For centuries manual palpation of the tissue has served as an indispensable diagnostic tool in the medical practice. By touching and feeling the tissue stiffness using clinicians’ hands, it allows the detection and differentiation of the lesions or diseases accompanied by the changing mechanical properties. In the recent two decades, this ancient art of diagnostic tool derived a new life by incorporating the elastic assessment tool into the imaging system from 1990s.1–7 This new medical imaging modality, named elastography, maps the mechanical properties or elasticity of the tissue using ultrasonographic methods to analyze the tissue motion. In other word, it provides a noninvasive evaluation of the tissue stiffness in vivo based on the close relationship between the mechanical property and macro-structure of the soft tissue.4 Though a wide variety of parameters can reflect the mechanical properties of the tissue, such as Young's modulus, shear modulus, bulk compressional modulus, Poisson's ratio, viscosity, anisotrophy, and heterogeneity indices, and so on, a grossly simplified physical parameter, that is, Young's modulus is sufficient in most practical cases to characterize the biomechanical property of the soft tissue.4 The Young's modulus (E) or shear elastic modulus (μ) are described by the terms “elasticity,” “stiffness,” or “hardness,” which are the most corresponding to the manual palpation.4
With the rapid advancement of technology, the elastography has evolved from quasi-static elastography to dynamic elastography.7 The key differentiation of these two categories roots in the stimuli applied, namely mechanical or acoustic radiation force, and the response of the soft tissue.8 These two distinct types of elastography have many different concrete techniques on different commercially available ultrasound machines. Each of these techniques though works in a different way, they follow the same basic principle that is inducing a motion or a deformation in the tissue by an external or internal stress or force, observing how the tissue responses during the tissue motion and consequently inferring the mechanical property of the tissue.4,8
The quasi-static elastography is also called strain elastography, which is a pioneering technique of elastography. As its name indicated, this technique uses the strain value to reflect the mechanical property of the tissue, that is the deformation rate of the tissue when a constant external stress applied to it.9 The basic physics is based on Young's modulus through the Hooke's law: E = S/e, where the Young's modulus (E) equals to the stress applied to the object (S) divided by the generated strain (e) (Fig. 1).7,10 Under the same external force, a soft tissue will have a greater strain compared with hard tissue, so that a larger strain value indicates a soft tissue and vice versa.
To perform a strain elastography, the operator needs to manually compress and decompress the tissue regularly and cyclically using the transducer. The ultrasound machine can track the motion of the tissue across the time of stimuli to calculate the strain. This strain value is influenced by two factors: the external force and the distance to the source of the force exerted. First, greater force could generate a lager extent of deformation in the tissue and it is not easy to standardize the external force exerted by different operators. Some authors arbitrarily and subjectively defined the compression as 1 cm advancement of the transvaginal probe towards the cervix and each cycle of compression and decompression lasting for about 1 second.11 But despite all this, the reproducibility of the measurement was poor in the area directly receiving the compression and decompression.11,12 Second, the stress conducted to the tissue will decrease with the increasing distance, indicating that the area far away from the transducer will have a smaller deformation due to less stress received even for a homogenous stiff tissue, just like compressing a sponge.2 The strain elastography has been widely used in the tumor assessment, where the strain of the solid mass can be compared with the surrounding normal tissue with the equal depth to the transducer. However, this is not the case when evaluating the normal cervix, where no reference tissue can be used for comparison.11 In other word, the assessment by the strain elastography only reflects strain distribution among different areas of the cervix and thus cannot be used to quantify the cervical ripeness.11 To quantitatively measure the stiffness of the cervix by strain elastography, Hee et al. developed a synthetic reference material made of silicone and oil with known Young's moduli interpositioned between the cervix and the transvaginal transducer and this was applied to predict the cervical dilation time prior to the induction of labor.10,11
To standardize the external force, another technique of elastography adopts tissue Doppler imaging tool where a maximum compression of the anterior cervical lip is applied by means of transvaginal probe until no further decreasing of the anteroposterior diameter can be observed.13 But this technique has been criticized to be not only causing the cervical deformation, but also dislocation under such an amount of compression, as well as a merely reflection of maximum cervical deformability, rather than a real stiffness of the cervix.14 To avoid the major disadvantage of the strain elastography, that is the operator-dependency, techniques relying on the endogenous motion have been developed. In which, the tissue motion is generated by the patients’ breathing movement and inherent arterial pulsation.15,16 Ordinal scores are assigned to different areas according to the elastographic colored map, with lower score indicating stiff tissue and vice versa. Nevertheless, the quasi-static elastography still cannot measure the stiffness of the tissue in absolute values, but only a qualitative or semiquantitative assessment tool at most. Though oscillatory compression to the tissue is required, it is too slow so that it is still considered to be “quasi-static”.17
By contrast, only the quantitative assessment of the tissue elasticity needs the generation of shear waves, which requires the dynamic force. Instead of inducing the tissue movement by an external force, a special ultrasound beam induced acoustic radiation force, which is a time-varying force is used to disturb the tissue.18 The generated micro-scale movement is tracked dynamically, that is the propagation of the mechanical wave in the tissue, to deduce the elasticity of the tissue. The mechanical wave can travel in the tissue as a longitudinal compressional wave (parallel to the propagation) or a transverse shear wave (perpendicular to the propagation). Whereas the longitudinal wave is used for conventional ultrasound imaging, the shear wave propagation speed (Vs) is related to the shear modulus (μ) of the medium: μ = ρVs2, where ρ is the density of the tissue and assumed to be a constant as 1000 kg/m3.7 In the incompressible biological tissue, the Young's modulus is approximately three times the shear modulus (E≈3 μ), which thus can be quantitated by measuring the shear wave propagation speed (Fig. 2). The tissue stiffness measured by shear wave elastography (SWE )can be expressed as either shear wave propagation speed in m/s, or Young's modulus in kPa.9 Different manufactures have developed several techniques based on the dynamic elastography, including acoustic radiation force impulse (ARFI) imaging, transient elastography (TE), and SWE imaging.
(1) ARFI technique emits short-duration focused ultrasound beam into a small localized area at a certain depth in the tissue, and consequently causes tiny displacement (μm) of the targeted area along the axis of the ultrasound beam which can be tracked by the ultrasonic correlation-based algorithms.19 The targeted tissue stiffness is inversely proportional to the ARFI-induced displacement magnitude, so that the displacement across the time of stimuli of ARFI including the maximum displacement, the time to reach the maximum displacement and the relaxation time of the total recovery from the displacement are used to calculate the elasticity for the focal area.8,19,20
(2) TE, a variant of SWE, shear wave is generated by an external vibrator fixed on the transducer. Therefore, TE is also known as vibration-controlled elastography.21 The dynamic vibration at the surface of the tissue produces axial shear wave at the interface of the transducer and the tissue which travels along the ultrasound plane. The tissue motion is tracked using the cross-correlation method by tracing the ultrasound speckles in consecutive ultrasound raw data to reconstruct the shear wave propagation movie. Both one-dimensional TE and two-dimensional TE have been developed.4,7 In the one-dimensional TE, the vibration frequency is as low as 50 Hz, with the frame rate of the tracking ultrasound more than 1000 per second. By comparison, the two-dimensional TE extends to perform the ultrafast imaging by developing a programmable ultrasound electronic device and the raw data are acquired with a frame rate over 5000 per second. But the ultrafast ultrasound imaging electronic device is very heavy and bulky, preventing its general use in practice.22
(3) SWE, similar to the ARFI, imposes the acoustic radiation force to disturb the tissue. Unlike ARFI detecting the axial motion, SWE uses the induced shear wave which travels laterally from the focused ultrasound beam. The ARFI is comparable to a “virtual figure” that can palpate the tissue interiorly, which is potentially superior to the palpation of the body surface. (a) point SWE: a short duration of ARFI is emitted at a fixed depth, a point measurement of the shear wave speed at the localized region of interest can be made.19 It is also known as ARFI quantification, but no elastographic color map can be generated. (b) Two-dimensional SWE (2D SWE): multiple ARFI are emitted at different depths to generate stronger shear waves, where elastographic color map is applicable.10,17 The term “SWE” specifically refers to “2D SWE” in many literatures.17 Supersonic shear imaging (SSI) is one of the most sophisticated techniques of 2D SWE by the combination of two core techniques, the Mach cone (pushing mode) and ultrafast imaging (imaging mode). With the SSI, successive focused ultrasound beams are emitted at different depths in the tissue. Each focused ultrasound beam will generate a weak shear wave and the Mach cone is formed by coherently summing all the single shear waves. With the formation of Mach cone, SSI can amplify the shear waves amplitude as well as increase their propagation distance, while minimizing the acoustic output power. The nomenclature “Supersonic” is termed attributed to a super high speed of the ultrasound beam emission, even faster than the generation of the shear wave. This supersonic source efficiently improves the efficiency of shear wave generation by a factor 4 to 8 compare with a non-supersonic source for a fixed acoustic power at a given depth.23 Realizing the sufficient shear wave generation, another technical challenge of SSI is how to capture the generated shear waves, which will totally cross an average ultrasound image plane in 10 to 20 milliseconds. The general frame rate of the modern ultrasound equipment is only approximately 50 frames per seconds, and 1/50 of a second is too long to capture the propagating shear waves before they disappear. The ultrafast imaging is able to reach ultrafast frame rate of thousands of frames per second, allowing the capture of the fleeting shear wave propagation.23 The main differences between strain elastography and SWE are summarized in Table 1.
The unabated technical innovation grants the elastography remarkable breakthrough. The knowledge of the basic physics of the various type of elastography facilitates the effective use of elastography. Using SWE, the most advanced elastography, the quantitative measurements of the tissue stiffness can be acquired without operator-dependency. The clinical application of elastography and its diagnostic capability has also been extended.
With the evolution from strain elastography to SWE, the application is not only limited to the superficial organs, but extending to the deeper tissue. So far various organs have been assessed by elastography, including liver, prostate, thyroid, lymph nodes, skin, cervix, and musculoskeletal diseases. The elastography is designed to evaluate the tissue stiffness in vivo, which is determined by its constitution and structural arrangement of the macromolecules which is altered in many pathological conditions. Compared with magnetic resonance-based elastography, the ultrasound-based elastography is much easier to perform, more convenient, more widely available and much cost-effective.
Differentiation of benign and malignant lesions
The earliest and the mot comment use for elastography is to assist the differentiation of benign and malignant lesions. Many studies have shown improved sensitivity and specificity in detecting the breast malignant masses with strain elastography, compared to the conventional ultrasound imaging, even for those smaller than 1 cm lesions.24–28 Raza et al. demonstrated a sensitivity of 92.7% and a specificity of 85.8% for breast nodular lesion differentiation using strain elastography.29 With SWE, high mean stiffness value is associated with poorer prognostic features, such as advanced histologic grade, large infiltration size, tumor classification, lymph node metastasis and vascular invasion.30–32
A large number of studies have investigated the usefulness of elastography in discriminating thyroid tumors.33–37 A meta-analysis demonstrated that the strain elastography has a sensitivity of 92% and a specificity of 90% in the diagnosis of malignant thyroid nodules, which is comparable to the fine needle aspiration.38 But a very recent study demonstrated that thyroid imaging reporting and data system alone, based on a constellation of suspicious grey-scale ultrasound features, is superior to the strain elastography in the prediction of malignant thyroid nodules and the clinical relevance of the strain elastography is negligible.39 In the malignant thyroid nodules, the shear wave travels significantly faster than in either normal thyroid tissue or benign nodules.33,40 However, for the thyroid nodules with indeterminate cytology, SWE failed to differentiate between benign and malignant nodules.41 Several factors can influence the discriminative ability of elastography in thyroid tumors. The cystic nodules have more liquid tissue elasticity,42,43 making the strain elastography unsuitable for the evaluation. The undistinguishable nodules or the multinodular goiter cannot be evaluated by the strain elastography.44 Nodules of large size (>2 cm), cystic components and calcification, which is not uncommon in thyroid nodules, can also impact the performance of SWE.43,45 In addition, the close proximity of thyroid gland to the pulsatile carotid artery can cause a compression-decompression effect on thyroid, which can lead to inaccurate assessment of the elastography.46
The diagnostic ability of elastography in prostate cancer has also intrigued numerous researchers due to the low specificity of prostate-specific antigen and the low sensitivity of biopsy.47 Compared with grey-scale ultrasound, strain elastography can significantly improve the detection of organ-confined prostate cancer and extracapsular extension.48 Strain elastography is more sensitive in the detection of apical and middle prostate lesions, whereas magnetic resonance imaging is more sensitive in the transitional and basal parts of the prostate.49–51 Current studies reported sensitivities of 51%–75.4% and specificities of 72%–83.3% for the detection of prostate cancer by strain elastography.48,52,53 However, the interobserver variability of manual compression-decompression strength resulted in artifacts in around one-third of the cases.54 SWE can achieve a sensitivity of 96.2% and a specificity of 96.2% in detecting prostate cancer.55 Elastography guided prostate biopsy is a valuable tool which can significantly improve the detection of prostate cancer than systemic biopsy, while requiring fewer cores sample.56–58 It should be aware that benign pathologies, such as prostatitis, fibrosis, atrophy, benign prostate hypertrophy and adenomyomatosis may present an increased stiffness, which makes them difficult to distinguish from prostate cancer.59
Liver fibrosis and cirrhosis
As a noninvasive method for liver stiffness assessment, TE is the first to be used in the field and this technique is mainly developed by the manufacturer EchoSens, with the trademark name of FibroScan. Studies have shown FibroScan has excellent correlation with staging of liver fibrosis, and is a reliable tool for the detection of liver cirrhosis,21,60–64 but less accurate on the discrimination of mild fibrosis from moderate and severe cirrhosis.65–68 A review including over 1100 patients concluded the ARFI elastography is more reliable than TE.69 Recently, SWE, SSI to be specific, has been applied in the live fibrosis evaluation.70,71 The results revealed that SWE significantly improved the detection of significant fibrosis compared with TE,71 and was superior to the liver fibrosis indices.72 Moreover, SWE outperforms TE in terms of being able to guide the location of measurement due to its real time nature which allows visualizing the anatomical structure and stiffness information simultaneously.71
During the pregnancy, the cervix undergoes dynamic remodeling of the collagen fibrillar network and increased water content and glycosaminoglycans in the extracellular matrix, which leads to the softening and ripening of the cervix.73–79 This can be reflected by the change in cervical elastic properties, and SWE can quantitatively detect this softening process across the gestation (Fig. 3).80 Preterm birth still remains a big challenge in the obstetric practice and is accountable for three-quarters of the neonatal deaths.81 To identify high risk patients in advance is desirable and is still a main challenge. The microstructure reorganization may be a prelude to the shortening of the cervix.82 Previous studies have shown that greater strain in the internal os83,84 or the anterior cervix lip85 is associated with a higher risk of preterm delivery. But none of them can measure the cervical elasticity in absolute value. Agarwal et al. demonstrated that the shear wave velocity performs better than either elastography index derived by ARFI or Bishop score in the prediction of preterm birth, with a sensitivity of 93% and a specificity of 90%.86
Induction of labor
Cervical assessment is essential before the induction of labor and this is now performed by digital vaginal examination of Bishop score,87 which is notoriously known as subjective. As mentioned above, elastography is able to offer the information of the cervical elastic property which is indictive of cervical ripening, one of the elements in Bishop score. Several studies have used elastography to generate objective assessment of the cervical softness, and proved its usefulness in the prediction of successful induction of labor.13,15,79–90 However, all these studies adopted the strain based elastography, which is diminished by the lack of quantitative measurements of cervical elasticity.
With the increasing utilization of elastography in superficial organs, that is, breast and thyroid, researchers have employed this new tool in the evaluation of skin lesions.91 Recently, Botar et al. have demonstrated the combination of very-high-frequency ultrasound, power Doppler ultrasound, and real-time strain elastography offered comprehensive information for the preoperative evaluation of cutaneous melanoma.92,93 Dasgeb et al.,94 Magarelli et al.,95 and Nakajima et al.96 have concluded that elastography is a valuable tool to help differentiate between benign and malignant skin lesions. But the softness of the skin lesions alters with the lesion size, which is a factor impacting the differential accuracy of the elastography.96 Additionally, as a relatively new method in the evaluation of the skin lesions, more studies are needed to validate the efficiency of the elastography.97
Both strain elastography98 and SWE99 have been shown usefulness in determining the severity of various musculoskeletal disease as well as the follow-up of treatment, including tendons, muscles, nerves, and ligaments. Among these structures, Achilles tendon was the first and the most investigated area. With the strain elastography, the normal Achilles tendons appear to be either homogeneous with stiff structures or inhomogeneous with considerable soft tissues, which is not in accordance with the findings on conventional ultrasound.100–102 However, limited study showed that Achilles tendons are homogeneously hard by SWE.103 Further studies are warranted in view of the inconsistent observations. The advent of SWE has brought about exponential increase in the investigation of skeletal muscles due to the ability to display muscle stiffness in real time during the muscle relaxation and contraction.104 The change in muscle stiffness is a primary indicator for many condition, such as injury, aging, exercise-induced muscle damage, myopathy, muscle spasticity, and spastic cerebral palsy.105–111 Recently, the investigation of elastography has extended to the evaluation of plantar fasciitis,112 congenital muscular torticollis.113
Diagnostic ultrasound has been applied into the clinical use for more than five decades without harmful events reported.114 However, the ultrasound is not without risks and can cause biological effects — the thermal and mechanical effects to the tissue.115
The thermal effect, a rise in temperature of the tissue, is the result of the absorbtion and convertion of the ultrasound wave into the heat energy.116 To estimate the relative risk of the thermal bioeffect, the thermal index (TI) is calculated, which is a ratio between the acoustic power exposing the tissue and power required for 1°C increase anywhere in the beam.117,118 It provides users with a rough instructions in terms of the probable maximum temperature increase during ultrasound wave exposure in a particular imaging mode. Many factors could influence the risk of thermal effects. Different tissues have different absorption coefficients of the ultrasound beam. The fluid has the lowest absorption coefficient whereas the bone has the highest one; the soft tissue has an in-between coefficient.116 The TI should be kept as low as reasonably achievable (ALARA) especially when fetuses are scanned, because the fetuses are susceptible to the exposure to various physical stressors due to the developing embryonic and fetal tissues, particularly in the early trimester.119,120 Therefore, there is strict guidelines for the safe use of ultrasound in obstetrics to follow.114 The risk of thermal bioeffect is also dependent on the duration of exposure.114 The longer the exposure time, the greater the risk is.114 The recommended restrict time is 30 minutes for 1.0< TI (bone) ≤1.5.114 The TI increases from 0.0 to 0.9–1.1 after the SWE modality activated of the SE 12-3 transvaginal transducer. Though the TI of SWE is lower than the recommended criteria, it may not be appropriate or valid to be applied in the SWE, because the TI is a steady state estimates while the SWE is generated by the ultra-fast repetitive of short-duration focused acoustic pulses.115,118 So far no specific risk indicator unique to ARFI has been developed yet, but the duration of the SWE should be kept as less as possible to reduce the thermal stress to the targeted tissue.
The mechanical effect is mainly seen in tissues with stable gas bubbles such as lungs, intestines, and the use of contrast, as a result of radiation force, acoustic streaming, and cavitation effect.121 Cavitation is a resultant phenomenon of the pulsating motion of the gas bubble, caused by the alternating expansion and contraction of the bubble in a varying pressure of the ultrasonic energy field.122 Similar as the thermal effect, the mechanical index (MI) is used to assess the likelihood of cavitation. It describes the relationship between the peak acoustic pressure and the center frequency of the ultrasound beam.123 There is no absolute threshold of MI above which the cavitation will definitely occur, but a higher MI indicates a higher risk of the likelihood of the occurrence of cavitation hazard. The absence of gas in obstetrics makes the mechanical effect less relevant during the scan.121 The MI should be kept as low as possible when examining fetuses as the bioeffects in the form of radiation force, acoustic streaming which is not related to gas bubbles may also occur. The MI of the push pulse generated by SWE is less 1.9, the limit determined by Food and Drug Administration (FDA), and is consistent with that of color Doppler imaging.
So far, FDA has not yet approved the application of SWE in human fetuses due to the potential risk concerns of SWE to the developing fetuses and the lack of literature reporting an ascertaining risk in this field.124 The major safety concern is the high power of the acoustic push pulse. For the exposure of the fetuses to the routine ultrasound, FDA recommends a maximum spatial peak temporal average intensity of 720 mW/cm2 and maximum MI of 1.9.125 But these criteria may not be extrapolated to the SWE because they are time-averaged indices and do not capture orders of magnitude higher mechanical energy peaks concentrated within a few microseconds.126 The duration of the acoustic push pulse is 1 μs in routine color Doppler ultrasound settings, while the duration is 200 μs and 300 μs under the ARFI setting.127 Nevertheless, Herman et al found that the ARFI caused transient temperature rise might still be within the permitted safe ranges determined by the FDA.128 For current clinical implementations, the transducer heating during ARFI imaging is less than 1 °C and, therefore, ARFI imaging of soft tissue is safe if the TI is properly monitored.129 However, there is a debate with respect to whether the hyperthermal teratologic effects is simply determined by a threshold or linearity kinetics.128,130 In order to gain a more comprehensive understanding of the safety of ultrasound radiation force, future studies are warranted.
In spite of unavailable data of SWE in the human fetuses, reassuring results are derived from premature infants as well as animal experiments. Quarello et al. demonstrated the possibility and feasibility of using SWE in fetal baboons in exploring fetal organs, where SWE values were relevant to different organs.131 For the premature human neonates, Alison et al. applied SWE in those delivered between gestational 26–31 weeks due to intrauterine growth restriction and demonstrated that SWE measurement is feasible and reproducible.132 Su et al. quantitatively assessed the brain stiffness using ARFI and found significantly higher elasticity in full-term neonates compared with preterm neonates.133 Both studies did not report adverse outcomes regarding the use of SWE/ARFI in premature neonates. Li et al. further explored the immediate and long-term impacts of dynamic radiation force exposure (SWE) on neonatal mice's brain. The result revealed neither detectable histological changes, nor the long-term effect on the mice's learning and memory abilities, although the cellular signaling pathway was disturbed when the duration of SWE scanning exceeded 30 minutes.134 The cochlea and semicircular canals are delicate structures that may be very sensitive to the mechanical pulsatile vibration caused by SWE.135 A follow up for 4 years of a small cohort which underwent SWE cervical scan during the pregnancy indicated that no hypoacusis was attributed by prenatal SWE cervical examination.126
In short, the strain elastography and transient SWE by generated by the external vibrator have exactly the same risk considerations as the conventional ultrasound imaging.17 The radiation force based elastography (ARFI, SWE) though involves higher TI, it is still within limits set by American Institute of Ultrasound in Medicine and risk considerations are similar to the Doppler imaging mode.17,136–138
Conflicts of Interest
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