Breast ultrasound knobology and the knobology of twinkling for marker detection
Introduction
Background
Fourteen years before X-ray devices using molybdenum tubes instead of tungsten tubes ushered in the era of modern mammography units (1), Dr. J. J. Wild from the Department of Surgery at the University of Minnesota first described using high-frequency ultrasound (then called an ultrasonoscope) to image the breast in 1951 (2). Technological advancements in ultrasound hardware and software over the ensuing decades helped to establish its diagnostic value. As early as forty years ago, ultrasound was recognized for its effectiveness in guiding procedures and assessing breast lesions preoperatively (3). Today, breast ultrasound is a standard-of-care diagnostic imaging modality in breast imaging. While ultrasound technology continues to improve, the quality of the ultrasound images remains largely operator-dependent.
Rationale and knowledge gap
In 2003, the risk assessment tool BI-RADS® (Breast Imaging Reporting And Data System), developed by the American College of Radiology (ACR), incorporated breast ultrasound to standardize terminology and communication of findings (4). Accurate description of ultrasound findings using the BI-RADS lexicon depends on the quality of the images acquired. While some parts of image quality may be vendor-dependent, many scanning parameters are vendor-agnostic and can be generally described, leaving it up to the operator to improve image quality based on the underlying science.
Objective
The purpose of this manuscript is to present a high-level approach to obtaining high-quality breast ultrasound images by describing the vendor-agnostic components and available adjustable scanner parameters (here, loosely called “knobs” encompassing both physical and touch-screen versions) when performing breast ultrasound. Additionally, color Doppler ultrasound, mentioned only once in the 2021 ACR Practice Parameter for the Performance of a Breast Ultrasound Examination (5), in the context of characterizing the internal vascularity of the lesion, has been used to evaluate the color Doppler twinkling properties of some breast biopsy markers (6-8). This manuscript includes a description of the knobology of color Doppler twinkling to aid in ultrasound detection of some breast biopsy markers.
Knobology
Ten knobology topics are discussed (Table 1), and for each topic, an “In practice” section provides examples and practical tips on implementation.
Table 1
Section | Topic |
---|---|
I | Transducers |
II | Beam focusing |
III | Power |
IV | Depth |
V | Gain and time gain compensation |
VI | Harmonic imaging |
VII | Spatial compounding |
VIII | Dynamic range |
IX | Beam steering |
X | Color Doppler |
(I) Transducers
The ultrasound transducer transmits sound waves generated by a voltage applied to piezoelectric crystals and detects returning sound waves. Each transducer has a preferred resonant frequency and bandwidth (range of frequencies). The 2021 ACR Practice Parameter for the Performance of a Breast Ultrasound Examination recommends using a high-resolution, real-time, linear-array, broad-bandwidth transducer operating at a center (resonant) frequency of at least 12 MHz, preferably higher (5). The recommendation for a higher center frequency is application-driven because the breasts are relatively superficial structures compared, for example, to the liver and gallbladder where a lower center frequency is more appropriate. The recommendation for a broad bandwidth describing a broader range of transmitted and received frequencies provides the benefits of higher resolution with higher frequencies and deeper tissue penetration with lower frequencies, all with the same transducer.
Transducers are primarily characterized by the range of sound wave frequencies (MHz), emitted from the transducer. The frequencies of the sound waves are determined by the properties of the piezoelectric crystals that make up part of the transducer. A high-frequency transducer typically used for breast ultrasound may operate at a frequency range of 5–15 MHz. On the scanner console, there is often a knob that allows the user to select a center frequency within the range of frequencies allowed by the transducer. The sound waves leave the transducer in short bursts or pulses at a rate characterized by the pulse repetition frequency (PRF) or number of pulses emitted from the transducer in one second (Hz).
One of the first steps in acquiring high-quality images is to understand which transducer may be best suited for the task at hand. Ultrasound image resolution of the desired imaging target is determined primarily by the transducer’s frequency and footprint (linear, curvilinear, or phased array). The axial and lateral resolutions (LRs) of the image acquisitions (Figure 1) primarily determine the in-plane resolution of the image, while the out-of-plane resolution or “slice thickness” is determined by the elevation resolution. The axial resolution is determined by the spatial pulse length (SPL), which is a function of frequency, f, and pulse length in terms of N cycles (SPL = Nλ = Nc/f where c is the speed of sound in tissue, commonly assumed as 1,540 m/s and λ is the ultrasound wavelength). The LR is also related to the wavelength and the size of the aperture or footprint used to transmit and receive. Linear transducers are favored for more superficial imaging, such as the breasts, while curvilinear transducers, which have a larger footprint or aperture compared to linear transducers, are often used for deeper structures, such as those in the abdomen or pelvis. The increased lateral coverage afforded with a curvilinear transducer compared to a linear transducer is different from its LR which is still dependent on wavelength or frequency (9). The relationship is fundamentally described by the following equation:
where zf is the focal depth and D is the aperture width.
On some ultrasound scanners, there is an option to turn on virtual convex imaging for linear transducers; this expands the field of view by post-processing acquired signals or employing vendor-specific steering.
In practice
Transducers with lower transmit frequencies send and receive signals that can penetrate through more tissue at the cost of lower axial resolution (Figure 1), but this may be useful in certain applications, for instance, when imaging breasts with more than 3 cm of tissue while in the supine position, deep lesions, lactating breasts, mastitis, inflammatory breast cancer, or dense breasts. High transmit frequencies (e.g., >12 MHz) mean higher axial resolution at the cost of less tissue penetration, but this may be ideal, for example, for imaging superficial lesions, interrogating the nipple-areolar complex, or locating superficial findings such as some biopsy markers.
When evaluating a possible sebaceous cyst or epidermal inclusion cyst and looking for the tract in the skin, using an even higher frequency transducer, 18 or 24 MHz, for example, may be helpful for identifying the tract in the skin or for better characterizing the finding (Figure 2). High-frequency transducers can sometimes be used to assess for the presence of a sonographically visible marker (clip) in a resected specimen, such as a positive lymph node, in the operating room while waiting for the specimen radiograph.
(II) Beam focusing knobs
The ultrasound beam, which is affected by many factors, refers to the collection of acoustic waves emanating from the piezoelectric crystals. Using beam-focusing knobs, the operator can narrow the ultrasound beam and improve the resolution in that area. Because the axial resolution is inherently better than the LR in ultrasound, narrowing the ultrasound beam improves the LR more than the axial resolution of the image. Beam-focusing knobs allow the operator to choose a single focus of beam narrowing or create a column or effective focus of narrowing by using multiple foci (Figure 3) and combining the results from multiple pulse-echo acquisitions. For some vendors, the distance between the foci of narrowing can be specified by the user. Regardless of the combination of adjustments made, the overall effect is to improve the resolution of the image at the area(s) of beam narrowing, generally referred to as the focal zone; the LR is further improved with higher transmit frequencies. One of the trade-offs of using multiple focal points is a decrease in frame rate, which is generally minimal and may not be readily noticeable.
In practice
Adjusting the focal zones is generally an automatic step in breast ultrasound, particularly when imaging a particular finding. Whether one focal zone or multiple focal zones are used depends on the case at hand. Spending time to cycle through a few focal zones can sometimes provide more information on the finding (Figures 4,5). For very superficial findings, such as those in the skin, a thick layer of gel may help bring the finding to the level of the most superficial focal zones (Figure 6). This technique may also be helpful when scanning the nipple-areolar complex or near surgical scars with keloid formations.
In practice, knob adjustments may not result in appreciable diagnostic changes (Figure 7), likely due to the variable sonographic features of suspicious breast findings. Until the pathologic changes contributing to sonographic characteristics are better understood, it is advisable to briefly adjust the knobs such as focal zones, as this may provide additional diagnostic information. One tip to consider when evaluating deeper structures is compressing the transducer a little more, effectively dispersing overlying tissues and suspensory ligaments that can shadow the deeper tissues. This tip, combined with optimizing the focal zone, can sometimes produce sharper images of a deep finding.
(III) Power knob
Ultrasound waves emitted from the transducer are a source of acoustic energy measured in Joules (J), and the rate at which the energy is deposited in the tissues is called the power [measured in Watts (W) or J/s]. The power or acoustic output knob on an ultrasound scanner is distinct from the on-off button. The power knob is an adjustable knob that controls the acoustic output power of the ultrasound waves which affects the intensity of the sound waves that penetrate the tissues. Increasing the intensity of the sound waves (i.e., the signal) can provide increased penetration of the sound waves, which may be advantageous in some settings, such as when imaging an obese patient (10). However, if the scanned target is associated with reverberations, increasing the power increases the signal arising from these artifacts as well, so the diagnostic value must consider these factors.
High-power deposition of sound waves into tissues can cause bioeffects such as tissue heating and cavitation (11,12). Regulations associated with the power did not arise until 1976 when the United States Food and Drug Administration set a limit for fetal use, but this was later increased in 1992 with the mandate to display the bioeffects of increased power (13). Displayed on ultrasound scanners are the mechanical index (MI) and the thermal index (TI), which change with changes in the power or acoustic output. The MI is unitless with higher values related to the probability of ultrasound waves that can generate very tiny gas bubbles in tissues and cause them to oscillate and break, causing adverse effects. The TI is also unitless and reflects the increase in temperature of the tissues at the focal zone of the ultrasound beam. For example, a TI of 2 would indicate that the temperature of the tissues there could potentially increase by 2 °C.
Although adverse bioeffects caused by acoustic output in breast ultrasound have not been described (14), one cross-sectional study of various ultrasound exams showed that breast imaging was associated with the highest TI (0.74±0.29) and the lowest MI (0.34±0.54) compared, for example, to thyroid ultrasounds with some of the lowest TI values and ankle ultrasounds with the highest MI values (15). Clinical ultrasound scans should generally be performed with an MI of 0–1.9 and a TI of 0–2.0.
In practice
Awareness of the MI and TI of a scan is particularly important in first-trimester fetal ultrasound when organogenesis occurs, and fetal tissue is most sensitive. Adhering to the principle of as low as reasonably achievable (ALARA) aids in achieving a diagnostic quality exam while maximizing safety. Lowering the power, using color flow Doppler judiciously, and decreasing the scan duration by either using the “Freeze” button when not scanning or avoiding keeping the probe stationary for long periods during scanning can be considered. In practice in breast imaging, the acoustic output is generally at 100% while still maintaining safe MI and TI values (Figure 8).
(IV) Depth knob
Breast sonographers are trained to capture most findings in the center of the field of view. The reason is not entirely to frame the finding but to improve frame rates. If the depth of the imaging field of view is 6 cm, sound waves need, at a minimum, to penetrate through at least 6 cm of tissue and return to the transducer. In practice, a little more time is needed to account for non-zero beam angle cases or for the somewhat more theoretical scenario when the signal from the leftmost element travels to the rightmost bottom corner of the field-of-view. A shallower depth means it takes less time for the sound waves to travel through this depth and travel back to the transducer. This increases the frame rate or how quickly the image refreshes; this can be important in evaluating moving structures, such as a pulsing artery. The underlying ultrasound parameter that ties the depth and frame rate together is the PRF, which again refers to the number of ultrasound pulses emitted from the transducer in one second. The higher the PRF, the lower the imaging depth because there is inadequate time for the echoes to travel back to the transducer.
In practice
While it is important to frame a finding so that it is centered in the image, it is also important to acquire at least one image that frames the finding to show the depth of the finding in the breast relative to known anatomic structures. For example, it is helpful to acquire an image of a finding that includes the pectoralis muscle so that it can be determined whether the finding is anterior depth, middle depth, or posterior depth. This can provide more confident correlation with a mammographic finding (Figure 9).
(V) Gain and time gain compensation (TGC) knobs
Adjusting the gain of a parameter generally amplifies the signal associated with that parameter without affecting the MI or TI. In B-mode (brightness or grayscale) ultrasound imaging, increasing the gain increases the overall brightness of the image because increasing the gain amplifies the signals of the echoes after being received by the transducer, effectively making the image brighter. On most ultrasound scanners, there are knobs (typically a collection of sliders on the physical console or touch screen) called TGC or depth gain compensation which allow the operator to adjust the gain at different depths. For instance, when there is a loss in the signal of the echoes due to scattering or absorption (i.e., attenuation) in the deeper tissues, the TGC knobs can be adjusted to preferentially increase the amplitude of the echoes in the deeper tissues returning to the transducer.
In practice
Adjusting the gain and TGC knobs are nearly reflexive for breast sonographers as they assess the echotexture of findings and surrounding tissues. It is important to know that an anechoic finding is not falsely anechoic because the gain was too low (Figure 10). When adjusting the gain of the signal, it is important to keep in mind the interrelation between various scanning parameters. For example, changing the B-mode transmit frequency affects the default gain. So, if there is a finding that cannot be optimally depicted, changing the frequency and then the gain or TGC knobs may be helpful.
This is particularly helpful when imaging more challenging anatomy such as the nipple or subareolar region, or when imaging deeper tissues or the axilla.
(VI) Harmonic imaging knob
Sound waves transmitted from the transducer leave the transducer at a fundamental frequency, f0, that enters the tissues. As the sound waves travel through the tissues, nonlinear effects create harmonic frequencies, which are generally integer multiples of the transmitted fundamental frequency (e.g., 2f0, 3f0, etc.). Of these harmonic frequencies, the second harmonic frequency, which is two times the fundamental frequency, 2f0, provides the most useful diagnostic information (16). The harmonic imaging knob sets the ultrasound scanner so that the harmonic frequencies are processed.
Imaging with harmonic frequencies generally results in fewer artifacts from scatter that arise from the fundamental frequency, particularly in deeper tissues, thereby creating clearer, less noisy images (16). This may be particularly notable in more heterogeneous breast tissues where there are several interfaces between the fatty lobules and fibroglandular tissues that are comprised mostly of suspensory ligaments, glandular components, ducts, and vasculature (Figure 11). A trade-off for clearer imaging with harmonic imaging is a slower frame rate because processing the harmonic frequencies takes longer than processing just the fundamental frequency or depending on the vendor may involve transmitting more than one time to create the harmonic image. Since harmonic imaging is often used when imaging deeper structures, the increased imaging depth also contributes to the slower frame rate. But, improving technologies provide strategies to mitigate the slower frame rate. For example, some scanners may use pulse inversion imaging which requires two transmissions for each beam/frame thereby lowering the frame rate by a factor of 2 (17).
In practice
Harmonic imaging can improve the contrast and sharpness of the tissue echotexture that often reflects the heterogeneous nature of breast parenchyma. For example, turning on harmonic imaging can provide another look at the margins of masses adjacent to glandular tissue, often improving their conspicuity (Figure 12). When using harmonic imaging, the functionality of the gain and TGC knobs also applies. The details of how harmonic imaging is implemented are often vendor-specific, and the operator would need to determine when and how best to use harmonic imaging.
Harmonic imaging can be helpful when searching for axillary lymph nodes (16); this is illustrated in Figure 13. While harmonic imaging decreases the frame rate and can be distracting during a procedure, it can still be used during a procedure to provide improved visualization of the target; the slower frame rate could be mitigated by having the sonographer toggle harmonic imaging on and off and if possible decreasing the depth to target. Additionally, harmonic imaging can be used with other transducers (Figure 14) or transmit frequencies (Figure 15).
With improved spatial resolution and contrast-to-noise ratio, harmonic imaging can be used to “clean up” cystic masses making them more anechoic by reducing any reverberation artifacts. However, it is important to realize that harmonic information alone may not provide sufficient information about the internal architecture of a mass, and additional characterization is needed to distinguish between a solid and a cystic mass.
(VII) Spatial compounding knob
The spatial compounding knob acquires multiple acquisitions of the same area usually at different steering angles to create a composite image. Doing so often increases the signal-to-noise ratio of the composite image improving clarity of details such as margin characteristics (Figures 16,17). Spatial compounding also reduces the speckle or graininess of the image.
Speckle occurs when small structures scatter the sound waves causing constructive and destructive interference that creates the speckly pattern. Like harmonic imaging, the details of how spatial compounding is implemented is usually vendor-specific. For example, speckle reduction can involve frame averaging or other filtering algorithms whereby information from more than one frame is combined to improve the signal yielding a less noisy image.
In practice
In breast ultrasound, spatial compound imaging is the default. On occasion, turning off spatial compound imaging may be helpful to evaluate shadowing characteristics of metallic biopsy markers, for example, or to evaluate for posterior acoustic enhancement associated with cysts.
(VIII) Dynamic range
Dynamic range in ultrasound provides control of how one wants to visualize the range of acquired echoes. Dynamic range is similar to window and leveling in computed tomography. Choosing to display a narrow dynamic range results in a high-contrast image, while a wide dynamic range results in a low-contrast image (Figure 18).
In practice
Lowering the dynamic range can be used to create a higher contrast image, which may provide more contrast at the margins. However, the trade-off is that some detail in the very high signal areas and in the very low signal areas can be lost. Analogously, a wide dynamic range image results in much less contrast, making it more challenging to distinguish the tissue planes (Figures 19-21).
(IX) Beam steering knob
Beam steering allows the operator to angle the beam of ultrasound waves emitted from the transducer. This effectively directs the beam of waves so their angle of insonation in tissues is changed, potentially improving the visualization.
In practice
Beam steering can be particularly helpful when looking for the needle tip during a fine-needle aspiration (FNA) of a deep axillary lymph node (Figure 22, Videos S1,S2).
(X) Color Doppler knob for twinkling detection of breast biopsy markers
Color Doppler is an ultrasound technique that can determine the velocity of moving structures, usually blood flow. Color Doppler twinkling, on the other hand, is characterized by a temporally changing color mosaic pattern that was first described with kidney stones in 1996 (18). Literature over the past three years reports ultrasound color Doppler twinkling as a readily available ultrasound technique for detecting some breast biopsy markers such as the Tumark Q (Hologic, Marlborough, MA, USA), the Trimark Cork (Hologic), and the Tumark MRI-safe Flex (Hologic) markers (6-8,19). The literature has also described some twinkling associated with the Twirl Ring marker (20).
Twinkling-detection of breast biopsy markers is currently reduced to five steps related to the probe (transducer), color Doppler frequency, gain, and scale.
Probe: select a lower-frequency range transducer (Figure 23), such as a curvilinear transducer with a transmit frequency of 1–6 MHz, which is often used in abdominal ultrasound imaging.
Color flow Doppler: color flow Doppler is a knob that is available on nearly every ultrasound scanner and is generally used for quantifying blood flow (Figure 24) with scanning techniques that often consider compression and the angle of the beam. But for twinkling detection, the color Doppler knob simply needs to be turned on without too much consideration paid to operator-dependent scanning. While the underlying cause of twinkling is still under active investigation, twinkling is a compelling qualitative diagnostic feature that is readily recognized.
Frequency: after color Doppler is turned on, there is an option for selecting the color Doppler transmit frequency (Figure 25). Selecting a color Doppler transmit frequency (f0) will change the scale (cm/s) because of the relationship between color Doppler transmit frequency (f0) and velocity (v) for a given Doppler shift (fd). Color Doppler twinkling changes with color Doppler frequencies, and lower color Doppler transmit frequencies typically lead to better twinkling.
Gain: as described before, gain affects the amplification of the overall signal measured. In this case, it is the Doppler gain, and adjusting the Doppler gain affects the strength or amplitude of the ultrasound signal affecting the appearance of the twinkling (Figure 26). Typical starting values are 60–80% of the maximum. High gain values may introduce noise from hand motion or patient respiration. Low gain values may suppress twinkling signals.
Scale: the scale associated with color Doppler adjusts the range of velocities measured by the Doppler imaging (Figure 27). It is usually a range of velocities between −v cm/s to +v cm/s. So, when imaging an artery, the scale can be increased to reflect higher blood flows in the arteries compared to the veins, and also to minimize aliasing. In the context of using color Doppler for detection of twinkling, adjusting the scale can be used to eliminate vascular flow, particularly when trying to minimize any false-positive twinkling that is arising from vascular flow. If the twinkling is weak, lowering the scale may be helpful. If the twinkling is strong, adjusting the scale may not appreciably change the appearance of the twinkling.
In practice
Ultrasound color Doppler twinkling is readily apparent for some commercial breast biopsy markers (Tumark Q, TriMark Cork, and Tumark MRI-safe Flex) (6-8,19) and for markers made from polymethyl methacrylate (Figure 28) (21).
Color Doppler is vendor agnostic making twinkling of markers a relatively straightforward scanning technique by adjusting four knobs: the color Doppler knob (turn it on); the color Doppler frequency; the gain; and the scale. This technique is summarized in Appendix 1 that summarizes tips for using color Doppler twinkling to detect some breast biopsy markers. Those who like to use mnemonics can consider “Penguins Can’t Fly Gracefully South” to recall the roles of probe (transducer) selection, color Doppler, color Doppler frequency, gain, and scale.
Discussion
Ultrasound is integral to any breast imaging practice, and awareness of the functionalities of the knobs on the ultrasound console is critical to ensure that imaging features accurately characterize a finding. Like other imaging modalities, ultrasound involves trade-offs. It is important to recognize that optimizing scanning parameters to enhance image quality will compromise other parameters, so being able to discern diagnostic features from artifacts is essential. The ever-questioning breast sonographer will always ask whether the scanning parameters have inadvertently made cancer look like a benign cyst which usually leads to unfortunate consequences. Skills in breast ultrasound must be dynamic and continuously improved to keep pace with advancing ultrasound technologies and to troubleshoot challenging patient cases effectively. This manuscript provides a vendor-agnostic, high-level review of ten frequently used knobs in breast ultrasound along with practical tips relevant to each knob.
Many ultrasound scanners offer an automated feature that optimizes scanning parameters without the user knowing exactly what may have been altered. Knowing how to optimize an ultrasound scan without the automated feature gives one more control over what one sees. Oftentimes, ultrasound image acquisitions are based on what the practice or individual breast radiologist prefers. Because of the varied preferences, many breast radiologists still back-scan after the breast sonographer, not so much to rectify a scanning error, but to better appreciate the imaging findings in real-time.
Many breast ultrasound practices establish scanning protocols for various clinical indications. For instance, a protocol for axillary imaging may include how many transverse and longitudinal images to take and how many images to take with measurements. Such protocols can add uniformity to scans and are usually executed after practice consensus. “Recipes” for how to approach a breast ultrasound may include tips such as “Use Auto Optimize to add contrast to your image as needed”. While such recipes may be helpful for those onboarding, de facto use of knobs has the potential to miss opportunities to optimize scanning parameters and acquire higher-quality, more convincing diagnostic ultrasound images. With advancing technologies in ultrasound scanners that tout nuanced differences based on vendors, basic breast ultrasound knobology remains the same, and the quality of breast ultrasound will still be very much operator-dependent. Therefore, a better understanding of breast ultrasound knobology can benefit the sonographer, the breast radiologist, and most importantly, the patient.
Ultrasound color Doppler twinkling for detecting some breast biopsy markers is a readily available technique that is relatively easy to execute. Of the more than three dozen breast biopsy markers commercially available, not all markers twinkle, but those that do twinkle, such as the Tumark Q, the Trimark Cork, the Tumark MRI-safe Flex, and a marker made of polymethyl methacrylate (21,22), improved confidence in identifying these markers for ultrasound-guided preoperative localization can make a significant impact on the management of patients with breast cancer.
One size does not fit all in breast ultrasound. More often than not, the ultrasound target is indeterminate, and ultrasound has to provide the best representation of relevant features of the finding that will ultimately determine the level of suspicion and the management. For example, distinguishing a benign cyst that may be slightly inflamed or contain internal debris from a cancer is often non-trivial. In Figure 29, the sonographer took a side-by-side image of a finding without and with harmonics. The information provided by acquiring images with and without harmonic imaging is non-contradictory when one realizes what harmonic imaging is acquiring. Assimilating nuanced information from additional image acquisitions can help with the interpretation.
Conclusions
A breast radiologist is only as good as the quality of the images acquired. Breast ultrasound knobology with additional consideration of ultrasound twinkling for marker detection, as presented here, hopes to help and empower those who perform breast ultrasounds to acquire the images that can make a positive difference in patient care.
Acknowledgments
Funding: The effort for this manuscript was funded in part by
Footnote
Peer Review File: Available at https://tbcr.amegroups.org/article/view/10.21037/tbcr-24-30/prf
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tbcr.amegroups.org/article/view/10.21037/tbcr-24-30/coif). C.U.L. serves as an unpaid editorial board member of Translational Breast Cancer Research from October 2023 to September 2025. C.U.L. and M.W.U. are co-PIs on a National Institute of Biomedical Imaging and Bioengineering (NIBIB) grant (R01 EB033008) to the Mayo Clinic and on an internal Mayo Clinic Discovery Translation Program award. Patents are pending for non-metallic ultrasound detectable markers as well as Doppler ultrasound twinkling technologies. G.K.H. was supported by NIBIB grant (R01 EB033008) to the Mayo Clinic and by an internal Mayo Clinic Discovery Translation Program award. The other authors have no other conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
References
- Nicosia L, Gnocchi G, Gorini I, et al. History of Mammography: Analysis of Breast Imaging Diagnostic Achievements over the Last Century. Healthcare (Basel) 2023;11:1596. [Crossref] [PubMed]
- WILD JJ. NEAL D. Use of high-frequency ultrasonic waves for detecting changes of texture in living tissues. Lancet 1951;1:655-7. [PubMed]
- Fornage BD, Toubas O, Morel M. Clinical, mammographic, and sonographic determination of preoperative breast cancer size. Cancer 1987;60:765-71. [Crossref] [PubMed]
- Lee J. Practical and illustrated summary of updated BI-RADS for ultrasonography. Ultrasonography 2017;36:71-81. [Crossref] [PubMed]
- Lee CS, Bohm-Velez M. ACR Practice Parameter for the Performance of a Diagnostic Breast Ultrasound Examination. Am Coll Radiol 2021. Available online: https://www.acr.org/-/media/ACR/Files/Practice-Parameters/US-Breast.pdf
- Jakub JW, Hesley GK, Larson NB, et al. Ultrasonographic Detection and Surgical Retrieval of a Nonmetallic Twinkle Marker in Breast Cancer: Pilot Study. Radiol Imaging Cancer 2022;4:e220053. [Crossref] [PubMed]
- Lee CU, Larson NB, Urban MW, et al. Factors Associated With Ultrasound Color Doppler Twinkling by Breast Biopsy Markers: In Vitro and Ex Vivo Evaluation of 35 Commercially Available Markers. AJR Am J Roentgenol 2023;220:358-70. [Crossref] [PubMed]
- Lee CU, Piltin MA, Moldoveanu D, et al. Using US Twinkling Artifact to Identify Breast Biopsy Markers: Brief Report. Radiol Imaging Cancer 2023;5:e220168. [Crossref] [PubMed]
- Hangiandreou NJ. AAPM/RSNA physics tutorial for residents. Topics in US: B-mode US: basic concepts and new technology. Radiographics 2003;23:1019-33. [Crossref] [PubMed]
- Cibull SL, Harris GR, Nell DM. Trends in diagnostic ultrasound acoustic output from data reported to the US Food and Drug Administration for device indications that include fetal applications. J Ultrasound Med 2013;32:1921-32. [Crossref] [PubMed]
- Quarato CMI, Lacedonia D, Salvemini M, et al. A Review on Biological Effects of Ultrasounds: Key Messages for Clinicians. Diagnostics (Basel) 2023;13:855. [Crossref] [PubMed]
- Fowlkes JBBioeffects Committee of the American Institute of Ultrasound in Medicine. American Institute of Ultrasound in Medicine consensus report on potential bioeffects of diagnostic ultrasound: executive summary. J Ultrasound Med 2008;27:503-15. [Crossref] [PubMed]
- Sheiner E, Freeman J, Abramowicz JS. Acoustic output as measured by mechanical and thermal indices during routine obstetric ultrasound examinations. J Ultrasound Med 2005;24:1665-70. [Crossref] [PubMed]
- Moyano DB, Paraiso DA, González-Lezcano RA. Possible Effects on Health of Ultrasound Exposure, Risk Factors in the Work Environment and Occupational Safety Review. Healthcare (Basel) 2022;10:423. [Crossref] [PubMed]
- Fatahi Asl J, Farzanegan Z, Tahmasbi M, et al. Evaluation of the Scan Duration and Mechanical and Thermal Indices Applied for the Diagnostic Ultrasound Examinations. J Ultrasound Med 2021;40:1839-50. [Crossref] [PubMed]
- Anvari A, Forsberg F, Samir AE. A Primer on the Physical Principles of Tissue Harmonic Imaging. Radiographics 2015;35:1955-64. [Crossref] [PubMed]
- Simpson DH, Chin CT, Burns PN. Pulse inversion Doppler: a new method for detecting nonlinear echoes from microbubble contrast agents. IEEE Trans Ultrason Ferroelectr Freq Control 1999;46:372-82. [Crossref] [PubMed]
- Rahmouni A, Bargoin R, Herment A, et al. Color Doppler twinkling artifact in hyperechoic regions. Radiology 1996;199:269-71. [Crossref] [PubMed]
- Lee CU, Hesley GK, Uthamaraj S, et al. Using Ultrasound Color Doppler Twinkling to Identify Biopsy Markers in the Breast and Axilla. Ultrasound Med Biol 2021;47:3122-34. [Crossref] [PubMed]
- Tan MP, Bi Z, Ong EMW. The ‘twinkle’ artifact - A novel method of clip identification to facilitate targeted axillary surgery following neoadjuvant chemotherapy in breast cancer patients. Clin Imaging 2020;68:36-44. [Crossref] [PubMed]
- Lee CU, Urban MW, Lee Miller A 2nd, et al. Twinkling-guided ultrasound detection of polymethyl methacrylate as a potential breast biopsy marker: a comparative investigation. Eur Radiol Exp 2022;6:26. [Crossref] [PubMed]
- Lee CU, Urban MW, Hesley GK, et al. Long-Term Ultrasound Twinkling Detectability and Safety of a Polymethyl Methacrylate Soft Tissue Marker Compared to Conventional Breast Biopsy Markers-A Preclinical Study in a Porcine Model. Ultrasound Med Biol 2024;50:1001-9. [Crossref] [PubMed]
Cite this article as: Lee CU, Hesley GK, Pierson TA, Higgins RL, Urban MW. Breast ultrasound knobology and the knobology of twinkling for marker detection. Transl Breast Cancer Res 2024;5:28.