Abstract
Background and aim
Multispectral optoacoustic tomography (MSOT) represents a new in vivo imaging technique with high resolution (~250 μm) and tissue penetration (>1 cm) using the photoacoustic effect. While ultrasound contains anatomical information for lesion detection, MSOT provides functional information based on intrinsic tissue chromophores. We aimed to evaluate the feasibility of combined ultrasound/MSOT imaging of breast cancer in patients compared to healthy volunteers.
Methods
Imaging was performed using a handheld MSOT system for clinical use in healthy volunteers (n = 6) and representative patients with histologically confirmed invasive breast carcinoma (n = 5) and ductal carcinoma in situ (DCIS, n = 2). MSOT values for haemoglobin and oxygen saturation were assessed at 0.5, 1.0 and 1.5 cm depth and selected wavelengths between 700 and 850 nm.
Results
Reproducible signals were obtained in all wavelengths with consistent MSOT signals in superficial tissue in breasts of healthy individuals. In contrast, we found increased signals for haemoglobin in invasive carcinoma, suggesting a higher perfusion of the tumour and tumour environment. For DCIS, MSOT values showed only little variation compared to healthy tissue.
Conclusions
This preliminary MSOT breast imaging study provided stable, reproducible data on tissue composition and physiological properties, potentially enabling differentiation of solid malignant and healthy tissue.
Key Points
• A handheld MSOT probe enables real-time molecular imaging of the breast.
• MSOT of healthy controls provides a reproducible reference for pathology identification.
• MSOT parameters allows for differentiation of invasive carcinoma and healthy tissue.
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Abbreviations
- DCIS:
-
Ductal carcinoma in situ
- MRI:
-
Magnetic resonance imaging
- MSOT:
-
Multispectral optoacoustic tomography
- OA:
-
Optoacoustic
- PET:
-
Positron emission tomography
- ROI:
-
Region of interest
- RUCT:
-
Reflection ultrasound computed tomography
- US:
-
Ultrasound
References
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90
Shankar LK, Hoffman JM, Bacharach S et al (2006) Consensus recommendations for the use of 18F-FDG PET as an indicator of therapeutic response in patients in National Cancer Institute Trials. J Nucl Med 47:1059–1066
Erickson-Bhatt SJ, Roman M, Gonzalez J, et al (2015) Noninvasive surface imaging of breast cancer in humans using a hand-held optical imager. Biomed Phys Eng Express 1(4). doi:10.1088/2057-1976/1/4/045001
Zografos G, Liakou P, Koulocheri D et al (2015) Differentiation of BIRADS-4 small breast lesions via Multimodal Ultrasound Tomography. Eur Radiol 25:410–418
Berg WA, Cosgrove DO, Dore CJ et al (2012) Shear-wave elastography improves the specificity of breast US: the BE1 multinational study of 939 masses. Radiology 262:435–449
Song JL, Chen C, Yuan JP, Sun SR (2016) Progress in the clinical detection of heterogeneity in breast cancer. Cancer Med 5:3475–3488
Buehler A, Kacprowicz M, Taruttis A, Ntziachristos V (2013) Real-time handheld multispectral optoacoustic imaging. Opt Lett 38:1404–1406
Valluru KS, Willmann JK (2016) Clinical photoacoustic imaging of cancer. Ultrasonography 35:267–280
Dima A, Ntziachristos V (2016) In-vivo handheld optoacoustic tomography of the human thyroid. Photoacoustics 4:65–69
Taruttis A, Timmermans AC, Wouters PC, Kacprowicz M, van Dam GM, Ntziachristos V (2016) Optoacoustic imaging of human vasculature: feasibility by using a handheld probe. Radiology 281:256–263
Bell AG (1881) The production of sound by radiant energy. Science 2:242–253
Taruttis A, Ntziachristos V (2015) Advances in real-time multispectral optoacoustic imaging and its applications. Nat Photonics 9:219–227
Taruttis A, Wildgruber M, Kosanke K et al (2013) Multispectral optoacoustic tomography of myocardial infarction. Photoacoustics 1:3–8
McCormack D, Al-Shaer M, Goldschmidt BS et al (2009) Photoacoustic detection of melanoma micrometastasis in sentinel lymph nodes. J Biomech Eng 131, 074519
McNally LR, Mezera M, Morgan DE et al (2016) Current and emerging clinical applications of Multispectral Optoacoustic Tomography (MSOT) in Oncology. Clin Cancer Res 22:3432–3439
Neuschmelting V, Lockau H, Ntziachristos V, Grimm J, Kircher MF (2016) Lymph node micrometastases and in-transit metastases from melanoma: in vivo detection with multispectral optoacoustic imaging in a mouse model. Radiology 280:137–150
Bhutiani N, Grizzle WE, Galandiuk S et al (2016) Non-invasive imaging of colitis using multispectral optoacoustic tomography. J Nucl Med 58:1009–1012
Grosenick D, Rinneberg H, Cubeddu R, Taroni P (2016) Review of optical breast imaging and spectroscopy. J Biomed Opt 21, 091311
Tromberg BJ, Shah N, Lanning R et al (2000) Non-invasive in vivo characterisation of breast tumors using photon migration spectroscopy. Neoplasia 2:26–40
Xu M, Wang LV (2005) Universal back-projection algorithm for photoacoustic computed tomography. Phys Rev E Stat Nonlin Soft Matter Phys 71, 016706
Mercep E, Burton NC, Claussen J, Razansky D (2015) Whole-body live mouse imaging by hybrid reflection-mode ultrasound and optoacoustic tomography. Opt Lett 40:4643–4646
Folkman J (1994) Angiogenesis and breast cancer. J Clin Oncol 12:441–443
Vaupel P, Hockel M (2000) Blood supply, oxygenation status and metabolic micromilieu of breast cancers: characterisation and therapeutic relevance. Int J Oncol 17:869–879
Becker A, Grosse Hokamp N, Zenker S et al (2015) Optical in vivo imaging of the alarmin S100A9 in tumor lesions allows for estimation of the individual malignant potential by evaluation of tumor-host cell interaction. J Nucl Med 56:450–456
Gilkes DM, Semenza GL (2013) Role of hypoxia-inducible factors in breast cancer metastasis. Future Oncol 9:1623–1636
Ham M, Moon A (2013) Inflammatory and microenvironmental factors involved in breast cancer progression. Arch Pharm Res 36:1419–1431
Heijblom M, Piras D, Brinkhuis M et al (2015) Photoacoustic image patterns of breast carcinoma and comparisons with Magnetic Resonance Imaging and vascular stained histopathology. Sci Rep 5:11778
Ntziachristos V, Yodh AG, Schnall MD, Chance B (2002) MRI-guided diffuse optical spectroscopy of malignant and benign breast lesions. Neoplasia 4:347–354
Enfield LC, Gibson AP, Hebden JC, Douek M (2009) Optical tomography of breast cancer-monitoring response to primary medical therapy. Target Oncol 4:219–233
Compliance with ethical standards
Guarantor
The scientific guarantor of this publication is Moritz Wildgruber.
Conflict of interest
The authors of this manuscript declare relationships with the following companies:
Jing Claussen and Steven J. Ford are employees of iThera Medical, a manufacturer of commercial optoacoustic scanners.
Funding
The authors state that this work has not received any funding.
Statistics and biometry
One of the authors has significant statistical expertise.
No complex statistical methods were necessary for this paper.
Informed consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical approval
Institutional Review Board approval was waived because scans were obtained during a pilot test series, which was covered under the Declaration of Helsinki §37 (‘individual healing research’)
Methodology
• prospective
• experimental
• performed at one institution
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Anne Becker and Max Masthoff contributed equally to this work.
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Becker, A., Masthoff, M., Claussen, J. et al. Multispectral optoacoustic tomography of the human breast: characterisation of healthy tissue and malignant lesions using a hybrid ultrasound-optoacoustic approach. Eur Radiol 28, 602–609 (2018). https://doi.org/10.1007/s00330-017-5002-x
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DOI: https://doi.org/10.1007/s00330-017-5002-x