Ann Nucl Med
DOI 10.1007/s12149-010-0352-3

ORIGINAL ARTICLE

The reproducibility of deep-inspiration breath-hold 18F-FDG
PET/CT technique in diagnosing various cancers affectedby respiratory motion
Shigeki Nagamachi • Hideyuki Wakamatsu •Shogo Kiyohara • Seigo Fujita • Shigemi Futami •Hideo Arita • Shozo Tamura • Keiichi Kawai

Received: 7 October 2008 / Accepted: 9 December 2009
Ó The Japanese Society of Nuclear Medicine 2010

Abstract
Background The deep-inspiration breath-hold PET/CT(DIBH PET/CT) technique improves the limitations ofdiagnosing a lesion located in an area influenced byrespiratory motion that results in spatial misregistrations
caused by respiration between PET and CT. However, its
reproducibility with regard to calculating the maximal
standardized uptake value (SUVmax) and metabolic volume(MV) in DIBH PET/CT has not been elucidated.
Objective The purpose of this study was to investigate thereproducibility of the DIBH PET/CT technique including
calculating the SUVmax and the MV.
Methods Sixty patients with various cancers were enrolled. The subjects had 47 abdominal lesions and 28 chest
lesions. All patients demonstrated a misregistered image inthe early whole-body image taken 50 min after FDG intravenous infusions. We added the delayed spot images 40 min
after the first image. On the delayed image, we performed
both conventional techniques with non-breath-hold (NBH)
and the DIBH technique. In the four times DIBH technique,we obtained the coefficient of variance (CV) in calculatingthese indices for evaluating reproducibility.
Results The SUVmax value with DIBH showed anincrease of 16.1–60.1% compared with that measured by

S. Nagamachi (&)  H. Wakamatsu  S. Kiyohara  S. Fujita 
S. Futami  H. Arita  S. Tamura
Department of Radiology, School of Medicine,
Miyazaki University, 5200 Kihara, Kiyotake,Miyazaki 889-1692, Japane-mail: snagama@med.miyazaki-u.ac.jp
K. Kawai
Faculty of Health Science, School of Medicine,
Kanazawa University, Ishikawa, Japan

NBH. The mean value of CV was 5.5 in thoracic lesions
and 6.3 in abdominal lesions. The values of MV with
DIBH showed a decrease of 14.0–20.1% compared withthose measured by NBH. Regarding reproducibility, meanvalue of CV was 7.1 in thoracic lesions and 11.9 inabdominal lesions.
Conclusion The DIBH technique improves the inaccuratequantification of both SUVmax and MV. Although the CV
value of SUVmax with DIBH technique is better in thoracic
lesions compared with that in abdominal lesions, thereproducibility was acceptable.
Keywords 18F-FDG PET/CT 
Deep-inspiration breath-hold  Reproducibility

Introduction
The combined PET/CT imaging yields increased sensitivity and specificity than either of the two modalities and,
therefore, provides improved diagnostic accuracy for various cancers [1–4]. Because attenuation correction in PET
is performed with the use of CT data, accurate spatial
registration of PET and CT image sets is required. In theinterpretation of PET/CT imaging, therefore, the misalignment of structures and lesions owing to respiratory
motion is a significant problem [5–7]. It causes not only themisdiagnosis of tumor location, but also errors of quantification [6, 8, 9]. To overcome this drawback, respiratory
gating of PET and CT is available using specific equipment
for gating data acquisition [7, 10–13]. However, themethod requires a long acquisition time for processing theexamination because we have to divide collection data into
certain phases [9–11]. Recently, the deep-inspiration
breath-hold (DIBH) technique has been reported to be123Ann Nucl Med

likely to overcome these problems. Particularly, it has beenvalidated as a useful technique in the diagnosis of thoracic
lesions, such as lung cancer [14–17].
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 value (SUVmax) values with DIBH
PET were significantly higher than those obtained withconventional non-breath-hold (NBH) PET [14, 15]. Using
the deep-inspiration breath-hold PET/CT (DIBH PET/CT)
technique, therefore, we can accurately evaluate lesions
close to the diaphragm in quantitative analysis. However,
to maintain a good quality imaging of DIBH PET/CT, weneed to repeat the DIBH technique and add some images.
Therefore, if CT images and repeated DIBH PET images
do not match constantly and completely, attenuation correction and SUV calculation will be inaccurate. To the bestof our knowledge, the reproducibility in the quantificationof SUVmax or MV by DIBH has not been focused on
previously.
The purpose of the current study was to investigate thereproducibility of the deep-inspiration breath-hold 18FFDG PET/CT (DIBH PET/CT) techniques in quantitative
analysis.

Materials and methods
Phantom study
Before clinical research of DIBH, we performed a phantom
experiment to examine the coefficient of variance (CV) of
18
F-FDG PET indices in imaging of motionless objects. We
used a cylinder phantom (10-cm high, diameter of 20 cm,
etc. test phantom, Kyoto Kagaku, Japan) and set three
elliptical pillar phantoms (8.0-cm high, diameter 2.0 cm,
Kyoto Kagaku, Japan) filled with 18F-FDG aqueous solution of different radioactivity (64, 32, and 8 kBq/ml) concentrations in a cylinder phantom. 18F-FDG was provided
by Nihon MediPhysics Company (Kurume, Fukuoka prefecture, Japan). All data were acquired on a combined PET/
CT in-line system (Biograph 16, Siemens). The PET/CT
scan was performed using a single bed position. CT wasused for CT-based attenuation correction. PET emission
data were acquired using a static collection method for
2 min and for 30 s. In condition with 30 s collections, a
total of 4 images were obtained per concentration.
All PET images were reconstructed using iterativealgorithms (Fourier rebinning plus attenuation-weighted
ordered-subset expectation maximization, 2 iterations, 8
subsets, 5-mm Gaussian filter) with CT-based attenuation
correction. The data were reconstructed with a 256 9 256
matrix and 2-mm slice thickness.

123

Image analysis was performed on a dedicated workstation (ESOFT4.5, Siemens). On the 3-dimensional (coronal,
sagittal and axial) PET/CT images, volumes of interest(VOIs) were drawn automatically around each cube abovea pre-set threshold of 50% of the maximal value ofradioactivity (Bq/ml), and 3-dimensional isocontours at
50% of the maximal value of radioactivity (Bq/ml). We
also calculated the metabolic volume (MV) of each cube.
We defined the MV as the total areas with radioactivity(Bq/ml) exceeding 50% of the maximal value of radioactivity.
The means and standard deviations (SDs) of the maximal value of radioactivity or MV for the 4 images with 30 s
data collections were calculated for all with the threecylinder phantoms with the various 18F-FDG radioactivity
concentrations. In addition, we calculated the CV for these
indices of four individual DIBH studies. The coefficient ofvariance (CV) was defined as SD 9 100/mean.
Clinical study
The current study was conducted from October 2007 to
July 2008. Sixty patients (34 male, 26 female; average age,63.5 years; age range, 35–72 years) with a biopsy-provendiagnosis of cancer confirmed by staff pathologists at the
School of Medicine, Miyazaki University, were included.
All patients were selected according to the findings of awhole-body image, which showed misregistration under
NBH.
All analyzed lesions comprised 25 liver tumors including multiple metastasis, 11 bile duct cancers including GB
cancer and lymph node metastasis, 11 pancreas cancers, 22lung cancers, 3 esophageal cancers and 3 chest wall
tumors. All lesions were solid tumors diagnosed by X-ray
CT and ultrasound (US). All patients were free of diabetes
or respiratory dysfunction such as chronic obstructive
pulmonary disease (COPD). They had normal respiratory
function (percentage of vital capacity (%VC) [80.0%,
forced expiratory volume in 1 s (FEV 1.0%) [70.0%).
With regard to the tumor maximal diameter, there wereno significant differences between thoracic lesions andabdominal lesions (Table 1).
We used the following protocol. Patients fasted for atleast 5 h before injection of 185 MBq of 18F-FDG. The
total 18F-FDG dosage in each person was from 166.5 to
238.5 MBq and the mean dosage was 218.3 MBq(3.76 MBq/kg). During the uptake phase of approximately
50 min, the patients remained in a quiet position. The firstwhole-body image was obtained in a supine position. The
imaging time was 15–18 min for each patient. The acquisition time per bed position was 2 min. In addition to theconventional whole-body PET/CT examination, we added
NBH imaging of a spot view. The acquisition time was also

Ann Nucl Med
Table 1 Patient’s clinicalcharacteristics

Thoracic lesions (n = 28)

Abdominal lesions (n = 32)

Age65.9 ± 10.1

61.3 ± 10.2

Gender (M:F)

16:12

18:14

Respiratory function%FEV1 forced expiratory
volume in 1 s%VC %vital capacity
COPD chronic obstructive
pulmonary disease

a

%FEV1

86.3 ± 12.5

87.2 ± 8.9%VC91.7 ± 8.985.1 ± 8.2

COPD

None

None

Diabetes mellitus

None

None

Imaging protocol

FDG
injection

50min

NBH
WBI

NBH SI60min

DIBH SI

30sec 30sec 30sec 30sec
NBH
WBI
SI

: Non-breath hold
: Whole body imaging: Spot imagingb

30 seconds

We used the same clinical reconstruction parameters forboth the NBH PET and DIBH PET images. All PET
images were reconstructed using iterative algorithms(Fourier rebinning plus attenuation-weighted ordered-subset expectation maximization, 2 iterations, 8 subsets, 5-mm
Gaussian filter) with CT-based attenuation correction. The
data were reconstructed with a 256 9 256 matrix and
2-mm slice thickness. All PET and CT images weretransformed to a dedicated workstation (e-soft; Siemens),
from which fusion PET/CT images were constructed.
All patients provided written informed consent. The
review board of the Miyazaki University School of Medicine approved this study protocol.
Image analysis

Start DIBH

End DIBH

Fig. 1 a Protocols for FDG PET/CT imaging of NBH and DIBH. b
Breathing signal of patient during NBH condition and DIBH PET/CT.
Patient was instructed to hold breath in maximal inspiratory position
for 30 s during DIBH PET scan

2 min. Just after the NBH imaging, we performed DIBH
spot imaging four times in all of the selected patients(Fig. 1a).
Each DIBH image datum was acquired under a condition with 30 s breath holding. The time from the beginningto the end of DIBH condition was recorded by referring to
the real-time display of the respiratory monitoring equipment (AZ-733V; Anzai Medical Co. Ltd., Japan). A
respiratory sensor (an elasticized belt around the patient’s
abdomen) provides respiratory information by detectingchanges in the patient’s abdominal pressure. Before performing the actual DIBH PET/CT examination, the patients
repeated exercises of DIBH several times to maintain each
DIBH posture equally. During the actual PET scan,patients were asked to hold their breath in maximal inspiratory position motionlessly for 30 s, with the respiratory
monitoring device fixed. We confirmed that they wereequal to the BH condition by referring to records of therespiratory monitoring system (Fig. 1b).

Image analysis was performed on the same dedicatedworkstation (ESOFT4.5, Siemens) as used for the phantom
study, which can display three orthogonal planes for CT,
PET and PET/CT fused images and maximum-intensity
projection (MIP) images. NBH PET/CT and four kindsof DIBH PET/CT image were visually assessed for the
anatomical location of the lesion, and accuracy of fusion
and alignment in separate instances by the same nuclear
medicine physicians.
On the 3-dimensional (coronal, sagittal and axial) PET/CT images, a VOI of a lesion above a pre-set threshold of
50% of SUVmax was automatically drawn using 3-dimensional isocontours at 50% of the maximum SUV. The
maximum value in the VOI was defined as SUVmax.
SUVmax was obtained for all lesions revealed on NBH
PET/CT images and DIBH PET/CT images.
Both the values of SUVmax and MV were compared
between NBH images and the mean of four DIBH images.
Continuous variables were expressed as mean ± SD. Statistical analyses were conducted by the unpaired Student’s ttest and paired t test. A p value of \0.05 was considered to
be statistically significant. In addition, we evaluated the
reproducibility of calculating these two indices in four
DIBH images. Namely, we calculated the CV for both
SUVmax and MV of four individual DIBH studies. The CV
was defined as SD 9 100/mean. Then we compared the123Ann Nucl Med

mean value of CV in imaging of thoracic lesions with thatof abdominal lesions.

Results
The results of the phantom study are shown in Table 2 andFig. 2. When we calculated the quantitative indices(maximal value of radioactivity and MV) in each of thefour 30-s studies, the reproducibility was acceptable in thethree kinds of concentrations (Fig. 2). The value of CV in
low-dose concentration (8 kBq/ml) was 5.7 and those in
the middle-dose (32 kBq/ml) or high-dose concentrations(64 kBq/ml) were 1.2 and 1.1. Regard as CV for calculating MV, the value of CV in low-dose concentration was
12.2 and those in the middle-dose or high-dose concentrations were 3.1 and 2.3, respectively (Table 2).
In the clinical studies, all patients who participated inthis current study were able to accomplish this protocol.
With regard to the clinical parameters, there were noapparent differences between abdominal lesions and thoracic lesions (Table 1). In both NBH and DIBH images, all
Table 2 Comparison of quantitative indices (phantom study)
Parameter

Low dose

Middle doselesions were clearly visualized. Under DIBH conditions, allmisregistration uptakes were corrected to the normal anatomical location (Figs. 3, 4, 5, 6). The DIBH PET/CT not
only allowed a more precise localization of lesions, butalso accurately corrected the misregistration under NBH
conditions in all cases.
In the quantitative analysis, the mean value of SUVmax
was statistically higher in the DIBH PET/CT techniquethan in the NBH study in all evaluated lesions. With regard
to the MV, the mean value of each MV was statisticallylower in the DIBH PET/CT technique than in the NBH
study (Table 3).
The mean value of CV in SUVmax was 5.5 in thoracic
lesions and 6.3 in abdominal lesions. These values werehigher in comparison with those obtained from the phantom experiment with middle- or high-dose concentrations.
In the comparison of CV in SUVmax, the mean value of CV
in thoracic lesions was better than that in abdominal
lesions. However, there was no statistical significance.
With regard to CV in MV, it was 7.1 in thoracic lesions and11.9 in abdominal lesions. This difference was not statistically significant either.

Discussion

High dose

SUVmax (Bq/ml)—30 s collection
1st

3.7 (2934.1)

14.6 (12040.2)

28.2 (23278.4)

2nd

3.8 (3055.2)

14.8 (12013.2)

28.1 (23728.6)

3rd

3.3 (2710.7)

14.5 (11734.4)

27.6 (23268.8)

4th

3.4 (2744.5)

14.8 (11989.2)

27.7 (23177.3)

Mean

3.5 (2861.1)

14.7 (11944.3)

27.9 (23363.3)

SD

0.2 (162.5)

0.17 (141.4)

0.31 (247.8)

CV

5.7

1.2

1.1

Because of its effectiveness, the DIBH technique is usuallyapplied to thoracic lesions [14–17]. It is effective in

SUVmax (Bq/ml)—2 min collection
3.5 (2801.1)

14.3 (11624.3)

27.4 (23151.9)

MV—30 s collection
1st

4.4

29.8

62.3

2nd

3.5

27.8

59.1

3rd

4.4

28.2

60.0

4th

4.7

28.8

60.2

Mean
SD

4.2
0.5

28.6
0.9

60.4
1.4

CV

12.2

3.1

2.3

29.3

60.7

MV—2 min collection
4.5

SUVmax (Bq/ml) maximal standardized uptake value (maximal valueof radioactivity count)
MV metabolic volume (ml)Low dose 8.0 kBq/ml
Middle dose 32.0 kBq/ml
High dose 64.0 kBq/ml

123

Fig. 2 Results of phantom study. In 2-min collections (left upper),the values of SUVmax were 3.5, 14.3 and 27.4 (low dose, middle dose,high dose), and MV (ml) were 4.5, 29.3 and 60.7, respectively. In the
30-s collections (middle and right), each value of SUVmax of low dosewas 3.7, 3.8, 3.3 and 3.4, respectively. Similarly, each SUVmax of
middle dose was 14.6, 14.8, 14.5 and 14.8. Each SUVmax of high dosewas 28.2, 28.1, 27.6 and 27.7. The CV of each concentration was 5.7,
1.2 and 1.1, respectively. Regarding MV (ml) in the 30-s collections,each value of low dose was 4.4, 3.5, 4.4 and 4.7, respectively. The
MV (ml) of middle dose was 29.8, 27.8, 28.2 and 28.8. The MV (ml)of high dose was 62.3, 59.1, 60.0 and 60.2. The CV of eachconcentration was 12.2, 3.1 and 2.3, respectively

Ann Nucl Med
Fig. 3 A 45-year-old woman
with right breast cancer. In the
NBH image, focal FDG uptake
is shown within the rib (leftupper). The value of SUVmax is
9.0 and MV (ml) was 4.5 in the
NBH image. Using the DIBH
technique, FDG uptake wasnoted to be consistent withbreast cancer. Each value of
SUVmax was 9.9, 9.3, 9.3 and
9.6, respectively. The value of
CV was 3.3. Regarding MV(ml), the values were 4.4, 3.9,
4.4 and 4.2, respectively, andthe value of CV was 6.2(middle and right)

Fig. 4 A 54-year-old woman
with liver metastasis from breast
cancer. In the NBH image(left upper), focal FDG uptake
appears to be lung metastasis.
The value of SUVmax was 16.5
and MV (ml) was 19.5 in NBH.
Using the DIBH technique, liver
metastasis was correctly
recognized. Each value of
SUVmax in DIBH was 28.5,
29.6, 28.6 and 28.3,
respectively. The value of CV
was 2.2. Regarding MV (ml) in
DIBH technique, the values
were 14.4, 14.9, 14.1 and 15.8,
respectively, and the value of
CV was 5.2 (middle and right)

diagnosing the exact location of the lesion and evaluationof the number of lesions by avoiding respiratory artifacts.
In addition, the method also has the advantage of providing
accurate quantitative indices [16, 17].
On the basis of very accurate local coregistration, whichmakes it possible to perform accurate attenuation correction and also to reduce blurring, increases in SUVmax wereobserved in most cases [14, 16–18]. The SUVmax values of
DIBH state increased 1.2–1.6 times in comparison withthose of the NBH state. This result was comparable to thoseof previous data with regard to thoracic tumors [10, 16–20]. In this mechanism, the voxel including SUVmax isdispersed under the NBH condition with respiratory motion

during the entire respiratory cycle, which causes underestimation of the true activity concentration [18–21]. In
contrast, under the DIBH condition, the voxel including theSUVmax tends to be fixed, resulting in an increase of
SUVmax. The reason why the effectiveness was prominently noted in thoracic lesions was probably due to the
distances moved by respiratory motions. Because thoracic
lesions were likely to be more influenced under respiratory
motion, SUVmax of thoracic lesion demonstrated more
remarkable changes than that of abdominal lesions.
The value of MV in the DIBH technique decreased toabout 80% of that in NBH in both thoracic and abdominal
lesions. In a previous respiration-gated study, a reduction

123Ann Nucl Med
Fig. 5 A 67-year-old man withcholangiocarcinoma. With NBH
image, the tumor was identified
partly in the chest. The value of
SUVmax was 8.5 and MV (ml)was 26.8 (upper left). Under
DIBH condition, the tumor wascorrectly coregistered. Eachvalue of SUVmax was 14.6, 17.2,
16.5 and 16.2, respectively. The
value of CV was 6.7. The valuesof MV (ml) in each DIBH
image were 20.3, 20.6, 26.0 and
30.5, respectively, and the valueof CV was 19.6 (middle andright)

Fig. 6 A 64-year-old man withprimary lung adenocarcinoma.
With NBH, FDG uptake waspartly dissociated with tumor
contour. The value of SUVmax
was 3.2 and MV (ml) was
4.6 (left upper). Under DIBH
condition, the tumor wascorrectly coregistered. Eachvalue of SUVmax was 6.4, 6.8,
7.0 and 6.5, respectively. The
values of MV (ml) in each
DIBH image was 3.2, 3.6, 3.5
and 3.8, and the value of CV
was 6.2 (middle and right)of about 30% in the total lesion volume was shown [21]. As
respiratory motion resulted in the spread of the tumor
contour to a larger size than the correct outline, the value of
MV seemed to be overestimated. Although the clinicalsignificance of the MV had not been determined yet, theindex was also likely to reflect the exact viable tumor tissue
amount [22]. The values of MV positively correlated wellwith those of SUVmax in our previous study and the coefficient correlations were around 0.6–0.7 [22]. The value of
MV would also preferably be calculated by the DIBH
technique.
With regard to the reproducibility of DIBH, the meanvalue of CV in calculating SUVmax was fairly good, ataround 5–6. In calculating MV, the CV value was 7.1 inthoracic lesions and 11.9 in abdominal lesions. These were
better than those of phantom studies with low-dose condition. Although the value of CV was higher than thatobtained in the phantoms with middle-dose or high-dose
conditions, they would be acceptable values clinically if we

123

recognize the ranges of values. Interestingly, the meanvalues of CV of both indices were better in thoracic lesions
compared with those in abdominal lesions. A possible
explanation regarding the relatively higher CV of theabdominal lesions may be that larger attenuation correction
factors including surrounding physiological uptake areapplied in this section compared to the thorax (lower
attenuation due to the lungs). Such a difference in anatomical and physiological conditions was considered to be
the main influencing factor.
The other possible influential factor is the length of
acquisition time with breath holding. We set 30 s for each
datum in each study to gather adequate counts for maintaining image qualities and reproducibility. Although thevalue of CV in 30-s collection is known to be better thanthat in 15-s collection in phantom study [16], 30-s breath
holding might be difficult in some cases. In some previous
studies on DIBH protocols, various and flexible breathholding times using list mode collections were set [16].

Ann Nucl Med
Table 3 Comparison of quantitative indices (clinical studies)
Thoracic lesions(n = 28)

Abdominal lesions(n = 47)

SUVmaxNBH

9.1 ± 7.5

9.5 ± 4.4

DIBH

12.0 ± 8.9*

13.5 ± 7.3*CV

5.5 ± 2.9

6.3 ± 4.8

NBH

25.7 ± 19.4

24.3 ± 17.9

DIBH
CV

21.6 ± 18.3*
7.1 ± 6.7

20.4 ± 15.9**
11.9 ± 8.6

Maximal diameter (mm)28.8 ± 14.8

36.3 ± 15.5

MV (cm3)

NBH Non-breath hold
DIBH Deep-inspiration breath hold
The maximal diameter was calculated as the mean value of lesions* P \ 0.01; the value of DIBH was significantly higher than that of
NBH

condition. This kind of unnecessary overdose could be
avoided by the DIBH technique.
Although the DIBH technique has a drawback in clinicaluse, that is, limited availability within only a one-bed range
at present, it will become a standard method if the sensitivity of the PET/CT system is improved further and thelongitudinal fields of view are increased. Future studies
should be done under an optimal protocol and appropriate
data collection time in multiple institutions.

Conclusion
The DIBH 18F-FDG PET/CT corrects the inaccuratequantification of both SUVmax and MV. The reproducibility of calculation in SUVmax or MV with DIBH technique
is favorable. However, at present it is better applicable tothoracic than abdominal lesions.

** P \ 0.05; the value of DIBH was significantly lower than that of
NBH

References
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DIBH studies might account for the higher CV values.
Another probable influential factor is the tumor component. Because we selected only tumors with a solid
component, lesion homogeneity was assured equally ineach study. In cases with inhomogeneous tumors, such as
cavity forming ones or ones containing a cystic component,
the reproducibility would be worse.
Taking into account the result that the values of SUVmax
of a lesion with DIBH technique were higher than thosewith NBH PET/CT, the optimal threshold of SUVmax for
differentiating between benign and malignant tumors
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The other implication is the contribution of this technique to the strategy for cancer treatment [14, 23].
Recently, radiotherapy has become more effective in various tumors [23, 24]. As accurate tumor location is an
important factor for determining the therapeutic method,correct diagnosis using the DIBH technique for anatomical
assignment is important [25]. When MV is used as a guidefor the radiotherapy planning target volume, a greater doseto the normal tissues may be irradiated under the NBH

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