Alonso A, Hennerici MG, Meairs S (eds): Translational Neurosonology. Front Neurol Neurosci. Basel, Karger, 2015, vol 36, pp 71–82 (DOI: 10.1159/000366238)
Parenchymal Imaging in Movement Disorders Rita de Cássia Leite Fernandes a · Daniela Berg b
a
Department of Neurology, University Hospital Clementino Fraga Filho, Federal University of Rio de Janeiro, 10º andar – Cidade Universitária, Rio de Janeiro, Brazil; b Department of Neurodegeneration at the UKT, Hertie Institut of Clinical Brain Research and German Center for Neurodegenerative Diseases, Tübingen, Germany
Abstract The use of B-mode sonography in neurological diagnosis was once considered of limited importance due to the barrier of the skull. However, modern ultrasound systems allow visualization of the brain parenchyma with a high degree of accuracy. Transcranial sonography (TCS) can offer unique information on brain tissue pathology, as it uses different physical principles for imaging acquisition than do other neuroimaging techniques. The method is harmless, is quick to perform at low cost and demands no sedation. The main limitations of this technique are dependence on the quality of the individual bone window and on proper operator training. A huge body of research has shown that patients with Parkinson’s disease (PD) display an enlarged hyperechogenic substantia nigra by TCS with a positive predictive value of 92.9%. Healthy individuals (8–15%) may show the same marker, in some cases correlating with decreased striatal dopamine uptake, motor slowing and prodromal markers of PD, indicating that this ultrasound sign may constitute a risk marker for PD. Other movement disorder diagnoses, although less extensively studied for TCS, may benefit from using this method as a supplementary diagnostic tool. This review provides a summary of the typical TCS findings and their value in the differential diagnosis of some movement disorders. © 2015 S. Karger AG, Basel
For more than five decades, the ultrasound technique has progressed towards being a well-established diagnostic method in general medicine. However, in the fields of neurology and neurosurgery, ultrasound has only relatively recently been introduced into clinical practice. This delay is likely due to the hindering of the passage of acoustic waves due to the osseous barrier of the skull bones. It was only in 1982 that Aaslid et al. [1] reported capturing Doppler signals from the middle and ante-
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Introduction
72
Fernandes · Berg Alonso A, Hennerici MG, Meairs S (eds): Translational Neurosonology. Front Neurol Neurosci. Basel, Karger, 2015, vol 36, pp 71–82 (DOI: 10.1159/000366238)
Downloaded by: Fudan University Library 61.129.42.15 - 5/12/2015 12:26:53 PM
rior cerebral arteries, as perceived via scanning through the temporal bone window with a 2-MHz pulsed Doppler. This discovery ushered in the era of non-invasive investigation of intracranial vascular disease. Studying the brain parenchyma using two-dimensional sonography had to wait until the last decade of the 20th century. In 1995, German investigators, led by Georg Becker [2], published the first report of an alteration at the mesencephalic substantia nigra (SN), which was depicted by B-mode sonography, in patients with Parkinson’s disease (PD). This group stated that the region at the anatomical site of the SN was much more echogenic in PD patients compared to individuals without PD and that this finding could be a useful neuroimaging marker for the disease. This astonishing finding was perceived with skepticism, as other structural neuroimaging methods, such as CT or MRI, were not capable of visualizing alterations typical of PD. However, scientific curiosity, the easy applicability of the method at low cost, the lack of side effects and the lack of discomfort during the investigation overcame this reluctance and piqued the interest of the scientific community. In the last 19 years, transcranial sonography (TCS) has thus been utilized in research, as well as in clinical routine in some centers, in the assessment of characteristic abnormalities of the substantia nigra, midbrain raphe, basal ganglia, and cerebral ventricles in various movement disorders [3]. TCS depicts echogenic, deep brain structures with high resolution [4] and has many important advantages. First, it is based on different physical principles than are other imaging techniques. Therefore, TCS can offer unique and complementary information on brain tissue pathology. Economically speaking, ultrasound equipment is much lower in cost than other imaging alternatives. The machines are generally widely available in health facilities where the same transducers are already used to perform transcranial Doppler. Moreover, bedside exams are a possibility, given that several types of ultrasound devices are relatively portable. Importantly, ultrasound only requires a short examination time and can be used in anxious patients. Because the investigator is able to compensate for the patient’s involuntary movements, there is also no need for sedation, and its inherent risks are low. Finally, the harmlessness of TCS allows for unlimited scans without the danger of radiation. Thus, ultrasound can be regarded as a convenient imaging technique that provides helpful supplementary information of the brain in healthy and diseased states. As with any imaging method, there are some limitations to ultrasound. The technique depends on the quality of the individual acoustic bone windows, and it provides poor access to brain regions near the insonating probe, basal skull bones and high frontoparietal regions. Ultrasound is also an operator-dependent technique, requiring proper training and experience for good data acquisition and interpretation [3]. For each of the following movement disorders, a comprehensive summary of the typical findings that have been acquired with TCS are described, and their values in diagnosis and differential diagnosis are provided.
Fig. 1. Standardized planes of transcranial sonography. OML = Orbitomeatal line; Line 1 = mesencephalic plane; Line 2 = basal ganglia plane.
Methods
Mesencephalic Brainstem Plane The examination starts in the axial scanning plane parallel to the so-called ‘orbitomeatal line’ to depict the key structures within this horizontal plane (fig. 2). At the center of the image, one finds the black (hypoechoic), butterfly-shaped mesencephalon contrasting with the surrounding white (hyperechoic) basal cisterns. By convention, the dorsal structures are displayed to the right, and the structures ipsilateral to the insonating probe are visualized at the superior part of the image. The nigral area is found in each cerebral peduncle and runs on an oblique, medio-lateral axis. Normally, the SN is depicted as
Parenchymal Imaging in Movement Disorders Alonso A, Hennerici MG, Meairs S (eds): Translational Neurosonology. Front Neurol Neurosci. Basel, Karger, 2015, vol 36, pp 71–82 (DOI: 10.1159/000366238)
73
Downloaded by: Fudan University Library 61.129.42.15 - 5/12/2015 12:26:53 PM
The exam is performed through the acoustic bone window in front of the ear (fig. 1). At this site, the temporal bone is thinner, allowing sound waves of low frequency to penetrate and reach the deep structures of the brain. In about 80–90% of the Caucasian population, the optimal quality of the bone window allows good visualization of all structures of interest when all age groups are considered. A higher prevalence of poor windows has been reported in elderly patients, women, and individuals of Asian descent [3, 5]. An optimized ultrasound system equipped with a low frequency (1–3 MHz), phased-array transducer should be used. A penetration depth of 14–16 cm allows for visualization of the contralateral skull bone when the focus is set in the middle of the image. The dynamic range should be set at 45–55 dB, with medium or high-contour amplification. Image brightness and time-gain compensation are individually adapted during each scan as needed. Tissue harmonic imaging allows for a more distinct depiction of tissue interfaces and may be used to improve resolution, but its dependency on the bone window prevents its more generalized use. Moreover, the size of structures seems exaggerated using tissue harmonic imaging [6]. The patient is placed in the supine position, and the investigator approaches both temporal windows from behind the head. The two scanning planes that are routinely used for the evaluation of relevant brain structures in movement disorders are the mesencephalic plane and the basal ganglia plane. Eventually, a cerebellar plane may also be used.
Aqueduct
Raphe
a
b
c
d
a thin, echogenic, sometimes rather patchy line. The echogenicity of the SN used to be graded semiquantitatively as isoechogenic, mildly echogenic, and hyperechogenic with regard to the surrounding mesencephalon. In contrast to this subjective evaluation, the planimetrically measured area of nigral echogenicity has been used more often because it allows for better comparison across observers and studies, thus enhancing the reproducibility of the method [5, 6]. After freezing and zooming, the SN echogenic area is manually encircled on the ipsilateral peduncle for the planimetrically area measurement. SN areas
Parenchymal Imaging in Movement Disorders Rita de Cássia Leite Fernandes a · Daniela Berg b
a
Department of Neurology, University Hospital Clementino Fraga Filho, Federal University of Rio de Janeiro, 10º andar – Cidade Universitária, Rio de Janeiro, Brazil; b Department of Neurodegeneration at the UKT, Hertie Institut of Clinical Brain Research and German Center for Neurodegenerative Diseases, Tübingen, Germany
Abstract The use of B-mode sonography in neurological diagnosis was once considered of limited importance due to the barrier of the skull. However, modern ultrasound systems allow visualization of the brain parenchyma with a high degree of accuracy. Transcranial sonography (TCS) can offer unique information on brain tissue pathology, as it uses different physical principles for imaging acquisition than do other neuroimaging techniques. The method is harmless, is quick to perform at low cost and demands no sedation. The main limitations of this technique are dependence on the quality of the individual bone window and on proper operator training. A huge body of research has shown that patients with Parkinson’s disease (PD) display an enlarged hyperechogenic substantia nigra by TCS with a positive predictive value of 92.9%. Healthy individuals (8–15%) may show the same marker, in some cases correlating with decreased striatal dopamine uptake, motor slowing and prodromal markers of PD, indicating that this ultrasound sign may constitute a risk marker for PD. Other movement disorder diagnoses, although less extensively studied for TCS, may benefit from using this method as a supplementary diagnostic tool. This review provides a summary of the typical TCS findings and their value in the differential diagnosis of some movement disorders. © 2015 S. Karger AG, Basel
For more than five decades, the ultrasound technique has progressed towards being a well-established diagnostic method in general medicine. However, in the fields of neurology and neurosurgery, ultrasound has only relatively recently been introduced into clinical practice. This delay is likely due to the hindering of the passage of acoustic waves due to the osseous barrier of the skull bones. It was only in 1982 that Aaslid et al. [1] reported capturing Doppler signals from the middle and ante-
Downloaded by: Fudan University Library 61.129.42.15 - 5/12/2015 12:26:53 PM
Introduction
72
Fernandes · Berg Alonso A, Hennerici MG, Meairs S (eds): Translational Neurosonology. Front Neurol Neurosci. Basel, Karger, 2015, vol 36, pp 71–82 (DOI: 10.1159/000366238)
Downloaded by: Fudan University Library 61.129.42.15 - 5/12/2015 12:26:53 PM
rior cerebral arteries, as perceived via scanning through the temporal bone window with a 2-MHz pulsed Doppler. This discovery ushered in the era of non-invasive investigation of intracranial vascular disease. Studying the brain parenchyma using two-dimensional sonography had to wait until the last decade of the 20th century. In 1995, German investigators, led by Georg Becker [2], published the first report of an alteration at the mesencephalic substantia nigra (SN), which was depicted by B-mode sonography, in patients with Parkinson’s disease (PD). This group stated that the region at the anatomical site of the SN was much more echogenic in PD patients compared to individuals without PD and that this finding could be a useful neuroimaging marker for the disease. This astonishing finding was perceived with skepticism, as other structural neuroimaging methods, such as CT or MRI, were not capable of visualizing alterations typical of PD. However, scientific curiosity, the easy applicability of the method at low cost, the lack of side effects and the lack of discomfort during the investigation overcame this reluctance and piqued the interest of the scientific community. In the last 19 years, transcranial sonography (TCS) has thus been utilized in research, as well as in clinical routine in some centers, in the assessment of characteristic abnormalities of the substantia nigra, midbrain raphe, basal ganglia, and cerebral ventricles in various movement disorders [3]. TCS depicts echogenic, deep brain structures with high resolution [4] and has many important advantages. First, it is based on different physical principles than are other imaging techniques. Therefore, TCS can offer unique and complementary information on brain tissue pathology. Economically speaking, ultrasound equipment is much lower in cost than other imaging alternatives. The machines are generally widely available in health facilities where the same transducers are already used to perform transcranial Doppler. Moreover, bedside exams are a possibility, given that several types of ultrasound devices are relatively portable. Importantly, ultrasound only requires a short examination time and can be used in anxious patients. Because the investigator is able to compensate for the patient’s involuntary movements, there is also no need for sedation, and its inherent risks are low. Finally, the harmlessness of TCS allows for unlimited scans without the danger of radiation. Thus, ultrasound can be regarded as a convenient imaging technique that provides helpful supplementary information of the brain in healthy and diseased states. As with any imaging method, there are some limitations to ultrasound. The technique depends on the quality of the individual acoustic bone windows, and it provides poor access to brain regions near the insonating probe, basal skull bones and high frontoparietal regions. Ultrasound is also an operator-dependent technique, requiring proper training and experience for good data acquisition and interpretation [3]. For each of the following movement disorders, a comprehensive summary of the typical findings that have been acquired with TCS are described, and their values in diagnosis and differential diagnosis are provided.
Fig. 1. Standardized planes of transcranial sonography. OML = Orbitomeatal line; Line 1 = mesencephalic plane; Line 2 = basal ganglia plane.
Methods
Mesencephalic Brainstem Plane The examination starts in the axial scanning plane parallel to the so-called ‘orbitomeatal line’ to depict the key structures within this horizontal plane (fig. 2). At the center of the image, one finds the black (hypoechoic), butterfly-shaped mesencephalon contrasting with the surrounding white (hyperechoic) basal cisterns. By convention, the dorsal structures are displayed to the right, and the structures ipsilateral to the insonating probe are visualized at the superior part of the image. The nigral area is found in each cerebral peduncle and runs on an oblique, medio-lateral axis. Normally, the SN is depicted as
Parenchymal Imaging in Movement Disorders Alonso A, Hennerici MG, Meairs S (eds): Translational Neurosonology. Front Neurol Neurosci. Basel, Karger, 2015, vol 36, pp 71–82 (DOI: 10.1159/000366238)
73
Downloaded by: Fudan University Library 61.129.42.15 - 5/12/2015 12:26:53 PM
The exam is performed through the acoustic bone window in front of the ear (fig. 1). At this site, the temporal bone is thinner, allowing sound waves of low frequency to penetrate and reach the deep structures of the brain. In about 80–90% of the Caucasian population, the optimal quality of the bone window allows good visualization of all structures of interest when all age groups are considered. A higher prevalence of poor windows has been reported in elderly patients, women, and individuals of Asian descent [3, 5]. An optimized ultrasound system equipped with a low frequency (1–3 MHz), phased-array transducer should be used. A penetration depth of 14–16 cm allows for visualization of the contralateral skull bone when the focus is set in the middle of the image. The dynamic range should be set at 45–55 dB, with medium or high-contour amplification. Image brightness and time-gain compensation are individually adapted during each scan as needed. Tissue harmonic imaging allows for a more distinct depiction of tissue interfaces and may be used to improve resolution, but its dependency on the bone window prevents its more generalized use. Moreover, the size of structures seems exaggerated using tissue harmonic imaging [6]. The patient is placed in the supine position, and the investigator approaches both temporal windows from behind the head. The two scanning planes that are routinely used for the evaluation of relevant brain structures in movement disorders are the mesencephalic plane and the basal ganglia plane. Eventually, a cerebellar plane may also be used.
Aqueduct
Raphe
a
b
c
d
a thin, echogenic, sometimes rather patchy line. The echogenicity of the SN used to be graded semiquantitatively as isoechogenic, mildly echogenic, and hyperechogenic with regard to the surrounding mesencephalon. In contrast to this subjective evaluation, the planimetrically measured area of nigral echogenicity has been used more often because it allows for better comparison across observers and studies, thus enhancing the reproducibility of the method [5, 6]. After freezing and zooming, the SN echogenic area is manually encircled on the ipsilateral peduncle for the planimetrically area measurement. SN areas
