 iterations,
8 subset, 5-mm Gaussian filter) with CT-based attenuation correction. The data were reconstructed with a128128 matrix and 3-mm slice thickness. All PET and
CT images were transferred to a dedicated workstation(E.CAM; Siemens Medical Solutions, Irinoi, USA), fromwhich fused PET/CT images were constructed.
We used the following protocol. All patients fasted forat least 5 h before injection of 185 MBq of 18F-FDG.
During the uptake phase of approximately 50 min, thepatients remained in a quiet position. The first wholebody image was done in a supine position. The imaging
time was 15–18 min for each patient. In addition to theconventional PET/CT examination, all selected patients
underwent a DIBH PET/CT scan.
We added a conventional NBH imaging of a spot view
after the end of the first whole-body imaging. Just after
NBH imaging, we added DIBH spot imaging four times.
Each DIBH image datum was acquired under a condition with 30-s breath holding. We completed the final
DIBH image by adding each four-DIBH image after the
decay correction. All patients provided written informed
consent. This study protocol was approved by the
Review Board of the Miyazaki University School of
Medicine, Japan.

328 Nuclear Medicine Communications 2009, Vol 30 No 5

Image analysis

Image interpretations were performed on a dedicatedworkstation (ESOFT4.5, Siemens Medical System) thatcan display three orthogonal planes for CT, PET, andPET/CT fused images (sagittal, coronal, and transaxial)
and maximum-intensity projection images. Both NBH
PET/CT and DIBH PET/CT images were visuallyassessed for accuracy of fusion and alignment in separate
instances by the same nuclear medicine radiologists,
who were unaware of the clinical information. The uptakeof 18F-FDG was considered positive if it was greaterthan that in the surrounding normal liver tissue. NBHPET/CT images were first interpreted alone and thenreevaluated with the addition of DIBH. We made a final
diagnosis with an agreement of opinion by three nuclear
medicine physicians. A volume of interest was automatically drawn on each lesion with 18F-FDG uptake on volume
images encompassing the entire lesion. The MV of tumor
was determined as the lesion with SUV that showed morethan 50% of the SUVmax value. The SUVmax, normalized
to the body weight, was recorded for each finding.
Both SUVmax and MV values were compared between
NBH and DIBH PET/CT. Continuous variables wereexpressed as the mean ± SD. Statistical analyses wereconducted by the unpaired Student’s t-test and thepaired t-test. A P value of less than 0.05 was considered
statistically significant.

Results
Under DIBH conditions, all misregistration uptakes
were corrected to the normal anatomical location. They
corrected the misregistration uptake from the incorrectorgan to the correct organ in 14 of 47 (29.8%) cases, suchas from the lung to the liver. Corrections within organs,such as from the upper to the lower area, were observedin 22 of 47 (46.8%) cases. Minor corrections wereobserved in 11 of 47 (23.4%) cases (Table 2). A minor
correction means a correction for various discrepancies
between the tumor configuration by CT and theaccumulation margin by FDG-PET. The DIBH PET/CT
not only allowed a more precise localization of lesion but

Table 2

Correction of anatomical location

Liver tumor a
Pancreas cancer
Bile duct cancer b

n

Major

Moderate

Mild

28
9
10

11
0
3

17
2
3

0
7
4

Criteria for the correction of tumor’s location:
Major: correction from incorrect organ to correct organ.
Mild: adjustment of tumor contour.
Moderate: correction within organ.
aLiver tumor included hepatocellular carcinoma, liver metastasis,and cholangiocarcinoma.
bBile duct cancer included extrahepatic bile duct cancer, gall bladder cancer,
and lymph node metastases of both.

also accurately corrected the misregistration under NBH
conditions in all cases (Figs 1–3).
In quantitative analysis, the mean value of SUVmax was
statistically higher in the DIBH PET/CT technique thanin the NBH study in all evaluated abdominal lesions(Table 3). With regard to MV, the mean value of eachregion was statistically lower in the DIBH PET/CT
technique than in the NBH study (Table 4).

Discussion
The DIBH technique is usually applied for thoracic
lesions because of its effectiveness [13–15]. It is effective
for diagnosing the exact location of a lesion and evaluating
the number of lesions by avoiding respiratory artifacts. In
addition, the method also has the advantage of providing
accurate quantitative indices [15].
We confirmed the diagnostic effectiveness of thistechnique in detecting the accurate anatomical portionof lesions that is located close to the diaphragm,
particularly, in the liver. Under the NBH condition,
localized uptake was sometimes noted in extrahepaticareas, such as the lower lung. Even when located within
the liver, these areas are sometimes overlooked by only
plain CT because their density is similar to that of
the surrounding tissues. Therefore, incorrectly coregisteredlocalized uptake areas are possibly diagnosed erroneously
as tumor location. As a result, tumor staging could
be overestimated, and inadequate treatment might beselected. Using the DIBH technique, they were corrected
to a true location. In this study, we detected misregisteredlesions of liver metastasis and intrahepatic bile duct cancer
by NBH. Using the DIBH technique, we could correct
the erroneous locations from incorrect to correct organ(39.3%) and from incorrect to correct region within theliver (60.7%). As a result, we could prevent conducting
any further examinations unnecessarily, such as thoracic
high-resolution CT or repeated respiratory function tests.
In addition, liver nodules are sometimes vaguely visualized
by NBH PET/CT because of various physiological uptakeof liver tissue. The DIBH technique overcomes thelimitations by improving tissue contrast and is helpful
for demarcating liver tumors.
Regarding pancreatic tumors, we could obtain relative
proper information even when we used the NBH method.
No patients showed interorgan misregistration. As thepancreas is located at a relatively greater distance fromthe diaphragm than the upper liver, the influence of
respiratory motion could be small. However, for accurate
staging diagnosis, the evaluation of cancer invasion toa surrounding tissue with DIBH technique would be
preferable.

DIBH 18F-FDG PET/CT is feasible technique Nagamachi et al. 329

Fig. 1

Fifty-four-year-old female with liver metastasis from breast cancer. In the nonbreath-hold (NBH) image (left upper and lower), focal
fluorodeoxyglucose uptake appears to show lung metastasis. Using the deep-inspiration breath-hold (DIBH) technique, the liver metastasis wascorrectly identified (right upper and lower). The maximal standardized uptake value (SUVmax) is 16.54 and the metabolic volume (MV) is 28.45 in
NBH, whereas the SUVmax is 19.53 and the MV is 28.25 in DIBH.

On the basis of very accurate local coregistration, whichmakes it possible to do correct attenuation correction
and obtain corrected SUV values, increases in the SUVmax
were observed in most cases [13,15]. The excess rates,
which were 20–60%, were comparable with those ofprevious data with regard to thoracic tumors [10,13,15–17].
Such a phenomenon, including an increased SUVmax andan excess rate of approximately 50%, was prominently
noted in the liver lesions.

a reduction of about 30% in the total lesion volume wasshown [18]. As respiratory motion resulted in the spreadof the tumor contour to a larger size than the correct
outline, the value of MV seemed to be overestimated.
Although the clinical significance of MV has not been
determined yet, such an overestimation of the lesion
volume may occur. Similar reports have been publishedin respiratory diffusion-weighted imaging of the liver [19].
The technique is feasible in differentiating malignancy
from benign focal liver lesions.

In this mechanism, the lesion of highest SUV is dispersed
under the NBH condition with respiratory motion thatcauses underestimation of the true activity concentration[16–18]. In contrast, under the DIBH condition, thelesion with the highest SUV tends to be fixed, resulting
in an increase of the SUVmax. As the liver tissue shows
physiological uptake in particular, which results in poordelineation, the DIBH technique improves contrast andis helpful for demarcating tumors.

Taking into account those consequences of the
DIBH technique, the optimal threshold of SUVmax for
differentiating between benign and malignant tumors
should be reevaluated under controlled respiratory
motion. The criteria of the value of the SUV-related
index, such as the percentage of increase of a dual-phasestudy or MV, in differentiation or staging should also
be evaluated in the future.

The MV measured by the DIBH technique decreased toabout 70% of those measured by NBH in both the liver
and the pancreas. In a previous respiration-gated study,

One more implication is the contribution of thistechnique to the strategy for cancer treatment [13,20].
Recently, radiotherapy has become effective in hepatic

330

Nuclear Medicine Communications 2009, Vol 30 No 5

Fig. 2

Sixty-seven-year-old male with cholangiocarcinoma. Under a condition with conventional respiration imaging, the tumor is identified to be partly in thechest (left upper and lower). Under the deep-inspiration breath-hold (DIBH) condition, the tumor is correctly coregistered (right upper and lower).
The maximal standardized uptake value (SUVmax) is 8.5 and the metabolic volume (MV) is 26.8 in nonbreath-hold, whereas the SUVmax is 17.2 and the
MV is 16.2 in DIBH.

Fig. 3

Table 3Comparison of SUVmax

Liver tumor
Pancreas cancer
Bile duct cancer

n

NBH

DIBH

P value28
910

11.6 ± 3.0
10.1 ± 6.4
6.0 ± 1.3

18.4 ± 4.2
12.4 ± 5.5
6.9 ± 1.5

0.001
0.024
0.002

DIBH, deep-inspiration breath-hold; NBH, nonbreath-hold; SUVmax, maximal
standardized uptake value.

Table 4

Fifty-seven-year-old male with gall bladder (GB) cancer. Under acondition with conventional nonbreath-hold (NBH) imaging, the lesion
appears to be multiple hepatic tumors (left). After the correction by
deep-inspiration breath-hold (DIBH), cancer is identified in the GB walland metastatic lymph node is identified in the hepatoduodenal ligament(middle and right). The maximal standardized uptake value (SUVmax) of
the primary lesion is 7.6 and the metabolic volume (MV) is 4.5. In themetastatic lymph node, the SUVmax value is 6.8 and the MV is 3.2 in
NBH. In DIBH, the SUVmax of the primary lesion is 8.8 and the MV is
2.7. In the metastatic lymph node, the SUVmax is 8.1 and the MV is 2.2.

or bile duct tumors [20,21]. As tumor location is an
important factor for determining the therapeutic method,such as combined radiochemotherapy in the case of bile
duct cancer, correct diagnosis using the DIBH technique

Comparison of metabolic volume

Liver tumor
Pancreas cancer
Bile duct cancern

NBH (cm3) DIBH (cm3)

P value2891027.3 ± 12.6 22.7 ± 13.2
16.8 ± 11.1 14.0 ± 11.2
13.9 ± 12.7 11.6 ± 10.7

0.013
0.044
0.021

DIBH, deep-inspiration breath-hold; NBH, nonbreath-hold.

for anatomical assignment is critical [22]. Moreover, boththe extension pattern surrounding the bile duct system
and lymph node metastasis also affect the therapeuticstrategy [23]. When MV is used as a guide for theradiotherapy planning target volume, a greater dose to
the normal tissues may be irradiated under the NBH
condition. As liver tissue has limited tolerance toDIBH 18F-FDG PET/CT is feasible technique Nagamachi et al. 331

radiation, inadequate radiation filed should be avoided[24]. This conclusion also applies to pancreatic cancer.
Major complications, such as radiation-induced liver
damage [24] or gastroduodenal ulcers [25–27], must be
taken into account. Such undesirable consequences
could be avoided by the DIBH technique, and suitable
methods, such as intensity-modulated radiation therapy,
could be chosen [28].

5

In addition, as the therapeutic effect cannot always
be accurately determined because of the influence of
respiratory motion in NBH [29], it is sometimes difficult
to select an effective treatment strategy. The FDGPET/CT technique is now being used to monitor
therapeutic effects, such as radio-frequency ablation[30] or the administration of antiangiogenic therapy[31] in liver metastasis. Within the clinical course, these
therapies sometimes resulted in unsuccessful treatment
or local relapse [30]. Using the DIBH method, we cancorrectly monitor the therapeutic effects before and after
chemotherapy, radiotherapy, and radio-frequency ablation
by referring to the change of the corrected SUVmax
or MV. Recently, by the development of radiotherapy
treatment methods [32], it has become possible toeffectively modify the dose distribution on the basis of
the accumulation degree of FDG uptake.

9

The large drawback of the DIBH technique is that it
is not practical for a whole-body scan as a routine
examination. The DIBH technique is available within
only a one-bed range, which presents limitations inclinical use. If the sensitivity of the PET/CT system isimproved and the longitudinal FOVs are increased, it
will become a standard method. A future study should
include an optimal protocol and appropriate data collection
time in many institutions.

6
7

8

10

11

12

13

14

15

16

17

18

19

20

Conclusion
The DIBH 18F-FDG PET/CT is a feasible techniqueyielding the precise localization of abdominal malignant
lesions located close to the diaphragm and influenced
by respiratory motion. In particular, it is useful for
diagnosing liver tumor, bile duct cancers, and pancreas
cancers. It also provides accurate quantifications for
SUVmax and MV.

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