Background:
Assessing endocardial strain using a single ^<13>-ammonia positron emission tomography (PET) scan would be clinically useful, given the association between ischemia and myocardial deformati
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for assessment of left ventricular volumes, mass, and ejection fraction: comparison with
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Nagao M, Hatakenaka M, Matsuo Y, Kamitani T, Higuchi K, Shikata F, et al. Subendocardial
contractile impairment in chronic ischemic myocardium: Assessment by strain analysis of 3T tagged
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Kido T, Nagao M, Kido T, Kurata A, Miyagawa M, Ogimoto A, et al. Stress/rest circumferential
strain in non-ischemia, ischemia, and infarction: Quantification by 3 tesla tagged magnetic resonance
imaging. Circ J 2013;77:1235-41.
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ventricular functional recovery after acute myocardial infarction with systolic dysfunction. Int J
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11. Stathogiannis K, Mor-Avi V, Rashedi N, Lang RM, Patel AR. Regional myocardial strain by cardiac
magnetic resonance feature tracking for detection of scar in ischemic heart disease. Magn Reson
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Imaging 2020;68:190-6.
12. Berry C, Mangion K, Pathan F. Spotlight on strain following myocardial infarction. JACC
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Cardiovasc Imaging 2018;11:1445-7.
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infarction. Circ Cardiovasc Imaging 2019;12:e009404.
14. Mordi I, Bezerra H, Carrick D, Tzemos N. The combined incremental prognostic value of LVEF,
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late gadolinium enhancement, and global circumferential strain assessed by CMR. JACC Cardiovasc
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Imaging 2015;8:540-9.
15. Kawakubo M, Yamasaki Y, Kamitani T, Sagiyama K, Matsuura Y, Hino T, et al. Clinical usefulness
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angioplasty in chronic thromboembolic pulmonary hypertension: comparison with 2D
feature-tracking MRI. Eur Radiol 2019;29:4583-92.
16. Kawakubo M, Nagao M, Ishizaki U, Shiina Y, Inai K, Yamasaki Y, et al. Feature-tracking MRI
fractal analysis of right ventricular remodeling in adults with congenitally corrected transposition of
the great arteries. Radiol Cardiothorac Imaging 2019;1:e190026.
17. Dilsizian V, Bacharach SL, Beanlands RS, Bergmann SR, Delbeke D, Dorbala S, et al. ASNC
imaging guidelines/SNMMI procedure standard for positron emission tomography (PET) nuclear
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cardiology procedures. J Nucl Cardiol 2016;23:1187-26.
18. Cerqueira MD, Weissman, NJ, Dilsizian V, Jacobs AK, Kaul S, Laskey WK, et al. Standardized
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19. Germano G, Erel J, Kiat H, Kavanagh PB, Berman DS. Quantitative LVEF and qualitative regional
function from gated thallium-201 perfusion SPECT. J Nucl Med 1997;38:749-54.
20. Yamasaki Y, Abe K, Kamitani T, Hosokawa K, Kawakubo M, Sagiyama K, et al. Balloon
pulmonary angioplasty improves right atrial reservoir and conduit functions in chronic
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thromboembolic pulmonary hypertension. Eur Heart J Cardiovasc Imaging 2020;21:855-62.
21. Mangion K, Burke NMM, McComb C, Carrick D, Woodward R, Berry C. Feature-tracking
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myocardial strain in healthy adults- a magnetic resonance study at 3.0 tesla. Sci Rep 2019;9:3239.
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22. Sicari R, Cortigiani L. The clinical use of stress echocardiography in ischemic heart disease.
Cardiovasc Ultrasound 2017;15:7.
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23. Weiss AT, Berman DS, Lew AS, Nielsen J, Potkin B, Swan HJ, et al. Transient ischemic dilation of
the left ventricle on stress thallium-201 scintigraphy: A marker of severe and extensive coronary
artery disease. J Am Coll Cardiol 1987;9:752-9.
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24. Eitel I, Stiermaier T, Lange T, Rommel KP, Koschalka A, Kowallick JT, et al. Cardiac magnetic
resonance myocardial feature tracking for optimized prediction of cardiovascular events following
myocardial infarction. JACC Cardiovasc Imaging 2018;11:1433-44.
25. Cheng A, Langer F, Rodriguez F, Criscione JC, Daughters GT, Miller DC, et al. Transmural cardiac
strains in the lateral wall of the ovine left ventricle. Am J Physiol Hear Circ Physiol
2005;288:1546-56.
26. Kawakubo M, Arai H, Nagao M, Yamasaki Y, Sanui K, Nishimura H, et al. Global left ventricular
area strain using standard two-dimensional cine magnetic resonance imaging with inter-slice
interpolation. Cardiovasc Imaging Asia 2018;2:187-93.
27. Ishizaki U, Nagao M, Shiina Y, Inai K, Mori H, Takahashi T, et al. Global strain and dyssynchrony
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of the single ventricle predict adverse cardiac events after the Fontan procedure: Analysis using
feature-tracking cine magnetic resonance imaging. J Cardiol 2019;73:163-70.
28. Schmidt B, Dick A, Treutlein M, Schiller P, Bunck AC, Maintz D, et al. Intra- and inter-observer
reproducibility of global and regional magnetic resonance feature tracking derived strain parameters
of the left and right ventricle. Eur J Radiol 2017;89:97-105.
29. Alfakih K, Plein S, Thiele H, Jones T, Ridgway JP, Sivananthan MU. Normal human left and right
ventricular dimensions for MRI as assessed by turbo gradient echo and steady-state free precession
imaging sequences. J Magn Reson Imaging 2003;17:323-9.
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FIGURE LEGENDS
Fig. 1 Resting and adenosine stress protocols for 13N-ammonia PET
A low-dose fast helical (1.5-s) computed tomography scan was performed for attenuation correction.
Next, 13N-ammonia (185 MBq) was administered intravenously, and electrocardiography-gated
acquisition was performed (10 min at 16 frames/cardiac cycle using a parallel list mode). After the resting
PET scan, an adenosine stress test was performed (0.12 mg/kg/min for 6 min). Then, 13N-ammonia (555
MBq) was infused at 3 min after completion of the vasodilator infusion, and the stress PET scan was
performed using the same acquisition parameters.
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PET, positron emission tomography
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Fig. 2 Semi-automatic strain analysis with feature-tracking
ee
(a) The regional endocardial border is manually defined at the end of the diastole frame (left: short-axis,
middle: horizontal long-axis, right: vertical long-axis). (b) Endocardium points are automatically and
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evenly set based on the line length. (c) The points are automatically tracked during a cardiac cycle using a
local template-matching technique. (d) The endocardial regions are automatically segmented as lines with
ev
spline interpolation of points tracked during a cardiac cycle. Systolic strain is calculated from the strain
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curves as the minimum values of the normalized regional lengths.
Fig. 3 Global systolic strain values according to global MFR status
(a) Global circumferential strain values for patients with abnormal global myocardial flow reserves
(purple/dark purple, <2.0) and normal global myocardial flow reserves (red/dark red,
and in control
patients (cyan/dark cyan). (b) Global longitudinal strain values for patients with abnormal global
myocardial flow reserves (purple/dark purple, <2.0) and normal global myocardial flow reserves
(red/dark red,
and in control patients (cyan/dark cyan).
**p<0.01, *p<0.05. MFR, myocardial flow reserve
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Fig. 4 Correlations between global strains and LVEFs
Scatter plots show the correlations between global strain and LVEF. Plots in the upper row and lower row
indicate the values in the stressed and resting states, respectively. Plots in the left and right columns
indicate the correlations of LVEF with circumferential and longitudinal strains, respectively.
LVEF, left ventricular ejection fraction
Fig. 5 Regional systolic strain values according to regional MFR status
Strain values for patients with abnormal myocardial flow reserves (purple/dark purple, <2.0) and normal
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myocardial flow reserves (red/dark red,
, and in control patients (cyan/dark cyan): the upper low
indicates the circumferential strain values of the right coronary artery territory (a), left anterior
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descending artery territory (b), and left circumflex coronary artery territory (c), and the lower low
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indicates the longitudinal strain values of the right coronary artery territory (d), left anterior descending
artery territory (e), and left circumflex coronary artery territory (f).
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**p<0.01, *p<0.05. MFR, myocardial flow reserve
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Fig. 6 Circumferential strain polar maps at stress (left) and 13N-ammonia PET cine images (right)
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for a woman in her 60s with 90% stenosis at the proximal LAD, 50% stenosis at the proximal RCA,
and 50% stenosis at the diagonal branch
Before (upper row) and after (lower row) percutaneous coronary intervention. The cold color of the strain
map indicates a decrease in strain, while the warm color indicates an increase. After percutaneous
coronary intervention, there is a marked improvement in strain reduction over a wide area of the apex to
anteroseptal wall, and the cine images show improvement of blood flow in the anteroseptal wall and
reduction of the left ventricular cavity.
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Journal of Nuclear Cardiology
TABLE 1 Baseline patient characteristics and 13N-ammonia PET measurements
Patients
Characteristics
Global
Control
Global
All
P-value
MFR<2.0
Number
95
39
56
Age (years)
68±11
71±10
65±11
Male/female
62/33
22/17
40/16
6/4
69 (73%)
29 (74%)
40 (71%)
0 (0%)
68 (72%)
23 (60%)
45 (80%)
0 (0%)
Cardiovascular risk factors
Dyslipidemia
Diabetes mellitus
Family history
10
<0.05
41±15
44 (46%)
18 (46%)
26 (46%)
0 (0%)
42 (44%)
15 (38%)
27 (48%)
0 (0%)
22 (23%)
8 (21%)
14 (25%)
0 (0%)
Clinical history of coronary artery disease
14 (15%)
11 (28%)
3 (5%)
0 (0%)
Percutaneous coronary intervention
21 (22%)
11 (28%)
10 (18%)
0 (0%)
8 (8%)
3 (8%)
5 (9%)
0 (0%)
Summed stress score
5.7±7.1
8.6± .3
3.6±5.3
<0.01
1.5±3.3
Summed resting score
1.8±3.4
2.7±4.2
1.1±2.5
<0.01
0.5±1.2
Summed difference score
3.9±5.8
5.9±7.5
2.5±3.7
<0.01
1.0±2.2
Stressed myocardial blood flow (mL/g/min)
2.07±0.65
1.62±0.55
2.39±0.52
<0.01
2.43±1.00
Resting myocardial blood flow (mL/g/min)
0.98±0.25
1.05±0.29
0.92±0.22
0.03
1.06±0.28
Global MFR
2.2±0.7
1.5±0.4
2.6±0.5
<0.01
2.2±0.6
RCA MFR
2.3±0.8
1.5±0.5
2.7±0.6
<0.01
2.3±0.6
Coronary artery bypass grafting
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Hypertension
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Ammonia PET measurements
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LAD MFR
2.2±0.7
1.6±0.5
2.6±0.6
<0.01
2.3±0.6
LCx MFR
2.2±0.7
1.6±0.4
2.6±0.6
<0.01
2.2±0.6
Resting LVEDV (mL)
88±28
90±34
86±24
0.79
71±15
Resting LVESV (mL)
30±22
36±28
25±15
0.14
17±5
Resting LVEF (%)
70±12
66±15
72±10
<0.05
76±5
Stress LVEDV (mL)
101±28
103±33
100±26
0.84
76±15
Stress LVESV (mL)
34±22
43±28
31±17
0.06
17±5
Stress LVEF (%)
67±12
62±16
71±9
<0.01
78±4
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MFR, myocardial flow reserve; RCA, right coronary artery; LAD, left anterior descending artery; LCx,
left circumflex artery; LV, left ventricular; EDV, end-diastole volume; ESV, end-systole volume; EF,
ejection fraction.
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TABLE 2 Reproducibility of strain analyses
Intra-observer reproducibility
Inter-observer reproducibility
ICC (95%
Parameter
Bias (LOA)
ICC (95%
SDD
Bias (LOA)
SDD
CI)
CI)
Stress
–0.7 (–3.5,
CS
0.98 (0.92–
(–2.7,
1.4
0.98 (0.93–
1.3
2.0)
0.99)
2.5)
0.95 (0.82–
3.2 (–0.2,
1.00)
Global
0.4 (–1.6,
LS
Fo
1.0
2.3)
(–6.6,
CS
0.99)
6.7)
0.97 (0.96–
0.8 (–4.0,
2.5
5.6)
2.1
0.985(0.83–
4.9 (1.5,
0.99)
8.4)
0.97 (0.88–
0.5 (–4.1,
0.99)
0.3 (–1.6,
0.99 (0.97–
LS
1.0
2.2)
1.00)
(–6.9,
CS
0.91 (0.68–
0.99)
0.96 (0.83–
5.1)
0.99)
2.5 (–2.2,
0.94 (0.79–
2.4
7.2)
0.99)
–0.8 (–6.2,
3.3
5.9)
0.97 (0.90–
2.4
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3.4)
LAD
0.99)
1.8
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–0.7 (–4.8,
CS
5.0)
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LS
0.96 (0.84–
2.6
0.98)
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RCA
0.99)
(–5.3,
3.2
6.1)
0.97 (0.89–
1.7
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0.91 (0.68–
2.8
0.98)
4.6)
0.99 (0.97–
3.0 (–1.1,
0.98)
LCx
–0.0 (–1.9,
LS
0.98
1.9)
0.96 (0.85–
2.1
1.00)
7.2)
0.99)
Resting
–0.7 (–3.5,
Global CS
0.99 (0.95–
(–2.7,
1.4
2.0)
0.98 (0.93–
1.3
1.00)
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2.5)
1.00)
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0.1 (–1.8,
LS
0.99 (0.97–
2.5 (–1.9,
1.00)
6.9)
0.96 (0.85–
1.0 (–3.8,
1.0
0.1 (–5.2,
CS
0.95 (0.83–
2.3
2.0)
2.7
0.99)
0.96 (0.86–
2.4
5.5)
0.99)
5.7)
0.99 (0.97–
3.0 (–1.1,
0.99)
RCA
LS
0.0 (1.9, 1.9)
1.0
(–5.2,
CS
1.00)
7.2)
0.96 (0.87–
–0.2 (–3.9,
2.6
0.2 (–2.2,
3.6)
0.99)
0.99 (0.96–
1.9 (–3.0,
0.94 (0.79–
1.2
2.6)
3.4
5.1)
0.94 (0.78–
0.3 (–7.4,
0.99 (0.97–
1.0
0.92 (0.70–
8.0)
0.98)
3.0 (–1.1,
0.96 (0.85–
2.1
7.2)
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1.00)
0.99)
3.9
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–0.0 (–1.9,
1.9)
6.9)
0.98)
LCx
LS
2.5
1.00)
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–1.5 (–8.2,
CS
0.98 (0.92–
0.99)
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LS
0.99)
1.9
5.0)
LAD
0.96 (0.85–
2.1
Fo
0.99)
RCA, right coronary artery; LAD, left anterior descending artery; LCx, left circumflex artery; CS;
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circumferential strain, LS; longitudinal strain, LOA, limit of agreement; SDD, standard deviation of the
difference; ICC, intraclass correlation coefficient; CI, confidence interval.
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Resting and adenosine stress protocols for 13N-ammonia positron emission tomography A lowdose fast helical (1.5-s) computed tomography scan was performed for attenuation correction. Next, 13Nammonia (185 MBq) was administered intravenously, and electrocardiography-gated acquisition was
performed (10 min at 16 frames/cardiac cycle using a parallel list mode). After the resting PET scan, an
adenosine stress test was performed (0.12 mg/kg/min for 6 min). Then, 13N-ammonia (555 MBq) was
infused at 3 min after completion of the vasodilator infusion, and the stress PET scan was performed using
the same acquisition parameters.PET, positron emission tomography
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84x59mm (600 x 600 DPI)
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Semi-automatic strain analysis with feature-tracking
(a) The regional endocardial border is manually defined at the end of the diastole frame (left: short-axis,
middle: horizontal long-axis, right: vertical long-axis). (b) Endocardium points are automatically and evenly
set based on the line length. (c) The points are automatically tracked during a cardiac cycle using a local
template-matching technique. (d) The endocardial regions are automatically segmented as lines with spline
interpolation of points tracked during a cardiac cycle. Systolic strain is calculated from the strain curves as
the minimum values of the normalized regional lengths.
iew
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Global systolic strain values according to global MFR status
(a) Global circumferential strain values for patients with abnormal global myocardial flow reserves
(purple/dark purple, <2.0) and normal global myocardial flow reserves (red/dark red,
and in control
patients (cyan/dark cyan). (b) Global longitudinal strain values for patients with abnormal global myocardial
flow reserves (purple/dark purple, <2.0) and normal global myocardial flow reserves (red/dark red,
and in control patients (cyan/dark cyan).
**p<0.01, *p<0.05. MFR, myocardial flow reserve
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Correlations between global strains and LVEFsScatter plots show the correlations between global strain
and LVEF. Plots in the upper row and lower row indicate the values in the stressed and resting states,
respectively. Plots in the left and right columns indicate the correlations of LVEF with circumferential and
longitudinal strains, respectively.LVEF, left ventricular ejection fraction
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Regional systolic strain values according to regional MFR status
Strain values for patients with abnormal myocardial flow reserves (purple/dark purple, <2.0) and normal
myocardial flow reserves (red/dark red,
and in control patients (cyan/dark cyan): the upper low
indicates the circumferential strain values of the right coronary artery territory (a), left anterior descending
artery territory (b), and left circumflex coronary artery territory (c), and the lower low indicates the
longitudinal strain values of the right coronary artery territory (d), left anterior descending artery territory
(e), and left circumflex coronary artery territory (f).
**p<0.01, *p<0.05. MFR, myocardial flow reserve
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Circumferential strain polar maps at stress (left) and 13N-ammonia PET cine images (right) for a
woman in her 60s with 90% stenosis at the proximal LAD, 50% stenosis at the proximal RCA,
and 50% stenosis at the diagonal branch
Before (upper row) and after (lower row) percutaneous coronary intervention. The cold color of the strain
map indicates a decrease in strain, while the warm color indicates an increase. After percutaneous coronary
intervention, there is a marked improvement in strain reduction over a wide area of the apex to anteroseptal
wall, and the cine images show improvement of blood flow in the anteroseptal wall and reduction of the left
ventricular cavity.
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Journal of Nuclear Cardiology
84x61mm (600 x 600 DPI)
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Supplementary Movies
Supplementary Movie 1
Short-axis: Calculation of the short-axis regional circumferential strain at the middle ventricle and the
tracked points during a cardiac cycle. Cyan solid and dotted lines indicate segments 7 and 8 of the left
ventricle, yellow solid and dotted lines indicate segments 9 and 10, and magenta solid and dotted lines
indicate segments 11 and 12. This algorithm can be made available by contacting our research team
(contact: k-mstr@hs.med.kyushu-u.ac.jp).
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Supplementary Movie 2
Horizontal long-axis: Calculation of the horizontal long-axis regional strain at the middle ventricle and
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the tracked points during a cardiac cycle. The magenta solid line indicates the longitudinal strain curve for
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a cardiac cycle. This algorithm can be made available by contacting our research team (contact: kmstr@hs.med.kyushu-u.ac.jp).
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Supplementary Movie 3
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Vertical long-axis: Calculation of vertical long-axis regional strain at the middle ventricle and the
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tracked points during a cardiac cycle. The magenta solid line indicates the longitudinal strain curve for a
cardiac cycle. This algorithm can be made available by contacting our research team (contact: kmstr@hs.med.kyushu-u.ac.jp).
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