The History of US: From Bats and Boats to the Bedside and Beyond: RSNA Centennial Article
2015; Radiological Society of North America; Volume: 35; Issue: 3 Linguagem: Inglês
10.1148/rg.2015140300
ISSN1527-1323
AutoresKatherine Kaproth-Joslin, Refky Nicola, Vikram S. Dogra,
Tópico(s)Phonocardiography and Auscultation Techniques
ResumoHomeRadioGraphicsVol. 35, No. 3 PreviousNext Special ExhibitsFree AccessThe History of US: From Bats and Boats to the Bedside and Beyond: RSNA Centennial ArticleKatherine A. Kaproth-Joslin , Refky Nicola, Vikram S. DograKatherine A. Kaproth-Joslin , Refky Nicola, Vikram S. DograAuthor AffiliationsFrom the Department of Imaging Science, University of Rochester Medical Center, 601 Elmwood Ave, Rochester, NY 14642.Address correspondence to K.A.K.J. (e-mail: [email protected]).Katherine A. Kaproth-Joslin Refky NicolaVikram S. DograPublished Online:Mar 30 2015https://doi.org/10.1148/rg.2015140300MoreSectionsPDF ToolsImage ViewerAdd to favoritesCiteTrack CitationsPermissionsReprints ShareShare onFacebookTwitterLinked In AbstractIntroductionUltrasonography (US) is one of the most commonly used imaging modalities worldwide. It provides a safe, reliable, noninvasive, and portable means to screen, diagnose, follow, and treat disease. This technology is driven by the science of sound waves, with images generated from the deflected echoes of inaudible high-frequency sound waves transmitted into an object of interest.The history of US imaging goes back hundreds of years, beginning in the late 1700s with a theoretic explanation for bat aviation. US imaging became a viable method for medical imaging in the early 1900s and finally developed into a pivotal diagnostic and therapeutic tool in modern medicine.The purpose of this article is to review the history of US, starting with the early research that formed the building blocks of US imaging. Then the beginnings of the medical era in US imaging are explored by examining the innovators behind the technologic discoveries of the transmission method and the pulse-echo method. Finally, the expanding role of US imaging is covered through its current and future directions: improved US portability and cost, innovative diagnostic applications, and the growing US role in interventional therapies.From Bats to Patient Care: Building Blocks of US ImagingThe history of US starts with Lazzaro Spallanzani (1729–1799), an Italian physiologist and priest who designed a set of experiments to explain how bats were able to fly at night (Fig 1). By studying the bat's ability to see and hear, Spallanzani noted that if a bat was blinded, it was still able to fly confidently through space; however, when a bat was made deaf, even in one ear, it could not fly safely in the experimental environment. On the basis of these findings, Spallanzani hypothesized that bats relied on sound, not their vision, to navigate (1). In 1938, two Harvard students, Donald Griffin and Robert Galambos, coined the word echolocation to explain how bats generate high-frequency clicks that bounce off surfaces and then receive and use the returned echoes to calculate the exact location of objects within their environment (1,2).Figure 1 Drawing of Lazzaro Spallanzani (1729–1799), an Italian physiologist and priest. (Image in the public domain.)Figure 1Download as PowerPointOpen in Image Viewer In 1826, Jean-Daniel Colladon (1802–1893), a Swiss physicist, and his assistant, Jacques Charles-Francois Sturm (1803–1855), demonstrated that the speed of sound in water is faster than its speed in air. Their experiment consisted of two boats separated by a distance of 10 miles (16 km). A church bell was suspended underwater from one boat, and a trumpetlike instrument used to amplify sound was suspended underwater from the other boat (Fig 2) (3). The purpose of the experiment was to measure the time that it took for the sound of the bell to reach the second boat, as timed from a flash of gunpowder ignited as the bell was rung. On the basis of this simple experiment, the speed of sound in water was calculated as 1435 m/sec, a value remarkably similar to the current standard of 1482 m/sec used in modern-day physics (4,5).Figure 2 Drawing of Jean-Daniel Colladon (1802–1893), a Swiss physicist, and his assistant, Jacques Charles-Francois Sturm (1803–1855), calculating the speed of sound in water. This image was originally published in reference 3. (Image in the public domain.)Figure 2Download as PowerPointOpen in Image Viewer Doppler shift, also known as the Doppler effect, was first postulated in 1842 by Austrian physicist Christian Doppler (1803–1853) (Fig 3). This concept described how changes in light wave frequency accounted for the visible color variation of stars (6,7). In 1845, this idea was applied to sound waves in an experiment performed by Dutch mathematician C. H. D. Buys Ballot (1817–1890), who used a train station and horn players on a train as a source of sound to explain how sound from a moving source changes as it is heard by an observer (7). When a sound-producing object moves toward an observer, the received frequency of sound is higher than the emitted frequency; when the sound producer and the observer are at the same point, the emitted and received frequencies are identical; and when the sound producer moves away from an observer, the received frequency is lower than the emitted frequency.Figure 3 Photograph of Christian Doppler (1803–1853), an Austrian physicist. (Image in the public domain.)Figure 3Download as PowerPointOpen in Image Viewer Piezoelectricity (from the Greek word piezen, meaning to press or squeeze) was first discovered by brothers Jacques (1856–1941) and Pierre (1859–1906) Curie. They demonstrated that crystals of tourmaline, quartz, topaz, cane sugar, or Rochelle salt can generate electricity under pressure and that when a voltage is applied to these crystalline materials, pressure waves can be generated (8,9). The capacity of these crystals to both generate and receive pressure waves in the range of megahertz frequencies allowed the development of modern-day transducer technology (9).After the tragic sinking of the Titanic in 1912, Reginald Fessenden (1866–1932), a Canadian electrical engineer, worked to pioneer an ultrasound-based collision avoidance system by converting an underwater Morse code generator into an echo sounder. The machine produced high-frequency sound waves with "a reciprocating induction motor" moving at the rate of 540 times per second (10). Although the machine was able to detect an iceberg as far as 2 miles (3.2 km) away, the continuous, rather than intermittent, output of echoes created its own interference, limiting the commercial application of the device as an iceberg avoidance system (Fig 4) (10,11).Figure 4 Photograph of Reginald Fessenden (1866–1932) and the Fessenden oscillator. This image was originally published in reference 11. (Image courtesy of the National Oceanic and Atmospheric Administration Photo Library.)Figure 4Download as PowerPointOpen in Image Viewer As submarine technology continued to advance during World War I, the field of US was quickly taking form. Using the dual nature of piezoelectricity, Paul Langevin (1872–1946), a French physicist, created a quartz-based transmitter-receiver of high-frequency sound waves called the hydrophone (1,10). Consisting of small quartz crystals glued between two steel plates, the underwater device was able to detect clearly the returning echoes from a submerged submarine (10). This apparatus was considered one of the most useful technologies for identifying enemy submarines, thereby protecting ship convoys. Subsequently, improvements in this technology during World War II led to the development of the field later known as sonar (acronym for sound navigation and ranging]) (1,10).Beginnings of Medical US: Technologic Discoveries and the Innovators behind ThemTransmission MethodThe first physician to use ultrasound for medical imaging was Karl Dussik (1908–1968), an Austrian neurologist who attempted to depict changes in brain ventricle size secondary to tumor growth. In his early application of US technology, transducers were placed on both sides of a patient's partly submerged head. The sound waves were transmitted at a known rate from one transducer to another transducer by using a through-transmission technique. The changes in the sound waves were recorded photographically on heat-sensitive paper, creating a two-dimensional representation of what was thought to be the patient's ventricles, referred to as a "ventriculogram" (12,13). Although the findings from later experiments demonstrated that many of these echo variations were actually artifacts secondary to normal reflections and attenuations of the skull, this experiment was one of the earliest attempts to depict an organ in vivo (14,15).Because of the limitations of the through-transmission technique, this imaging method was largely abandoned in the 1950s. This technique was replaced by the more-traditional pulse-echo method of US imaging, in which the transducer both produces and receives the transmitted sound wave and its reflected echo. The pulse-echo method is used in A-, B-, and M-mode US imaging.Pulse-Echo MethodA-Mode US.—A-mode (amplitude-mode) US represents a one-dimensional characterization of a reflected sound wave that uses a pulse-echo technique to determine the depth and dimensions of an organ. Echo amplitude is plotted on the vertical axis, and the time needed for the echo to return is plotted on the horizontal axis. This creates a graph of different heights along a single line in the plane of the sound beam. Limitations of this method include the inability to determine direction or the shape of an object from which the echo originated. This mode has been made relatively obsolete by B-mode US; however, A-mode US is still used today in ophthalmology to measure the orbital length and assess for intraocular masses (16).George D. Ludwig (1922–1973), an American physician, was the first to convert A-mode US imaging, which had been used to detect minute flaws in metal, into medical applications (Figs 5, 6). His initial research focused on the physical characteristics of ultrasound in various tissues, identifying the acoustic impedance of fat, muscle, and various types of gallstones (17). Ludwig then implanted human gallstones into the back muscle of a dog and into the gallbladders of three dogs and subsequently was able to show discrete US echoes consistent with the implanted gallstones (17). This observation was the first in vivo depiction of a human gallstone in an animal model.Figures 5 Photograph of George D. Ludwig (1922–1973), an American physician. (Image courtesy of American Institute of Ultrasound in Medicine [AIUM] historical archive.)Figures 5Download as PowerPointOpen in Image Viewer Figures 6 Photograph of A-mode US scanning equipment used by George D. Ludwig to assess the diagnostic capabilities of US. (Image courtesy of AIUM historical archive.)Figures 6Download as PowerPointOpen in Image Viewer B-Mode US.—B-mode (brightness-mode) US, or gray-scale US, is the workhorse of modern US, displaying two-dimensional images of echo-generating boundaries in a single plane, adding directionality to the traditional one-dimensional A-mode data. Each sound wave reflected back to the transducer is represented as a point on a gray-scale image. The brightness of the point is proportional to the strength of the returning sound wave. The location of the point is extrapolated from the position of the transducer and the transit time of the sound wave. As the technology improved, the ability to create multiple individual B-mode images in rapid succession allowed real-time imaging and subsequent recordings of cine images.John J. Wild (1914–2009), a World War II surgeon, became interested in using US as a noninvasive method to detect bowel injury. Using A-mode US equipment originally designed to read radar maps of enemy territory, Wild (18) was able to accurately measure wall thickness in living bowel and to identify tumor arising from the stomach wall of a patient. Wild collaborated with John M. Reid (1926–), an electrical engineer, and they developed a method to detect and image tumors of the soft tissues, including the breast and colon (Fig 7). In 1952, they produced two-dimensional US (B-mode) images of the bovine kidney cortex; Wild and Reid (19) subsequently identified recurrent tumor in the thigh of a human patient. Further research led to the development of the original handheld B-mode transducer (20,21). The device was then modified for internal imaging with the development of the rectal and vaginal probes, which were used to identify colon and ovarian pathologic abnormalities.Figure 7 Photograph of John J. Wild (1914–2009) (at left), a surgeon, and John M. Reid (1926–) (at right), an electrical engineer, comparing the echogenic traces from tumor and normal tissue. (Image courtesy of AIUM historical archive.)Figure 7Download as PowerPointOpen in Image Viewer Wild and Reid were not alone in their quest to improve pulse-echo US. Douglas Howry (1920–1969) chose to leave his formal radiology residency training in 1948 to focus on US research (Fig 8). In his studies, Howry concentrated on the reflection of sound waves from tissue interfaces and understanding how these echoes could be used to produce diagnostic-quality images. By using an "immersion tank ultrasound system," which required a patient or the specimen to be submerged in water, Howry and associates produced the first two-dimensional cross-sectional images of diagnostic quality, which were published in 1952 and 1954 (22,23). The first motorized "Somascope" had a submerged US transducer that moved horizontally along a wooden rail around the rim of the patient's immersion tank, producing compound circumferential images from different angles. The multiposition nature of the imaging reduced artifact from extraneous echoes, producing high-quality diagnostic images, which were referred to as "somagrams." To eliminate the need for total immersion, a pan-scanner was later developed in 1957 by Howry's team, in which a semicircular pan of water with a submerged transducer carriage was strapped to the patient's body, producing diagnostic-quality somagrams.Figure 8 Photograph of Douglas Howry (1920–1969). (Image courtesy of AIUM historical archive.)Figure 8Download as PowerPointOpen in Image Viewer The limitations of submersion-based US imaging included the need to immerse the patient in water, the length of time needed to scan, and the immobility of the apparatus. Although this imaging modality created superior diagnostic-quality sonographic images when compared with handheld direct-contact scanners, the inconveniences of this system would lead this imaging method to fall into disfavor.M-Mode US.—M-mode (motion-mode) US is commonly used in cardiac and fetal cardiac imaging to evaluate heart motion. This modality displays a one-dimensional image of echo amplitude over time. The ultrasound beam is repeatedly transmitted into a single plane, with the reflected echo amplitudes displayed as pixels of varying strengths projected over time. Nonmoving echogenic structures create flat lines, whereas moving structures cause upward and downward inflections of the line. Image interpretation relies on assessment of these variation patterns in conjunction with a solid understanding of the underlying anatomic relationships from specific motion configurations, which are especially important in the assessment of cardiac valves, chambers, and vessel walls.In the late 1940s, physicians started performing surgery to dilate stenotic mitral valves, a procedure that helped many but not all patients. Because of this variable response, patients underwent preoperative screening with cardiac catheterization to assess for other conditions, such as mitral regurgitation (24). Unhappy with the invasive nature of cardiac catheterization, Inge Edler (1911–2001), a Swedish physician, and Carl Hellmuth Hertz (1920–1990), a physicist, began investigating US as a noninvasive alternative (24,25). Using a borrowed reflectoscope, which was designed for nondestructive materials testing, Edler and Hertz were able to detect heart motion on the existing oscilloscope screen (Fig 9). Encouraged by these results, they began characterizing heart anatomy, measuring cardiac free wall and septal thickness, and establishing the visibility of the muscle-fluid interface (24,25). One of the key concepts developed by Edler and Hertz was a recording technique designed to image the actively moving cardiac structures over time. As they filmed the oscilloscope screen at constant speed, straight lines represented echoes returning from nonmoving structures, and modulations of line position corresponded to echoes returning from moving structures (Fig 10) (24,25).Figure 9 Photograph of a reflectoscope converted by Inge Edler (1911–2001) and Carl Hellmuth Hertz (1920–1990) into an M-mode echocardiographic machine with a camera attached. (Image courtesy of AIUM historical archive.)Figure 9Download as PowerPointOpen in Image Viewer Figure 10 Original M-mode images obtained from the converted reflectoscope shown in Figure 9. Left: Image shows normal motion of the anterior leaflet of the mitral valve. Right: Image shows stenosis of the anterior leaflet of the mitral valve. (Images courtesy of AIUM historical archive.)Figure 10Download as PowerPointOpen in Image Viewer Doppler Imaging.—Traditional gray-scale images are dependent on the strength of the returning echo and the length of time that the echo took to return to the transducer. Doppler imaging takes into account a third factor, the change, or shift, in the frequency of the returning echo as compared with the emitted frequency. On the basis of the phenomenon of Doppler shift, echoes reflecting off structures traveling toward the transducer will have an increased frequency when they are compared with the transmitted frequency, and echoes reflecting off structures moving away from the transducer will have a lower frequency (Fig 11). The change in frequency, or frequency shift, identified within a region of interest can be directly converted to a measurement of velocity. Interestingly, the shifts in blood velocity Doppler frequency are within the audible range, producing the characteristic pulsing sound of blood flow that can be played through the speakers of the US machine. Doppler imaging remains a powerful tool in the analysis of vascular structures by evaluating the presence, direction, and velocity of flow.Figure 11 Doppler effect, or Doppler shift. Drawings show that for stationary structures such as the kidney, the returning echo does not show a change in frequency (Doppler shift) when compared with the transmitted frequency. For moving echogenic structures, such as the red blood cell, echoes reflecting off objects traveling toward the transducer will have an increased frequency compared with the transmitted frequency, and echoes reflecting off objects moving away from the transducer will have a lower frequency.Figure 11Download as PowerPointOpen in Image Viewer Japanese physicist Shigeo Satomura (1919–1960) began his career studying the effects of ultrasound and microwave vibration on wooden boards, before shifting his interest to the medical applications of ultrasound. Interested in cardiac wall motion, Satomura showed that Doppler signals could be obtained from the beat of the heart and from valve movement by using a 3-MHz transducer with a frequency spectrogram output (26–28). On the basis of these findings, Satomura and his associates began applying Doppler methods to the study of heart movement and flow in peripheral vessels (27–31). Importantly, the findings from this work established that blood flow in peripheral veins and arteries could be identified transcutaneously. In addition, the results of Satomura's studies showed that the velocity of blood flow corresponds to changes in frequency shift. Although it was originally thought that the detected Doppler signal originated from the flow of blood itself, it was later discovered that the return signal was generated by echoes reflecting off red blood cells moving within the blood. In addition, it was shown that the wave frequency shift was proportional to the velocity of the flow and that the magnitude of the voltage output corresponded to the number of red blood cells (27,28,32).Important improvements in Doppler imaging occurred in the 1970s, including the development of color Doppler imaging, spectral Doppler imaging, and continuous-wave Doppler imaging. For color Doppler imaging, a color-coded map of mean Doppler shifts is overlaid at a particular position onto a B-mode image. The color values typically represent direction of flow and magnitude of signal. Spectral Doppler imaging allows measurement of both the velocity change throughout a cardiac cycle and also the distribution of velocities in a sample volume by plotting the velocity change of a single region with time and generating an analyzable waveform pattern. Continuous-wave Doppler US imaging can be used to measure all flow velocities along an entire line of interrogation, which allows detection of high flow that is above the pulsed wave detection threshold (Fig 12). The disadvantage of continuous-wave Doppler imaging is the inability to determine the depth of signal origin.Figure 12 Image showing the first spectral analysis of a continuous-wave Doppler flow signal. (Image courtesy of AIUM historical archive.)Figure 12Download as PowerPointOpen in Image Viewer Power Doppler imaging was added to the Doppler imaging arsenal in 1993 through the work of Jonathan M. Rubin and Ronald S. Adler (33). With this method, the power or strength of the Doppler signal is encoded regardless of flow direction or velocity once a frequency shift has been detected. This imaging technique is most useful when the flow signal is weak, especially in the setting of slow flow, deep vessels, or small-caliber vessels.Expanding Role of US: Current and Future DirectionsThe field of US has allowed important strides in medical imaging, not only in the improved caliber of diagnostic imaging, but also in new and unique medical applications. Driven by the groundbreaking historical and early medical advances of US, improvements in sonography continue to provide innovative ways to detect, diagnose, and treat disease.The Radiological Society of North America (RSNA) has been instrumental in facilitating US research and education nationally and internationally, especially through its journals and national meetings. US research made its debut in Radiology in 1965 with a discussion of its role in cerebral tomography (34). Since that landmark article, more than 7500 articles focusing on US research and the clinical applications of US technology have been published in Radiology and RadioGraphics, the two main journals of the RSNA.Two additional influential and pioneering US-based organizations are the AIUM and the Society of Radiologists in Ultrasound (SRU). The AIUM was established to promote US education, scientific activities, and professional activities for all US professionals, including physicians, sonographers, scientists, engineers, health care providers, and manufacturers of US equipment. The SRU focuses on radiologists who perform US and promotes the advancement of US-based science, practice, and teaching in the field of radiology.Although a full discussion of all the current and future uses of US is too vast to include in this article, a few of the most promising avenues in US research are discussed. These research avenues include improvements in portability and cost, innovative diagnostic applications, and a growing role in interventional therapies.Improved Portability and Cost: Compact USThe original immersion tanks used by Dussik and Howry, which required the patient to be submerged in water, were cumbersome, inconvenient, and expensive. Research investigators have worked to overcome these limitations by improving portability and imaging quality, decreasing expense, and improving the patient experience, all while enhancing diagnostic accuracy. Compact US, a portable and inexpensive handheld US device, has improved the accessibility of US, especially for fields outside radiology, such as cardiology and emergency medicine, and in areas in which medical care is limited, such as in developing countries (35,36). Compact US has also allowed improvement of procedure-based skills in the hospital and outpatient setting, particularly in the guidance of central venous catheter insertion and thoracentesis. As a result, patient outcomes have improved because of the decreased risk of adverse events associated with these procedures (37,38).Innovative Diagnostic ApplicationsUS Elastography.—US elastography is the sonographic technique that provides a quantitative measurement of tissue stiffness based on the premise that malignancy tends to reduce the elasticity of the affected tissue. Stiff tissues demonstrate less distortion under compression and transmit sound waves more rapidly, as compared with softer more-elastic tissues (39,40). Two basic methods for measuring tissue elasticity are strain imaging and shear-wave imaging. Strain imaging measures how easily tissues deform in response to applied pressure. In this method, a region of interest is first identified with B-mode US. Changes in dimensions and echo pattern are then obtained before and after external manual or automatic compression, generating an "elastogram," or qualitative map of relative tissue stiffness (Fig 13) (39–41). Shear-wave imaging uses a high-power "push-pulse" transmitted into a region of interest to cause displacement of the tissues and then generates a shear wave that is perpendicular to the original push-pulse. The velocity of the shear wave is used to calculate tissue stiffness, with stiffer tissues propagating waves faster than softer tissues (40).Figure 13a Elastography of the prostate. (a) Two-dimensional gray-scale US image of the prostate shows a normal appearance of the parenchyma. (b) Corresponding sonoelastogram shows an isolated peripheral lesion of the prostate depicted as a dark area (arrows) in a background of normal prostate parenchyma (green). Note that the color overlay corresponds to tissue elasticity, with black being the hardest or stiffest. Later, a biopsy of this lesion was performed, and the histopathologic findings disclosed cancer of the prostate. (Reprinted, with permission, from reference 41.)Figure 13aDownload as PowerPointOpen in Image Viewer Figure 13b Elastography of the prostate. (a) Two-dimensional gray-scale US image of the prostate shows a normal appearance of the parenchyma. (b) Corresponding sonoelastogram shows an isolated peripheral lesion of the prostate depicted as a dark area (arrows) in a background of normal prostate parenchyma (green). Note that the color overlay corresponds to tissue elasticity, with black being the hardest or stiffest. Later, a biopsy of this lesion was performed, and the histopathologic findings disclosed cancer of the prostate. (Reprinted, with permission, from reference 41.)Figure 13bDownload as PowerPointOpen in Image Viewer Contrast Agent–enhanced US.—Contrast-enhanced US imaging improves depiction of flow in small-caliber vessels or in the setting of slow blood flow, common limitations of traditional Doppler imaging. The most commonly used US contrast agent is microbubbles, which are small microspheres composed of a gas core and a lipid, protein, or polymer stabilizer shell (42,43). The microspheres measure 1–4 µm in diameter and are restricted to the vasculature. The gas core of the microbubbles creates a highly reflective surface that scatters sound waves and produces unique harmonics at imaging frequencies of 1–15 MHz (40,42). Similar to computed tomographic (CT) and magnetic resonance (MR) imaging contrast agents, US contrast agents enable both identification and characterization of lesions, including a dynamic vascular assessment (Fig 14) (41). Unlike CT and MR imaging contrast agents, however, US contrast agents typically are limited to evaluation of a single lesion for each dynamic contrast injection because the transducer must remain fixed over an area or lesion during the course of the contrast injection.Figure 14 Contrast-enhanced US. Gray-scale (B-mode) US image of the kidney shows US contrast enhancement of the renal arterial blood supply. (Reprinted, with permission, from reference 41.)Figure 14Download as PowerPointOpen in Image Viewer Tissue Harmonic Imaging.—Tissue harmonic imaging takes advantage of the harmonic signal created by the nonlinear transmission of sound waves as they pass through a plane of tissue. Because sound propagates faster through compressed tissue, as compared with loose tissue, the transmitted wave becomes altered when traversing heterogeneous tissue, producing a series of low-amplitude harmonic echoes that are multiples of the original insonated frequency (41,44–47). By using a low-frequency transmission signal, tissue harmonic imaging can be used to separate the returning secondary harmonic signal from the insonated frequency; then these echoes can be used to generate an image, improving the imaging of structures at depth, which is especially important for deep structures and in the obese patient. The signal-to-noise ratio and contrast resolution are also enhanced because tissue harmonic imaging uses signals primarily generated from the center of the transmitted beam, eliminating artifacts caused by weaker nonharmonic signals such as sid
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