Accepted Manuscript Title: Basics, principles, techniques and modern methods in paediatric ultrasonography Author: Riccabona Michael PII: DOI: Reference:

S0720-048X(14)00234-4 http://dx.doi.org/doi:10.1016/j.ejrad.2014.04.032 EURR 6768

To appear in:

European Journal of Radiology

Received date: Revised date: Accepted date:

1-4-2014 25-4-2014 29-4-2014

Please cite this article as: Michael R, Basics, principles, techniques and modern methods in paediatric ultrasonography, European Journal of Radiology (2014), http://dx.doi.org/10.1016/j.ejrad.2014.04.032 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

*Title Page (including paper title & Complete corresponding auth

Basics, principles, techniques and modern methods in paediatric ultrasonography Riccabona Michael

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University Hospital Graz, Austria

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Department of Radiology, Division of Pediatric Radiology

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Correspondence address: Univ. Prof. Univ. Doz. OA Michael Riccabona, MD

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Department of Radiology, Division of Paediatric Radiology

Fax 0043 316 385 14299

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Tel 0043 316 385 14202

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University Hospital LKH Graz, Auenbruggenplatz 34, A – 8036 Graz, Austria

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Email: [email protected]

Disclosure:

The author is member of the Kretz European advisory board on 3DUS, and has ongoing cooperation with GE (and its subcompany Kretz), and Siemens Medical for development and clinical adaptations of paediatric US devices and transducers. Furthermore, a cooperation of our paediatric radiology division with Toshiba aims at improving paediatric CT applications with a particular focus on radiation protection and reduction.

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Abstract: Ultrasonography (US) is the mainstay of paediatric Radiology. This review aims at revisiting basic US principles, to list specific needs throughout childhood, and to discuss the

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application of new and modern US methods. The various sections elude to basic US physics, technical requisites and tips for handling, diagnostically valuable applications of modern

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techniques, and how to properly address hazards, risks and limitations. In conclusion, US

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holds vast potential throughout childhood in almost all body regions and many childhood specific queries - helping to reduce the need for or to optimise more invasive or irradiating

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imaging. Make the most of US and offerings a dedicated paediatric US service throughout

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the day, the week and the year thus is and will stay a major task of Paediatric Radiology.

1. Introduction

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Keywords: Paediatrics / childhood, Ultrasonography, Paediatric imaging, Neonates

When talking about ultrasonography (US) as a diagnostic imaging method in infants, neonates and children, a few basic considerations have to be revisited in order to properly

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understand the needs and to adequately apply the method in the various age groups and conditions. This is particularly important as technical development has enormously increased US potential, but still - which ever method is applied - the basic physics remain the same and the respective needs and phenomena have to be understood to make the most of these US capabilities. The following will briefly address basic physics, technical requisites, instrumentation and handling, limitations and artefacts as well as modern US methods applicable to paediatric US.

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2. Physics revisited It needs to be remembered that most of US relies on echoes emitted by transducer, then being reflected by various tissue interfaces of different density. The intensity of the echo

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received by the same transducer crystals is used to calculate the brightness of the specific

reflector, whereas the position and space is defined by the time sound needs to travel from

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emission to reception. This means that the US image on the screen is a calculated image

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and not a real photography which may lead to artefacts - intrinsically caused by the underlying assumptions and calculations. The received echoes can be displayed either in a

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linear graph displaying the altitude of the echo (A-Mode, the first method used - today practically not applied any longer) pr as a time-space relation using a graph describing

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motion of the targeted structure over time in a linear behaviour (M-Mode, still used in ophthalmology, echocardiography and some abdominal applications, such as assessment of

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ureteral peristalsis or diaphragmatic motion) (Fig. 1) (1). The most widely used display is the so-called brightness mode (B-Mode) which displays the brightness of the echoes throughout

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an entire section; fast image update in a real time fashion provides a film-like presentation of a cross-sectional view of the imaged region. This technique heavily relies on reasonable frame rates (= image updates), made possible by the high speed of the sound in tissue that allows to very quickly cover the targeted area and modern computer processing power.

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A range of phenomena occur during that travel of the US beam, which may interfere with image quality and phenomena. As resolution and penetration depend on the frequency applied, proper transducer selection needs to be based on the query-defined the area of interest and application – higher frequencies offer a higher resolution at less penetration which is ideally applicable to young children, infants and neonates, and to superficial structures, whereas lower frequencies are necessary for penetrating into deeper areas as needed for deep body compartments and older children as well as adolescence - at the cost of restricted resolution. This implies that for paediatric US a range of transducers usually is

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necessary, as one often has to cover all queries from head to toe in large age group – from preterm neonates of about 400 gram bodyweight to obese adolescents with up to 150 kilogram bodyweight. Image quality is influenced by a variety of other factors such as the focus zone or time gain

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compensation (TGC). These aspects are essential for proper images and have to be constantly instrumented and updated during the investigation. Modern equipment offer auto-

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optimization options, but these only partially address the necessary changes adequately and cannot replace the examiners skill and instrumentation. Common mistakes include using only

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the upper third of the monitor instead of having the organ of interest in a proper scale (“remember: you bought the entire monitor, so use the entire one”), inadequate TGC

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adaption, wrong focus position, inadequate frequency and transducer selection, and

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inadequate output- and receive-gain manipulation (Fig. 2).

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3. Technical requirements, child adapted environment, specific tips and tricks

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Most modern US equipments offer several pre-set options which are very helpful to easily and quickly adjust the device towards the scanned region; having additional age-adapted pre-sets for each transducer is particularly helpful. TCG adaptation and flexible (multi-)focus options are essential for many applications, also Doppler sonography options. A range of transducers is necessary to cover all areas throughout the entire childhood: A high frequency

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sector (vector) probe for neonatal brain US and echocardiography as well as some chest applications, high resolution (multi-)frequency linear transducers possibly supplemented by high frequency micro-curved array for the infants abdomen (also very useful for the brain, and essential for US of the small parts, joints, musculoskelettal system and bowel), and low (multi-)frequency curved array for the other abdominal applications. For echocardiography in older children and transcranial brain US, lower frequency sector transducers may become necessary as well as low frequency curved arrays for obese children. With modern transducers stand-off pads (which sometimes may be useful) are usually not necessary – Page 4 of 44

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this can be replaced by liberal use of US gel. Proper documentation has become standard mostly using digital formats with DICOM compatibility. In children cine-loop is particularly helpful – the export of video clips is increasingly recommended, and scrolling through such a clip will allow capturing the most appropriate image for diagnosis and documentation. This applies not only for high-end devices but also for average equipment, as newer approaches

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coming from point of care developments (that rely on even non-medical, briefly trained staff to acquire to the US sweep over a defined area or acquiring a standardized 3DUS-volume

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that then is send to the central reading office for diagnosis) is being introduced particularly for

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low resource areas with poor health facilities and restricted access of e.g., the rural population to basic medical services. But this also is being discussed as an option for more

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developed countries to reduce healthcare costs and supplement shortcomings from an increasing need for presently unavailable trained medical staff. Therefore sophisticated

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electronic export, communication and storing options are becoming indispensable. Due to the child’s restricted co-operability a different handling is necessary: you need enough

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space also for helping and accompanying persons (nurses, parents and relatives…) as well as swaddling facilities, heater, toys and games, books, warm tea and a pacifier (potentially

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supported by some drops of glucose). The US gel can be warmed; however, hygiene precautions have to be taken to avoid bacterial or fungal growth. It is helpful to first relate to the child - basically trying to explain the procedure before starting an US investigation. The transducer then is handled gently and – particularly in infants and small children – a constant

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connection with the child’s skin is usually welcomed as the procedure becomes more like a massage than an investigation, thus creating a cooperative patient and enabling a diagnostic examination. If positioning manoeuvers are necessary they should be performed slowly and gentle. Transducer movements also should be without any sudden change of position. If graded compression is used this should be applied gradually avoiding too much pressure in painful areas. If commands are used to improve US access, try to phrase them in a child’s wording, such as, instead of “hold your breath” it often works better to have the child imaging “a deep dive in the swimming pool”, or to ask to “show how big the belly can get after having

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visited your favourite restaurant”. Additionally, particularly in the abdomen, US access can be gained by replacing the air/gas within gastrointestinal structures with some fluid that will allow sound penetration as well as assessment of patency, distensibility and intraluminal structures. This can be achieved by feeding a bottle of tea, in neonates sometimes by installing the fluid via a gastric tube, or by a gentle enema using warm saline for the colon

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(Fig. 3) (2-6). Unconventional approaches such as a perineal access (to see structures of the lesser pelvis and the perineum, the urethra, the vagina etc.) are usually nicely tolerated and

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significantly enhance US diagnostic capabilities for certain conditions (e.g. urethral

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pathology, anal atresia, US genitography…) (Fig. 4) (7-9).

4. Modern techniques

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As in adults many modern techniques have become standard for routine imaging also throughout childhood. Harmonic imaging – relying on the second harmonic response of the

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emitted sound signal and not of the reflection of the basic frequency - improves resolution and reduces noise and artefacts; despite the slightly restricted penetration and the slightly

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higher output pressure this technique is very valuable throughout the body also in infants, neonates and children (10-14). Speckle reduction filtering algorithms significantly improve image quality usually without reducing frame rate, which will occur when compounding, multifocus and high persistence are applied (Fig. 5). These other techniques such as image

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(frequency or spatial) compounding and multi-focus imaging can be helpful in specific situations, but do not necessarily have to be applied for the routine scan, particularly as they increase the risk of motion induced blurriness and artefacts. However with skilful handling these, as well as for example also “extended field of view” or “panoramic imaging” can be successfully applied and useful in the individual case (Fig. 6) (9,14,15). Doppler techniques have become an essential tool for many queries and applications throughout childhood too (16-18). Doppler sonography relies on the frequency shift that occurs when the sound is reflected by a moving surface. Analysis of this frequency shift will Page 6 of 44

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allow calculation of flow direction and velocity using the Doppler equation - provided the angle between the incoming US beam and the movement/flow (mostly defined by the axis of vessel) can be defined. Remember that the cosine of the angle is part of this equation therefore any motion perpendicular to the sound direction is not depictable, as cosine of 90° is zero. The motion/flow information is then displayed either acoustically or by a graphic

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curve-like display after Fourier analyses of incoming signals for spectral analyses. With this technique a pre-defined sample area is assessed, depending on the Doppler frequency there

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is a varying upper velocity limit (Nyquist border) - velocities beyond that limit will “wrap

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around” and cause aliasing. Therefore, for assessment of very high velocity also in deeper body areas (i.e. repetition frequency higher than achievable by conventional Doppler

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sonography), continuous wave Doppler is available on some equipments, particularly when using the echocardiography set-up. Colour Doppler sonography (CDS) uses the same

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Doppler principles - only the flow direction as well as the mean velocity is displayed by a colour map overlaying the conventional B-Mode image. Note that these velocities usually are

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mean and not peak velocities and thus not useful for quantitative assessment. Furthermore, in CDS no angle correction is available. However – it has become an indispensable option in

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US diagnosis throughout childhood (Fig. 7a,b). Power Doppler sonography (amplitude coded colour Doppler sonography = aCDS) uses the integral from of the flow curve, thus is less angle depended and more sensitive to even low flow but lacks ability to display flow direction (19). This technique demonstrates more flow volume than flow velocity and thus is

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particularly valuable for looking at peripheral perfused vasculature and vascular architecture; however, due to its high sensibility it is more susceptible to motion (flash) artefacts even considering its lower internal signal noise which allows application of higher Doppler gains. Therefore skilful handling of all settings such as filter, scale, gate and persistence is indispensible for a diagnostic image quality; but in spite of these obstacles aCDS has become a very useful tool for certain applications, such as for depiction of renal peripheral perfusion defects (e.g., scares, focal renal involvement in urinary tract infection…) (Fig. 7c,d) (9,18,20-23). All these Doppler techniques use relatively high output gain with higher risk of

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US induced tissue damage and heating. This may be overcome by new non-Doppler depending motion-sensitive imaging techniques, such as “B-Flow” - an image subtraction technique that became feasible by the high temporal and spatial resolution of modern transducers, combined with fast processing rates and high computer speed. But this technique will also have other diagnostic features and should then not be confused with

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normal CDS; e.g., the twinkling artefact - a useful CDS phenomenon that is used for

detection of stones (though not only stones twinkle, and not all stones twinkle; Fig 8) (24,25)

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– will not be available with this technique.

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Contrast-enhanced US (ce-US) is becoming increasingly important also in children. Both the intracavitary application (e.g. contrast enhanced voiding uro-sonography = ce-VUS for

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assessment of vesico-ureteral reflux = VUR) as well as intravascular applications (usually addressed as CEUS) have been studied and found safe and useful in children, too (26-31).

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Combining ce-VUS with a perineal scanning approach allows visualisation of the urethra, too (Fig. 4c) (32). In spite of the lack of any approved US contrast agent for paediatric use the

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technique is becoming increasingly popular and holds vast potential to reduce the need for more invasive or irradiating imaging. Recommendations on how to perform these studies or

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on safety issues are available (30,31,33). Further details and applications will be covered in a dedicated article and therefore are not further addressed here, but numerous articles have shown its reliability (27,28,34-40). The same applies to US-elastography, a technique using non-linear sound propagation attributes for assessing the “stiffness” of a tissue, e.g., by

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measuring the velocity of a shear wave induced by a defined sound pressure wave. 3D- and 4DUS has become an essential part in foetal imaging. Though there are a variety of reports on its value and applicability in neonates and infants, it did not yet become part of routine scanning partially also because of time demands for post-processing and restricted availability (also of dedicated paediatric 3DUS transducers) on many systems. However, the option to create a volume data set that will allow for data manipulation with reconstructions of any desired plane, rendering options, surface viewing options and increased accuracy in

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volume calculations of particularly irregularly shaped structures holds vast potential that may become more important in the future with allowing a complete and superior documentation of the entire scanned structures, also allowing for reliable off-site interpretation and second opinion statements as well as good comparison to other sectional imaging such as CT or

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MRI (Fig. 9) (41-44).

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5. Hazards, risks and limitations

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Basic limitations of US also hold true for paediatric applications: Where ever sound cannot penetrate, no sonographic information can be achieved. This applies for bone and air/gas

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filled structures such as the aerated lung or the meteoristic bowel. However in both conditions the surface echo can be used diagnostically and certain phenomena such as

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shadowing behind calcifications, the twinkling artefact from crystals, reverberation artefacts from air, repetition artefacts from other strong echoic surfaces should not only been known,

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but can be useful for diagnoses and differential diagnoses. Other important artefacts are the through transmission enhancement behind fluid filled structures or the mirror artefact that

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occurs when the US beam hits a strong reflector (see Fig. 2, 5). Another limitation of US is the high intra-observer reliability. Due to varying transducer handling and different sonographic windows a standardized approach is difficult to find for all sections; however, by using reference structures some standardization can be achieved. This standard sections are

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well defined and should be the mainstay of any documentation – recommendations are outlined for most of the frequently scanned regions and systems (e.g. ÖGUM/DEGUM recommendations for documentation in paediatric brain, hip, uro-genital, and abdominal US – www.oegum.at). Finally a word concerning risks of US induced tissue damage: intrinsically the sound wave is a pressure wave that causes mechanical and thermal response in the tissue. Basically US can be a very powerful tool and can destroy tissues – this effect is used by ultrasonic lithotripsy or treatment of tendon calcifications etc. However, this effect is strictly correlated to Page 9 of 44

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the energy applied and to present state of knowledge has no “stochastic” component as one observes with radiation. Therefore, reducing the sound burden on the tissue by short insonation time with long “listening” periods and restricting the sound power (“output gain”) to save limits grant a negligible risk of US inducing damage. When the respective parameters are strictly observed no harmful biological effect of diagnostic US have been reported so far.

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The risk of sound induced damage is correlated to mechanical and thermal effects and is

displayed on modern equipment using the mechanical index (MI) and thermal index (TI), with

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different thermal indices for different tissues and areas (41,42). As a rule of thumb MI and TI

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values around one are considered safe. For a short time even higher, particularly TI values can be accepted - as necessary for e.g. trans-cranial Doppler. There are specifically

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vulnerable areas in children which have to be specifically addressed. These are the neonatal brain, the eye and orbit, the testis and all areas adjacent to strong reflectors – for

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investigations of these areas lower MI and TI limits are recommended (e.g., neonatal transfontanellar brain US < 0.7 / 1.0, US of the orbit < 0.4 ..) (43). And there is another US

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induced phenomenon that is called cavitation. It describes potential damage by US that occurs when air / gas (micro-) bubbles implode and create a secondary pressure wave when

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hit by a sound beam due to resonance phenomena. This phenomenon can be observed wherever gas bubbles are in the US field, and particularly is encountered with ce-US, as the US contrast agents are encapsulated and stabilized micro-bubbles. For all these applications very low MI-techniques (MI < 0,1-0,2) are recommended, not only to reduce the risk of sound

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induced damage but also to increase the duration of the contrast bubbles. And finally, some external limitations have also to be addressed such as the often insufficient remuneration of paediatric US that does not account for the more difficult scanning conditions with the longer scanning time often necessary in less cooperative children. And – intrinsically - the restricted availability of dedicated paediatric examiners with state of the art equipment throughout the day and throughout the week all over the year poses a significant limitation for a profound universal paediatric US service.

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6. Conclusion Ultrasound is the mainstay of imaging in paediatric radiology. It does not use radiation, is often completely non-invasive and most of the time can be performed without sedation. It is

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easily available also at the bedside or the emergency room / ward, can repeated without risking an increased (radiation, contrast agent) burden, and allows reliable and safe

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assessment of many paediatric conditions. To make utmost use of this fascinating imaging

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modality, the basic physical principle has to be understood, device handling and how to investigate infants and children has to be learned and trained, and a profound knowledge

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about paediatric conditions and the respective sonomorphologic appearance is essential - as well as adequate equipment and transducers. Applying modern methods US has advanced

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form an basic orienting technique to a reliable high-end imaging tool that in quite a few occasions offers not only superb information, but also ever better diagnostic yield than other

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modalities. Thus dedicated paediatric US should be made available to all children in need

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throughout the day, the week and the year

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Bosio M. Cystosonography with echocontrast: a new imaging modality to detect vesicoureteric reflux in children. Pediatr Radiol 1998; 28: 250-255

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Darge K, Tröger J, Duetting T et al. Reflux in young patients: Comparison of voiding US of the bladder and the retrovesical space with echoenhancment versus voiding cystourethrography for diagnosis. Radiology 1999; 210: 201–207

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Darge K, Zieger B, Rohrschneider W, Ghods S, Wunsch R, Troeger J. Contrast-enhanced harmonic imaging for the diagnosis of vesicoureteral reflux in pediatric patients. Am J Roentgenol 2001; 177: 1411-1415

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Duran C, del Riego J, Riera L, Martin C, Serrano C, Palaña P. Voiding urosonography including urethrosonography: high-quality examinations with an optimised procedure using a secondgeneration US contrast agent. Pediatr Radiol 2012; 42: 660-667

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Kenda RB, Novljan G, Kenig A, Hojker S, Fettich JJ. Echo-enhanced ultrasound voiding

Fritz GA, Riccabona M, Weitzer C, Deutschmann HA, Resch B. Three-dimensional ultrasound

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cystography in children: a new approach. Pediatr Nephrol 2000; 14: 297-300

(3DUS) of the neonatal brain: clinical application in patients of the neonatal intensive care

Riccabona M, Nelson TR, Resch B, Pretorius DP. Potential of three-dimensional ultrasound in

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unit. Ultraschall Med 2005; 26: 299-306.

neonatal and pediatric neurosonography: a pictorial essay. Eur Radiol 2003; 13: 2082-2093 Riccabona M, Fritz G, Ring E. Potential application of three-dimensional ultrasound in

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Riccabona M. Paediatric 3D-Ultrasound (3DUS) – an editorial review. Ultrason Poln 2014; 2 in press

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pediatric urinary tract: pictorial demonstration based on preliminary results. Eur Radiol 2003;

The British Medical Ultrasound Society. Guidelines for the safe use of diagnostic ultrasound equipment. 2009 http://www.bmus.org/policies-guides/BMUS-Safety-Guidelines-2009-

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revision-FINAL-Nov-2009.pdf

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American Institute of Ultrasound in Medicine (AIUM). Medical Ultrasound Safety. 2011. http://www.aium.org/soundWaves/article.aspx?aId=390&iId=20110915

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American Institute of Ultrasound in Medicine (AIUM) Statement. Bioeffects of Diagnostic Ultrasound with Gas Body Contrast Agents. 2008 http://www.aium.org/officialStatements/25

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ter Haar G. (ed) The safe use of Ultrasound in medical diagnosis, 3rd ed. The British Institute of Radiology 2012, ISBN 978-0-905749-78-5

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Miller DL, Averkiou MA, Brayman AA, et al. Bioeffects considerations for diagnostic ultrasound contrast agents. J Ultrasound Med 2008; 27:611–632 European Committee of Medical Ultrasound Safety (ECMUS). Clinical Safety Statement for

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O'Brien WD. Jr. Ultrasound - biophysics mechanisms. Prog Biophys Mol Biol 2007; 93: 212–

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Diagnostic Ultrasound. 2010 http://www.efsumb.org/ecmus/safety-statement2010.pdf

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Legend of Figures:

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Fig. 1 M-Mode:

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Documentation of peristalsis in megaureter (a), and lack of respiratory motion in a traumatic liver and diaphragmatic injury (b)

Fig. 2 Proper device handling

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a,b) TGC adaptation – TGC not adapted with too much through transmission and thus too bright image behind bladder (a), and proper TGC adaptation allowing to properly assess also retro-vesical space (b) c,d) Child’s kidney without (c) and with (d) speckle reduction filtering and compounding: note better parenchymal details and less artefacts (e.g. in gall bladder), but at the cost of a less crispy image

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Fig. 3 Filling techniques for improved visualisation and US-guided therapy Fluid in stomach for assessing HPSt (does tea pass pyloric channel?) (a), saline enema for conspicuous depiction of a colonic stenosis in a newborn after NEC (distending left colon allows depiction of non-distendable, steniotic segment with thickened wall at the left colon

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flexure) (b), and saline pressure enema for reducing intussusception (c)

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(arrow) is hardly visible.

Fig. 6 Extended field of view US in an enlarged spleen (26 cm in length!) The spleen is too big to be captured and measured (+ ... +) on a conventional image: coronal (a) and axial (b) section using panoramic imaging. The black sectors in (a) indicate data gaps.

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Fig. 7 (Amplitude-coded) Colour Doppler sonography [(a)CDS / Power Doppler] a) Post-traumatic arterio-venous aneurysm of the liver (a): CDS reveals the shunt by showing

arterial flow as well as the arterialised draining venous flow.

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aliasing in the affected vessels, and spectral analysis confirms the low resistance feeding

b) Persistent venous duct of Arrantii (b) – CDS depicts the vessel in a neonate; spectral

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DS shows “twinkling” (aliasing= bidirectional sparking colour signals)- in a neonatal kidney with some residual physiologic medullary / pre-papillary deposits (a), and intrahepatic sparkling directional colour signals (arrow) in an older infant due to aerobolia (b).

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Fig. 9 3DUS - Three orthogonal sections with a rendered view (right lower box) a) 3DUS of a neonatal eye: Nice demonstration of the intra-bulbar, septated multi-cystic tumour b) 3DUS of as hydronephrotic kidney in an infant due to UPJO with HN IV°: the segmented dilated collecting system is conspicuously demonstrated by the rendered view, this method

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can also be used for calculating renal parenchymal volume (by deducting of the dilated

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collecting system form the overall renal volume).

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Basics, principles, techniques and modern methods in paediatric ultrasonography.

Ultrasonography (US) is the mainstay of paediatric Radiology. This review aims at revisiting basic US principles, to list specific needs throughout ch...
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