Abstract
Recent technological developments in ultrasound (US) imaging and ultrasound contrast
agents (UCAs) have improved diagnostic confidence in echography. In the clinical management
of melanoma, contrast-enhanced ultrasound (CEUS) imaging complements conventional
US imaging (i.e., high-resolution US and Doppler imaging) for clinical examination and therapeutic
follow-up. These developments have set into motion the combined use of ultrasound
and UCAs as a new modality for drug delivery. This modality, called sonoporation,
has emerged as a non-invasive, targeted and safe method for the delivery of therapeutic
drugs into melanoma. This review focuses on the results and prospects of using US
and UCAs as dual modalities for CEUS imaging and melanoma treatment.
Key Words
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Ultrasound in Medicine and BiologyAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Basic immunology: Functions and disorders of the immune system.Saunders, Philadelphia, PA2006
- Evaluation of the potential of doxorubicin loaded microbubbles as a theranostic modality using a murine tumor model.Acta Biomater. 2015; 19: 112-118
- Asymptomatic metastatic melanoma of the gallbladder diagnosed with contrast-enhanced ultrasonography.J Ultrasound Med. 2010; 29: 1133-1137
- Imaging methods for ultrasound contrast agents.Ultrasound Med Biol. 2020; 46: 498-517
- Metastases of malignant melanoma in the gastrointestinal tract.Geriatrics. 1969; 24: 112-120
- Ultrasound-mediated delivery and distribution of polymeric nanoparticles in the normal brain parenchyma of a metastatic brain tumour model.PLoS One. 2018; 13e0191102
- MRI and PET/CT features of abdominal manifestations of cutaneous melanoma: A review of current concepts in the era of tumor-specific therapies.Abdom Radiol. 2021; 46: 2219-2235
- Doxil®—The first FDA-approved nano-drug: lessons learned.J Control Release. 2012; 160: 117-134
- Gallbladder metastasis: Spectrum of imaging findings.Abdom Imaging. 2011; 36: 729-734
- Contrast-enhanced ultrasound with perflubutane for sentinel lymph node mapping in cutaneous melanoma: A pilot study.Laryngoscope. 2019; 129: 1117-1122
- American Academy of Dermatology. Guidelines of care for the management of primary cutaneous melanoma.J Am Acad Dermatol. 2011; 65: 1032-1047
- Current uses of diagnostic high-frequency US in dermatology.Eur J Radiol. 1998; 27: S215-S223
- Doxorubicin: The good, the bad and the ugly effect.Curr Med Chem. 2009; 16: 3267-3285
- Critical analysis of the ultrasonographic criteria for diagnosing lymph node metastasis in patients with cutaneous melanoma: A systematic review.J Ultrasound Med. 2011; 30: 547-560
- Metastatic melanoma in the chest and abdomen: The great radiologic imitator.Semin Ultrasound CT MR. 2014; 35: 272-289
- SPECT/CT improves detection of metastatic sentinel lymph nodes in patients with head and neck melanoma.Ann Surg Oncol. 2016; 23: 2652-2657
- One-step surgical removal of cutaneous melanoma with surgical margins based on preoperative ultrasound measurement of the thickness of the melanoma.Eur J Dermatol. 2018; 28: 202-208
- Core needle biopsy of soft tissue tumors, CEUS vs US guided: A pilot study.J Ultrasound. 2015; 18: 335-342
- Rectal melanoma presenting as a solitary complex cystic liver lesion: Role of contrast-specific low-MI real-time ultrasound imaging.J Ultrasound. 2016; 19: 135-139
- The tail and the string sign: New Sonographic features of subcutaneous melanoma metastasis.Ultrasound Med Biol. 2017; 43: 370-374
- Contrast-enhanced ultrasound: A filter role in AJCC stage I/II melanoma patients.Oncology. 2010; 79: 370-375
- Accuracy of core-needle biopsy after contrast-enhanced ultrasound in soft-tissue tumours.Eur Radiol. 2010; 20: 2740-2748
- The potential of antigen and TriMix sonoporation using mRNA-loaded microbubbles for ultrasound-triggered cancer immunotherapy.J Control Release. 2014; 194: 28-36
- Cochrane Skin Cancer Diagnostic Test Accuracy Group. Ultrasound, CT, MRI, or PET-CT for staging and re-staging of adults with cutaneous melanoma.Cochrane Database Syst Rev. 2019; 7CD012806
- Update on current treatment recommendations for primary cutaneous melanoma.Dermatol Clin. 2019; 37: 397-407
- Bubble-assisted ultrasound: Application in immunotherapy and vaccination.Adv Exp Med Biol. 2016; 880: 243-261
- Phase I trial of sorafenib in combination with IFN alpha-2a in patients with unresectable and/or metastatic renal cell carcinoma or malignant melanoma.Clin Cancer Res. 2007; 13: 1801-1809
- Cancer incidence and mortality patterns in Europe: Estimates for 40 countries and 25 major cancers in 2018.Eur J Cancer. 2018; 103: 356-387
- Evaluation of tumor angiogenesis with US: Imaging, Doppler, and contrast agents.Acad Radiol. 2000; 7: 824-839
- Phase I/II trial of imatinib and bevacizumab in patients with advanced melanoma and other advanced cancers.Oncologist. 2015; 20: 952-959
- Comparing contrast-enhanced ultrasound to immunohistochemical markers of angiogenesis in a human melanoma xenograft model: Preliminary results.Ultrasound Med Biol. 2002; 28: 445-451
- Monitoring angiogenesis in human melanoma xenograft model using contrast-enhanced ultrasound imaging.Ultrason Imaging. 2008; 30: 237-246
- The antiangiogenic effects of a vascular endothelial growth factor decoy receptor can be monitored in vivo using contrast-enhanced ultrasound imaging.Mol Imaging. 2014; 13: 1-9
- Ultrasound contrast imaging: Current and new potential methods.Ultrasound Med Biol. 2000; 26: 965-975
- Three decades of ultrasound contrast agents: A review of the past, present and future improvements.Ultrasound Med Biol. 2020; 46: 892-908
- Preoperative ultrasonic assessment of thin melanocytic skin lesions using a 100-MHz ultrasound transducer: A comparative study.Dermatol Surg. 2007; 33: 818-824
- Gasfilled ultrasound microbubbles enhance the immunoactivity of the HSP70MAGEA1 fusion protein against MAGEA1expressing tumours.Mol Med Rep. 2018; 18: 315-321
- Estimation of intra-operator variability in perfusion parameter measurements using DCE-US.World J Radiol. 2011; 3: 70-81
- Assessment of quantitative perfusion parameters by dynamic contrast-enhanced sonography using a deconvolution method: An in vitro and in vivo study.J Ultrasound Med. 2012; 31: 595-608
- Self-assembled liposome-loaded microbubbles: The missing link for safe and efficient ultrasound triggered drug-delivery.J Control Release. 2011; 152: 249-256
- Melanoma staging: American Joint Committee on Cancer (AJCC) 8th edition and beyond.Ann Surg Oncol. 2018; 25: 2105-2110
- Sentinel lymph nodes in a swine model with melanoma: Contrast-enhanced lymphatic US.Radiology. 2004; 230: 727-734
- Contrast-enhanced ultrasound imaging of sentinel lymph nodes after peritumoral administration of Sonazoid in a melanoma tumor animal model.J Ultrasound Med. 2011; 30: 441-453
- The molecular basis for the pharmacokinetics and pharmacodynamics of curcumin and its metabolites in relation to cancer.Pharmacol Rev. 2014; 66: 222-307
- Ultrasound diagnosis of metastatic melanoma of the gallbladder.Br J Radiol. 1997; 70: 1122-1125
- Opto-acoustic synergistic irradiation for vaporization of natural melanin-cored nanodroplets at safe energy levels and efficient sono-chemo-photothermal cancer therapy.Theranostics. 2020; 10: 10448-10465
- The global burden of melanoma: Results from the Global Burden of Disease Study 2015.Br J Dermatol. 2017; 177: 134-140
- Surgical management of melanoma of the gallbladder: A report of 13 cases and review of the literature.Am J Surg. 2007; 193: 493-497
- Ultrasound molecular imaging of cancer: design and formulation strategies of targeted contrast agents.Recent Results Cancer Res. 2020; 216: 319-336
- Ultrasound-responsive cavitation nuclei for therapy and drug delivery.Ultrasound Med Biol. 2020; 46: 1296-1325
- Prognostic value of angiogenesis evaluated with high-frequency and color Doppler sonography for preoperative assessment of melanomas.AJR Am J Roentgenol. 2002; 178: 1547-1551
- Prognostic value of angiogenesis evaluated with high-frequency and colour Doppler sonography for preoperative assessment of primary cutaneous melanomas: Correlation with recurrence after a 5 year follow-up period.Cancer Imaging. 2006; 6: 24-29
- Dynamic contrast-enhanced ultrasonography (DCE-US) with quantification of tumor perfusion: A new diagnostic tool to evaluate the early effects of antiangiogenic treatment.Eur Radiol. 2007; 17: F89-F98
- Dynamic contrast-enhanced ultrasonography (DCE-US): A new tool for the early evaluation of antiangiogenic treatment.Target Oncol. 2010; 5: 53-58
- Validation of dynamic contrast-enhanced ultrasound in predicting outcomes of antiangiogenic therapy for solid tumors: The French Multicenter Support for Innovative and Expensive Techniques study.Invest Radiol. 2014; 49: 794-800
- Early quantitative evaluation of a tumor vasculature disruptive agent AVE8062 using dynamic contrast-enhanced ultrasonography.Invest Radiol. 2008; 43: 100-111
- Combining functional imaging and interstitial pressure measurements to evaluate two anti-angiogenic treatments.Invest New Drugs. 2012; 30: 144-156
- Molecular ultrasound imaging using contrast agents targeting endoglin, vascular endothelial growth factor receptor 2 and integrin.Ultrasound Med Biol. 2015; 41: 197-207
- Versatile utilization of real-time intraoperative contrast-enhanced ultrasound in cranial neurosurgery: Technical note and retrospective case series.Neurosurg Focus. 2016; 40: E6
- Design and evaluation of doxorubicin-containing microbubbles for ultrasound-triggered doxorubicin delivery: Cytotoxicity and mechanisms involved.Mol Ther. 2010; 18: 101-108
- Clinical development and potential of photothermal and photodynamic therapies for cancer.Nat Rev Clin Oncol. 2020; 17: 657-674
- Contrast-enhanced sonography for detection of secondary lymph nodes in a melanoma tumor animal model.J Ultrasound Med. 2014; 33: 939-947
- IR780-Based light-responsive nanocomplexes combining phase transition for enhancing multimodal imaging-guided photothermal therapy.Biomater Sci. 2019; 7: 1132-1146
- Value of perfusion parameters for differentiating hepatocellular carcinoma and liver metastasis with hypervascularity and a normal hepatic background on contrast-enhanced ultrasound imaging.J Ultrasound Med. 2019; 38: 2601-2608
- Preoperative measurement of thickness of cutaneous melanoma using high-resolution 20 MHz ultrasound imaging: A monocenter prospective study and systematic review of the literature.Ultrasound Med Biol. 2009; 35: 1411-1420
- Synergistic inhibition of malignant melanoma proliferation by melphalan combined with ultrasound and microbubbles.Ultrason Sonochem. 2011; 18: 1218-1224
- Quantitative assessment of cancer vascular architecture by skeletonization of high-resolution 3-D contrast-enhanced ultrasound images: Role of liposomes and microbubbles.Technol Cancer Res Treat. 2014; 13: 541-550
- Are metastases really hypovascular in the arterial phase? The perspective based on contrast-enhanced ultrasonography.J Ultrasound Med. 2007; 26: 1545-1556
- Sentinel lymph node characterization with a dual-targeted molecular ultrasound contrast agent.Mol Imaging Biol. 2018; 20: 221-229
- Performance of molecular lymphosonography for detection and quantification of metastatic involvement in sentinel lymph nodes.J Ultrasound Med. 2019; 38: 2103-2110
- Sentinel node detection in melanomas using contrast-enhanced ultrasound.Acta Radiol. 2009; 50: 412-417
- CAELYX Breast Cancer Study Group. Reduced cardiotoxicity and comparable efficacy in a phase III trial of pegylated liposomal doxorubicin HCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer.Ann Oncol. 2004; 15: 440-449
- Prophylactic immunization with bubble liposomes and ultrasound-treated dendritic cells provided a four-fold decrease in the frequency of melanoma lung metastasis.J Control Release. 2012; 160: 362-366
- Dynamic contrast-enhanced ultrasound parametric maps to evaluate intratumoral vascularization.Invest Radiol. 2015; 50: 212-217
- Intraoperative contrast-enhanced ultrasound for brain tumor surgery.Neurosurgery. 2014; 74 (discussion 552): 542-552
- Ultrasound-triggered spatiotemporal delivery of topotecan and curcumin as combination therapy for cancer.J Pharmacol Exp Ther. 2019; 370: 876-893
- Curcumin encapsulated lecithin nanoemulsions: An oral platform for ultrasound mediated spatiotemporal delivery of curcumin to the tumor.Sci Rep. 2020; 10: 8587
- Endothelial cells, first target of drug delivery using microbubble-assisted ultrasound.Ultrasound Med Biol. 2020; 46: 1565-1583
- Microbubble ultrasound: How can it help detect melanoma metastasis?.Int J Dermatol. 2006; 45: 1004-1006
- Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: Diagnostic performance and confidence.Radiology. 2004; 232: 420-430
- Staging melanoma: What's old and new.Surg Clin North Am. 2020; 100: 29-41
- Combination of HIFU therapy with contrast-enhanced sonography for quantitative assessment of therapeutic efficiency on tumor grafted mice.Ultrasound Med Biol. 2006; 32: 729-740
- Contrast-enhanced ultrasound for characterizing lymph nodes with focal cortical thickening in patients with cutaneous melanoma.AJR Am J Roentgenol. 2011; 196: W8-W12
- Potential use of contrast-enhanced ultrasound (CEUS) in the detection of metastatic superficial lymph nodes in melanoma patients.Ultraschall Med. 2014; 35: 67-71
- Current clinical trials in the treatment of advanced melanomas.Surg Clin North Am. 2020; 100: 201-208
- Improved differentiation of benign and malignant lymphadenopathy in patients with cutaneous melanoma by contrast-enhanced color Doppler sonography.Arch Dermatol. 2002; 138: 491-497
- Tumor vascularization in experimental melanomas: Correlation between unenhanced and contrast enhanced power Doppler imaging and histological grading.Ultrasound Med Biol. 2001; 27: 761-771
- F-18-fluoro-2-deoxyglucose positron emission tomography (PET) and PET/computed tomography imaging in primary staging of patients with malignant melanoma: A systematic review.Syst Rev. 2012; 1: 62
- Sehgal CM. Dose–response relationship of ultrasound contrast agent in an in vivo murine melanoma model.Cancer Imaging. 2007; 7: 216-223
- Microbubble-mediated ultrasound drug-delivery and therapeutic monitoring.Expert Opin Drug Deliv. 2017; 14: 1031-1043
- High frequency ultrasound in the preoperative staging of primary melanoma: A statistical analysis.Melanoma Res. 2002; 12: 287-290
- Helper T-cell responses and clinical activity of a melanoma vaccine with multiple peptides from MAGE and melanocytic differentiation antigens.J Clin Oncol. 2008; 26: 4973-4980
- MR imaging of hepatic metastasis in patients with malignant melanoma: Evaluation of suspected lesions screened at contrast-enhanced CT.Eur J Radiol. 2012; 81: 714-718
- Inhibition of melanoma by ultrasound-microbubble-aided drug delivery suggests membrane permeabilization.Cancer Biol Ther. 2007; 6: 1276-1283
- Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure.J Control Release. 2010; 142: 245-250
- Sentinel lymph node biopsy in cutaneous melanoma: Standard and new technical procedures and clinical advances. A systematic review of the literature.Clin Nucl Med. 2016; 41: e498-e507
- Therapeutic effects of paclitaxel-containing ultrasound contrast agents.Ultrasound Med Biol. 2006; 32: 1771-1780
- Development of an ultrasound-responsive and mannose-modified gene carrier for DNA vaccine therapy.Biomaterials. 2010; 31: 7813-7826
- Suppression of melanoma growth and metastasis by DNA vaccination using an ultrasound-responsive and mannose-modified gene carrier.Mol Pharm. 2011; 8: 543-544
- Enhancement of gene expression by transcriptional activation using doxorubicin-loaded liposome/pDNA complexes.Pharmazie. 2012; 67: 400-405
- The role of lymph node ultrasound evaluation in melanoma—Review of the literature.Med Ultrason. 2016; 18: 224-230
- Diffuse hepatic infiltration by metastatic melanoma.Oncology (Williston Park). 2019; 33629386
- Ultrasound morphology criteria predict metastatic disease of the sentinel nodes in patients with melanoma.J Clin Oncol. 2010; 28: 847-852
- Synergistic delivery of gold nanorods using multifunctional microbubbles for enhanced plasmonic photothermal therapy.Sci Rep. 2014; 4: 5685
- Differentiation of malignant liver tumors by software-based perfusion quantification with dynamic contrast-enhanced ultrasound (DCEUS).Clin Hemorheol Microcirc. 2019; 71: 39-51
- Acute increases in murine tumor echogenicity after antivascular ultrasound therapy: A pilot preclinical study.J Ultrasound Med. 2009; 28: 795-800
- Multifunctional PVCL nanogels with redox-responsiveness enable enhanced MR imaging and ultrasound-promoted tumor chemotherapy.Theranostics. 2020; 10: 4349-4358
- Ultrasound-mediated interferon beta gene transfection inhibits growth of malignant melanoma.Biochem Biophys Res Commun. 2011; 411: 137-142
- Sonoporation delivery of interleukin-27 gene therapy efficiently reduces prostate tumor cell growth in vivo.Hum Gene Ther. 2011; 22: 1537-1550
Article info
Publication history
Published online: August 29, 2022
Accepted:
June 24,
2022
Received in revised form:
June 21,
2022
Received:
May 3,
2022
Footnotes
Rose-Anne Thépault's present location is UMR 1307, CRCI2NA, Université de Nantes, INSERM, Nantes, France.
Identification
Copyright
© 2022 World Federation for Ultrasound in Medicine & Biology. All rights reserved.