Skip to main content

Hemispherical photoacoustic imaging of myocardial infarction: in vivo detection and monitoring

European Radiology volume 28, pages 2176–2183 (2018)Cite this article

Abstract

Objectives

This study aimed to demonstrate the capacity for noninvasive localisation and characterisation of myocardial infarction (MI) in vivo using a hemispherical photoacoustic imaging (PAI) system. MI remains a leading cause of morbidity and mortality worldwide. To enable optimal treatment of patients, timely and accurate diagnosis and longitudinal monitoring is critical.

Methods

Ischaemia was induced in Balb/c mice by ligation of the left anterior descending artery. The hemispherical PAI system, equipped with 128 ultrasonic transducers spirally distributed on the surface, along with parallel data acquisition, was applied for imaging of the mouse heart.

Results

Our study showed that hemispherical PAI can delineate thoracic vessels and the morphology of the entire heart. Longitudinal PAI images revealed gradual expansion of the infarcted area along with necrosis and fibrosis, which were quantitatively validated by triphenyltetrazolium chloride staining. After MI modelling, the photoacoustic (PA) signal intensity decreased by 399.1 ± 56.3 (p < 0.001), a ~2.5-fold reduction compared to that of healthy cardiac tissue. The calculated size of the enlarged heart, 10.4 ± 6.0 mm2 (p < 0.001), represents an increase of ~18% versus that of a healthy heart.

Conclusions

PAI enables MI diagnosis and injury localisation with its capabilities for both deep organ imaging and lesion region differentiation.

Key Points

• Photoacoustic imaging (PAI), combining optical absorption and ultrasonic resolution, can delineate cardiac anatomy.

• PAI can diagnose myocardial infarction lesions with 10 mm imaging depth in vivo.

• Quantified results are in excellent agreement with enzyme and histological examinations.

• PAI can serve as a complementary modality to SPECT and ultrasound imaging.

• This study will encourage further PAI development for clinical use.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

MI:

Myocardial infarction

SPECT:

Single-photon emission computed tomography

US:

Ultrasound

PA:

Photoacoustic

PAI:

Photoacoustic imaging

ROI:

Region of interest

sO2 :

Oxygen saturation

cTnT:

Cardiac troponin T

TTC:

Triphenyltetrazolium chloride

LVIDd:

Left ventricular internal diameter diastole

LVIDs:

Left ventricular internal diameter systole

LVEF:

Left ventricular ejection fraction

LVFS:

Left ventricular fraction shortening

References

  1. Nguyen HL, Yarzebski J, Lessard D, Gore JM, McManus DD, Goldberg RJ (2017) Ten-Year (2001-2011) Trends in the Incidence Rates and Short-Term Outcomes of Early Versus Late Onset Cardiogenic Shock After Hospitalization for Acute Myocardial Infarction. J Am Heart Assoc 6:e005566

    Article  PubMed  PubMed Central  Google Scholar 

  2. Acharya D, Loyaga-Rendon RY, Pamboukian SV et al (2016) Ventricular Assist Device in Acute Myocardial Infarction. J Am Coll Cardiol 67:1871–1880

    Article  PubMed  Google Scholar 

  3. Wong ND (2014) Epidemiological studies of CHD and the evolution of preventive cardiology. Nat Rev Cardiol 11:276–289

    Article  PubMed  Google Scholar 

  4. Tanabe Y, Kido T, Uetani T et al (2016) Differentiation of myocardial ischemia and infarction assessed by dynamic computed tomography perfusion imaging and comparison with cardiac magnetic resonance and single-photon emission computed tomography. Eur Radiol 26:3790–3801

    Article  PubMed  Google Scholar 

  5. Cho SG, Jabin Z, Park KS et al (2017) Clinical values of left ventricular mechanical dyssynchrony assessment by gated myocardial perfusion SPECT in patients with acute myocardial infarction and multivessel disease. Eur J Nucl Med Mol Imaging 44:259–266

    Article  PubMed  Google Scholar 

  6. Osmanski BF, Pezet S, Ricobaraza A, Lenkei Z, Tanter M (2014) Functional ultrasound imaging of intrinsic connectivity in the living rat brain with high spatiotemporal resolution. Nat Commun 5:5023

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Greco A, Mancini M, Gargiulo S et al (2012) Ultrasound biomicroscopy in small animal research: applications in molecular and preclinical imaging. J Biomed Biotechnol 2012:519238

  8. Brenner DJ, Hall EJ (2007) Current concepts - Computed tomography - An increasing source of radiation exposure. New Engl J Med 357:2277–2284

    CAS  Article  PubMed  Google Scholar 

  9. Yao J, Kaberniuk AA, Li L et al (2016) Multiscale photoacoustic tomography using reversibly switchable bacterial phytochrome as a near-infrared photochromic probe. Nat Methods 13:67–73

    CAS  Article  PubMed  Google Scholar 

  10. Li L, Zhu L, Ma C et al (2017) Single-impulse panoramic photoacoustic computed tomography of small-animal whole-body dynamics at high spatiotemporal resolution. Nat Biomed Eng 1:0071

    Article  PubMed  PubMed Central  Google Scholar 

  11. Kruger RA, Lam RB, Reinecke DR, Del Rio SP, Doyle RP (2010) Photoacoustic angiography of the breast. Med Phys 37:6096–6100

    Article  PubMed  PubMed Central  Google Scholar 

  12. Wang LHV, Hu S (2012) Photoacoustic Tomography: In Vivo Imaging from Organelles to Organs. Science 335:1458–1462

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Xia J, Chatni MR, Maslov K et al (2012) Whole-body ring-shaped confocal photoacoustic computed tomography of small animals in vivo. J Biomed Opt 17:050506

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li W, Sun X, Wang Y et al (2014) In vivo quantitative photoacoustic microscopy of gold nanostar kinetics in mouse organs. Biomed Opt Express 5:2679–2685

    Article  PubMed  PubMed Central  Google Scholar 

  15. Heijblom M, Piras D, van den Engh FM et al (2016) The state of the art in breast imaging using the Twente Photoacoustic Mammoscope: results from 31 measurements on malignancies. Eur Radiol 26:3874–3887

    Article  PubMed  PubMed Central  Google Scholar 

  16. Liu Y, Nie L, Chen X (2016) Photoacoustic Molecular Imaging: From Multiscale Biomedical Applications Towards Early-Stage Theranostics. Trends Biotechnol 34:420–433

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Jathoul AP, Laufer J, Ogunlade O et al (2015) Deep in vivo photoacoustic imaging of mammalian tissues using a tyrosinase-based genetic reporter. Nat Photonics 9:239–246

    CAS  Article  Google Scholar 

  18. Lee S, Kim JH, Lee JH, Lee JH, Han JK (2017) Non-invasive monitoring of the therapeutic response in sorafenib-treated hepatocellular carcinoma based on photoacoustic imaging. Eur Radiol Suppl 3:1–10

    Google Scholar 

  19. Nie L, Chen X (2014) Structural and functional photoacoustic molecular tomography aided by emerging contrast agents. Chem Soc Rev 43:7132–7170

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Liu Y, Yang Y, Sun M et al (2017) Highly specific noninvasive photoacoustic and positron emission tomography of brain plaque with functionalized croconium dye labeled by a radiotracer. Chem Sci 8:2710–2716

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Gao E, Lei YH, Shang X et al (2010) A novel and efficient model of coronary artery ligation and myocardial infarction in the mouse. Circ Res 107:1445–1453

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Nie L, Wang S, Wang X et al (2014) In vivo volumetric photoacoustic molecular angiography and therapeutic monitoring with targeted plasmonic nanostars. Small 10:1585–1593

    CAS  Article  PubMed  Google Scholar 

  23. Bang JS, Kwon OK, Kim JE et al (2012) Quantitative angiographic comparison with the OSIRIS program between the direct and indirect revascularization modalities in adult moyamoya disease. Neurosurgery 70:625–632

    Article  PubMed  Google Scholar 

  24. Rubin SA, Fishbein MC, Swan HJ (1983) Compensatory hypertrophy in the heart after myocardial infarction in the rat. J Am Coll Cardiol 1:1435–1441

    CAS  Article  PubMed  Google Scholar 

  25. Gajarsa JJ, Kloner RA (2011) Left ventricular remodeling in the post-infarction heart: a review of cellular, molecular mechanisms, and therapeutic modalities. Heart Fail Rev 16:13–21

    Article  PubMed  Google Scholar 

  26. Garcia-Uribe A, Erpelding TN, Krumholz A et al (2015) Dual-Modality Photoacoustic and Ultrasound Imaging System for Noninvasive Sentinel Lymph Node Detection in Patients with Breast Cancer. Sci Rep 5:15748

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Menke J (2015) Photoacoustic breast tomography prototypes with reported human applications. Eur Radiol 25:2205–2213

    Article  PubMed  Google Scholar 

  28. Zhou Y, Wang D, Zhang Y et al (2016) A Phosphorus Phthalocyanine Formulation with Intense Absorbance at 1000 nm for Deep Optical Imaging. Theranostics 6:688–697

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Heijblom M, Steenbergen W, Manohar S (2015) Clinical photoacoustic breast imaging: the Twente experience. IEEE Pulse 6:42–46

    Article  PubMed  Google Scholar 

  30. Horiguchi A, Tsujita K, Irisawa K et al (2016) A pilot study of photoacoustic imaging system for improved real-time visualization of neurovascular bundle during radical prostatectomy. Prostate 76:307–315

    CAS  Article  PubMed  Google Scholar 

  31. Thomas RJ, Rockwell BA, Marshall WJ, Aldrich RC, Zimmerman SA, Rockwell RJ (2002) A procedure for laser hazard classification under the Z136.1-2000 American National Standard for Safe Use of Lasers. J Laser App 14:57–66

    Article  Google Scholar 

  32. Li W, Chen X (2015) Gold nanoparticles for photoacoustic imaging. Nanomedicine (London) 10:299–320

    CAS  Article  Google Scholar 

Download references

Funding

This work was supported by the National Science Foundation of China (81571744 & 81601489), the National Basic Research Program of China (863 Program 2015AA020502), the Fundamental Research Funds for the Central Universities (20720170065 & 20720170036), and the Science Foundation of Fujian Province (no. 2014Y2004).

Author information

Affiliations

  1. State Key Laboratory of Molecular Vaccinology and Molecular Diagnosis & Center for Molecular Imaging and Translational Medicine, School of Public Health, Xiamen University, Xiang’an South Road, Xiang’an District, Xiamen, 361102, Fujian Province, People’s Republic of China

    Jing Lv, Ya Peng, Shi Li, Zhide Guo, Qingliang Zhao, Xianzhong Zhang & Liming Nie

Authors
  1. Jing Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhide Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qingliang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xianzhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Liming Nie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Liming Nie.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Liming Nie, PhD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

Yeda Chen kindly provided statistical advice for this manuscript. No complex statistical methods were necessary for this paper.

Ethical approval

Approval from the institutional animal care committee was obtained.

Methodology

• Prospective

• Experimental

• Performed at one institution

Electronic supplementary material

ESM 1

(DOCX 2243 kb)

ESM 2

(MOV 11657 kb)

ESM 3

(MOV 10971 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lv, J., Peng, Y., Li, S. et al. Hemispherical photoacoustic imaging of myocardial infarction: in vivo detection and monitoring. Eur Radiol 28, 2176–2183 (2018). https://doi.org/10.1007/s00330-017-5209-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-5209-x

Keywords

  • Myocardial infarction
  • Optical imaging
  • Diagnosis
  • Ultrasonography
  • Single-photon emission computed tomography