3D for Early Detection of Lesions. Evaluation on a Pressure Ulcer Mimicking Phantom. Jean-François Deprez, Guy Cloutier, Cedric Schmitt, Claudine Gehin, André Dittmar, Olivier Basset, Elisabeth Brusseau

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Jean-François Deprez, Guy Cloutier, Cedric Schmitt, Claudine Gehin, André Dittmar, et al.. 3D Ultrasound Elastography for Early Detection of Lesions. Evaluation on a Pressure Ulcer Mim- icking Phantom.. Conference proceedings : .. Annual International Conference of the IEEE En- gineering in Medicine and Biology Society. IEEE Engineering in Medicine and Biology Society. Annual Conference, Institute of Electrical and Electronics Engineers (IEEE), 2007, 1, pp.79-82. ￿10.1109/IEMBS.2007.4352227￿. ￿inserm-00192829￿

HAL Id: inserm-00192829 https://www.hal.inserm.fr/inserm-00192829 Submitted on 29 Nov 2007

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Conf Proc IEEE Eng Med Biol Soc 2007;1:79-82 3D Ultrasound Elastography for Early Detection of Lesions. Evaluation on a Pressure Ulcer Mimicking Phantom.

Jean-François Deprez, Guy Cloutier, Cédric Schmitt,

HAL author manuscript inserm-00192829, version 1 Claudine Gehin, André Dittmar, Olivier Basset and Elisabeth Brusseau

Abstract— A pressure ulcer is a damaged tissue area induced of bedsores affect these two locations. by an unrelieved pressure compressing the tissue during a Above a threshold, compression results in local occlusions prolonged period of immobility. The lack of information and of blood capillaries. This shortage of blood supply, called studies on the development of this pathology makes its ischemia, prevents the natural exchanges of oxygen and prevention difficult. However, it is both acknowledged that nutrients between the blood and body cells to occur. These lesions initiate in the deep muscular tissues before they expand to the skin, and that lesions are harder than healthy tissues. ischemic conditions may lead to cell death and severe tissue Elastography is therefore an interesting tool for an early damages. Besides, skin and muscle have different detection of the pathology. A 3D strain estimation algorithm is metabolisms: skin metabolism is anaerobic, while muscle presented and evaluated on a PVA-cryogel phantom, has an aerobic metabolism, requiring much more oxygen [1]. mimicking a pressure ulcer at an early stage. Muscles are therefore more vulnerable to ischemia than the skin and surrounding fat tissues. Thus, lesions first initiate in I. INTRODUCTION the deep muscle tissue before expanding to the skin, making ressure ulcers, also known as bedsores, are lesions of the difficult their early detection. This explains why the sore is P skin and underlying tissues, caused by a high and already at a severe stage when it appears on the skin surface. prolonged pressure at the body interface. This pathology In the literature, few studies are available on pressure concerns any people with weakened sensitivity or limited ulcer mechanical properties. The main reference in this area mobility. But it mostly strikes elders and spinal cord injury is given by Gefen et al. [2], who showed that tissues patients. This disease is painful, handicapping and becomes damaged by pressure ulcer are harder than healthy tissues. a growing issue, as life expectancy increases in western By applying a prolonged compression on rat muscle tissues countries. Yet, it has been neglected till now, and there is in vivo, they observed a significant increase of tissue elastic still little consensus about the pathological process that modulus with time and pressure level. triggers the formation of bedsores. Because of this process of hardening of damaged areas It is now acknowledged that pressure ulcers appear after a and the deep origin of the ulcer, ultrasound elastography prolonged period of immobility, during which the body seems especially appropriate for the early detection of interface lying on a support (either a bed or a wheelchair) pressure ulcer formation. undergoes a high and unrelieved pressure. During a short Elastography is a promising technique, which aim is to time, biological soft tissues can tolerate relatively high provide information about the mechanical properties of soft pressures. However, a weaker but continuous pressure can biological tissues, by investigating their deformation under result in severe injuries and a pressure ulcer can therefore an external load. Pre- and post-compression ultrasonic (US) appear anywhere in the body as soon as it is subjected to a radio-frequency (RF) signals are first acquired. Then, significant pressure. Nevertheless, thin layered tissues in changes within the signals induced by the stress are analyzed regard to a bony prominence are privileged regions, as a to compute a map of local strains. high stress is focused on a small volume. This pattern is met Since static elastography has appeared in the early 90s [3], for sacrum or heels. These are privileged regions and 80 % mainly 1D methods were developed. A few 2D methods have also been worked out [4]-[10]. These techniques are

Manuscript received April 2, 2007. This work was supported in part by a adapted to current clinical equipment since ultrasound grant of the Region Rhône-Alpes, France. scanners essentially provides 2D data. However they may J.F. Deprez, O. Basset and E. Brusseau are with the laboratory lead to noisy elastograms if significant out-of plane motion CREATIS (Application & Research Center for Image and Signal occurs, since it represents a source of decorrelation between Processing), INSA-Lyon, Université de Lyon, CNRS UMR 5220 & INSERM U630 (corresponding author mail: 7 avenue Jean Capelle, pre- and post-compression signals. To overcome this Villeurbanne, 69621 France; phone: 33 4 72 43 62 54; fax: 33 4 72 43 85 decorrelation problem, and with the development of 2D 26; e-mail: [email protected] ). transducer arrays, we use in this study a 3D estimator, which G. Cloutier and C. Schmitt are with the Laboratory of Biorheology and Medical Ultrasonics of the University of Montreal Hospital, Canada (e- computes the axial strain while considering lateral and mail: [email protected] , [email protected] ). azimuthal motions. This strain estimation model is further C. Gehin and A. Dittmar are with the Biomedical Microsensors Department of Institut des Nanotechnologies de Lyon of INSA (National Institute of Applied Sciences), France (e-mail: [email protected] and [email protected] ).

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scatterers due to the compression and enables to work on US probe corresponding tissue regions, and therefore equivalent US y (lateral) data in both volumes. To cover the whole US volume V1, the l) ha Healthy ut pre-compression region of study R1 is regularly moved by im tissues az constant steps of ∆ , ∆ , and ∆ in the axial, lateral and ( (1 cycle) ax lat azim z azimuthal directions, respectively. An adaptive displacement x (axial) Ulcer is considered for R2: its axial displacement results from the

HAL author manuscript inserm-00192829, version 1 (2 cycles) accumulation of axial deformations of the regions located Bone between the probe and the region of interest, and the lateral

m and azimuthal displacements are directly linked to those 30 mm 30 m 0 1 1 estimated over adjacent regions. uR1 and uR2, the positions of 60 mm R1 in V1 and R2 in V2, respectively, are then given by: G G G Fig. 1. Phantom scheme. = ∆ + ∆ + ∆ uR (m,n,q) m. ax .i n. lat . j q. azim .k 1 (1) m −1 G n−1 G q −1 G u (m,n,q) = ( 1 ).∆ .i + τ . j + ν .k detailed in the following section. Pressure ulcer early R 2 ∑ α ax ∑ k ∑ k k detection is then investigated with the proposed method. k =0 k =0 k =0 where α is the axial scaling factor at u (m,n,q), τ k R1 k the lateral displacement and vk the azimuthal displacement, estimated on step k. The axial time-delay (parameter d) is II. METHOD directly linked to the axial coordinate of uR2. Hence, with The proposed 3D strain estimator is based on an adaptive such an initialization for the location of R2 in V2, the and iterative constrained optimization process. For each parameter d is already determined, and the three parameters elementary RF region R1 selected in the pre-compression α, τ and ν remain to be estimated, the two latter being of volume V1, its deformed version R2 is searched in the post- small magnitude. compression volume V2 and the corresponding local strain is then estimated. In the axial direction (see directions in fig. 1), R2 is considered as a time-delayed (parameter d) and B. Joint estimation of the parameters α, τ and ν scaled (parameter α) replica of R1. Because lateral and A joint estimation of the parameters α, τ and ν is then azimuthal resolutions are much coarser than the axial performed. The region of interest R2 is searched within V2, as resolution, R2 is only considered to be a shifted version of R1 an axially scaled, laterally and azimuthally shifted replica of in these directions (parameters τ and ν). The axial delay d R1, noted R2(αx,y+τ,z+ν).This is done thanks to the results from the accumulation of axial deformations of the minimization of the objective function f, which computes the regions located between the probe and the region of interest. opposite of the normalized correlation coefficient between After having compensated for this axial delay, three R1 and R2, when R2 is compensated for the three searched parameters remain to be calculated: the axial scaling factor parameters: α, the lateral shift τ and the azimuthal shift ν. They are [αˆ,τˆ,νˆ] = arg min f (α,τ ,ν ) , (2) estimated as the arguments that minimize an objective α ,τ ,ν function f, defined as the opposite of the correlation with: α τ ν = coefficient between R1 and its deformed version R2 f ( , , ) compensated for the three parameters. Since this objective − ~ ~ α + τ + ν R1(x, y,z).R 2 ( x, y ,z ) (3) function f may suffer from multiple local minima, and could ∑ x,y ,z , therefore yield to incorrect estimations, strong constraints ~ 2 ~ α + τ + ν 2 ∑ (R1(x, y,z)) . ∑ (R 2 ( x, y ,z )) are introduced on the different arguments. An admissible set x,y ,z x,y ,z of values is thus defined. where ~ = − (4) A three step process is applied to compute the strains. R i (x, y,z) R i (x, y,z) R i (x, y,z) . First, an adaptive windowing of the region of study is used, R i (x,y,z) is the mean value of the region Ri. In followed by the joint estimation of the three parameters α, τ elastography, deformations are of small magnitude (a few and ν. The strain map is finally computed. %). The optimization is therefore submitted to a set of linear inequalities constraints, drastically limiting the occurrence of A. Adaptive windowing of the region of study local minima: α ≤ α ≤ α τ ≤ τ ≤ τ ν ≤ ν ≤ ν (5) The axial tissue compression yields also to lateral and out- min max , min max , min max . of-plane motion in the region of interest, resulting in a Reducing the parameter domain also saves calculation time. transformation of the acoustical footprint of the pre- The algorithm is implemented as a descent method, compression signal. To overcome the subsequent loss of following the scheme: correlation, an adaptive displacement of the 3D region of ()()α τ ν = α τ ν + ρ (6) k +1 k +1 k +1 k k k k .Sk study is considered. It allows tracking the motion of the

where ρk is the descent step computed by a linear search, and Sk is the descent direction. 3 The first iteration is chosen as the middle of the admissible set K={(α,τ,ν) | αmin ≤ α ≤ αmax, τmin ≤ τ ≤ τmax, νmin 2 ≤ ν ≤ νmax}, and a sequence of admissible iterations is then generated, until a stop criteria is met. 1

HAL author manuscript inserm-00192829, version 1 C. Strain computation (a) Strain maps are then computed thanks to the set of 0.4 parameters calculated for the whole US volume. We focus here on the axial strain, which is directly linked to the 0.2 estimated parameter αk according to the relation: 0 ε = 1 − (7) ˆax ,k α 1 . ˆk -0.2 -0.4 (b) III. EXPERIMENTAL RESULTS A polyvinyl alcohol (PVA) cryogel phantom was 0.18 designed to mimic a pressure ulcer at an early stage. Since 0.14 PVA cryogel is a material whose acoustical properties are very close to those of soft biological tissues, it can easily be 0.1 imaged with an ultrasound device. Moreover its stiffness 0.06 increases with the number of freeze-thaw cycles applied. 0.02 This typically allows encompassing the range of elasticity (c) values commonly met in soft biological tissues [11]. As previously mentioned, pressure ulcers are found on sites where thin layered tissues are in regard to a bony 0.8 prominence. Therefore, the phantom is designed as a 0.6 parallelepiped of dimensions 30 mm x 60 mm x 110 mm, with three distinct areas: a bone, a region mimicking the 0.4 pressure ulcer at an early stage and healthy tissues 0.2 surrounding it. The geometry is further detailed in figure 1. The bone, taken from the forward limb of a dog, measured (d) 10 mm in diameter. The pathological area underwent 2 freeze-thaw cycles, which is one more than the healthy region. This led to a harder material for the pressure ulcer mimicking area [12]. Acquisitions of RF US data were performed with an Ultrasonix - Sonix RP device. The probe and sampling frequencies were 7 MHz and 40 MHz, respectively. Each image was composed of 128 RF A-lines, with a line interdistance of 0.29 mm. A linear stepper motor was used to (e)

move the probe azimuthally and to acquire regularly spaced Fig. 2. Results for a volume centered on the middle of the phantom. 2D scans (by steps of 0.2 mm). A first set of scans was (a) is the axial strain (%). (b) is the lateral displacement (mm). (c) is the azimuthal displacement (mm). (d) is the correlation coefficient performed with the phantom in a pre-compression state. The map. (e) is a B-mode image. corresponding RF data volume was built by stacking the images. Then a flat plate was used to uniformly compress the phantom and achieve a global axial deformation of 2%, slides, and the overlap was 80 %, both axially and laterally and the same protocol was once again applied to compute (no azimuthal overlap). The results for an area centered on the post-compression volume. the middle of the phantom are presented in fig. 2. A B-mode The ability of our algorithm to detect the pathological area image of the region is shown in fig. 2e. Even if the bone is was evaluated on these data. The size of the region of visible because of its echogenicity, the echography does not exhibit any mechanical information. On the contrary, the interest R1 was 60 axial points x 3 RF lines x 3 azimuthal axial strain map (fig. 2a) is of great help for distinction between the lesion, the healthy tissues and the bone. Due to

differentiated, since the deformation of healthy tissues is Healthy tissues approximately twice the deformation of the diseased region. 4

area area 3

Pathol. IV. CONCLUSION 2 A 3D strain estimator has been described in this paper. Bone Thanks to an optimized adaptive and iterative process, it HAL author manuscript inserm-00192829, version 1 1 enables accurate estimations of the axial strain distribution, (a) while considering lateral and azimuthal motion. The strain Healthy 2 estimation technique was evaluated on a PVA-cryogel tissues phantom mimicking a pressure ulcer at an early stage. Results are very encouraging, both for the potential of our 1 3D elastographic method, and for the possibility of detecting this pathology at an early stage. Complementary tests on in area area vitro and in vivo biological tissues are now planed. Pathological (b) 0

Fig. 3. Axial strain along the z axis, for a slice centered on the middle REFERENCES of the phantom (a), and for an off-centered slice (b). [1] G.T. Nola and L.M. Vistnes, “Differential response of skin and muscle in the experimental production of pressure sores,” Plast. Reconstr. Surg., vol. 66, pp. 728-733, Nov. 1980. the low compression level, strain values remain within a [2] A. Gefen, N. Gefen, E. Linder-Ganz and S.S. Margulies, “In vivo small range. However, the deformation of the bone is almost muscle stiffening under bone compression promotes deep pressure sores”, Trans. of the ASME, vol. 127, pp. 512-524, June 2005. zero, while the mean axial strain of the pathological area is [3] J. Ophir, I. Céspedes, H. Ponnekanti, Y. Yazdi and X. Li, about half that of surrounding tissues (0.75% vs. 1.5%). “Elastography: a quantitative method for imaging the elasticity of Moreover, the boundary between the healthy region and the biological tissues”, Ultrasonic Imaging, vol.13, pp. 111-134, Apr. 1991. ulcer is recognizable, which could allow a diagnostic about [4] M. O'Donnell, A.R. Skovoroda, B.M. Shapo and S.Y. Emelianov, the stage of the illness. The lateral displacement map (fig. “Internal displacement and strain imaging using ultrasonic speckle 2b) displays this limit too, especially in the top corners of tracking”, IEEE Trans. Ultrasonics, Ferro. and Freq. Control, Vol. the image. Azimuthal displacement estimations are shown 41, no. 3, pp. 314-324, May 1994. [5] P. Chaturvedi, M.F. Insana and T.J. Hall, “2D Companding for noise fig. 2c. Surprisingly, there are large displacements for tissues reduction in strain imaging”, IEEE Trans. Ultrasonics, Ferro. and immediately surrounding the bone. This might be due to Freq. Control, vol. 45, no. 1, pp. 179-191, Jan. 1998. slippery conditions at the bone/cryogel interface and to a [6] E. Konofagou and J. Ophir, “A new elastographic method for estimation and imaging of lateral displacements, lateral strains, weak link between them when the phantom was built. corrected axial strains and Poisson's ratio in tissues”, Ultrasound in Because of the poor resolution in the azimuthal direction, Medicine and Biology, Vol. 24, pp. 1183-1199, Oct. 1998. this map is also noisy. But it especially demonstrates the [7] X. Chen, M. J. Zohdy, S. Y. Emilianov and M. O'Donnell, “Lateral Speckle Tracking Using Synthetic Lateral Phase”, IEEE Trans. interest of considering the 3D motion of soft tissues. The Ultrasonics, Ferro. and Freq. Control, vol. 51, no. 5, pp. 540-550, objective function of our algorithm is based on the May 2004. normalized correlation coefficient, that’s why it is also [8] R. L. Maurice, J. Ohayon, Y. Frétigny, M. Bertrand, G. Soulez and G. Cloutier, “Non-invasive vascular elastography: Theoretical interesting to consider the correlation coefficient map (fig. framework”, IEEE Trans. , Vol. 23, No 2, pp. 164- 2d). Its mean value over the image reaches a satisfying level 180, Feb. 2004. of 0.93, which means that the estimations can be trusted. [9] E. Brusseau, J. Kybic, J.F. Deprez and O. Basset, “2D locally regularized strain estimation algorithm: Theoretical developments and Since the algorithm is three-dimensional, these results on experimental data”, IEEE Trans. Medical Imaging, to be information (axial strain, lateral and azimuthal published, 2007. displacements) are available for the whole scanned volume. [10] C. Schmitt, G. Soulez, R. L. Maurice, M.F. Giroux, and G. Cloutier, For clinical purpose, the desired parameter could be “Non-invasive vascular elastography: toward a complementary characterization tool of atherosclerosis in carotid arteries”, Ultrasound displayed like a movie (with the z axis corresponding to in Medicine and Biology, to be published, 2007. time), to see its evolution along the azimuth and to provide [11] J. Fromageau, J.L. Gennisson, C. Schmitt, R. L. Maurice, R. the physician with a better understanding of the imaged area. Mongrain, and G. Cloutier, “Estimation of polyvinyl alcohol cryogel mechanical properties with four ultrasound elastography methods and We chose here to present the axial strain along the z axis comparison with gold standard testings”, IEEE Trans. Ultrasonics, (perpendicular to the US scan) for two different positions Ferro. and Freq. Control, vol. 54, no. 3, pp. 498-509, Mar. 2007. (fig. 3). The axial strain for the middle slice (corresponding [12] J. Fromageau, E. Brusseau, D. Vray, G. Gimenez, and P. Delachartre, “Characterization of PVA cryogel for to the axe of the bone axis) is shown fig. 3a. Here again, the elasticity imaging”, IEEE Trans. Ultrasonics, Ferro. and Freq. coarse resolution is a limitation. Yet, it is still possible to Control, vol. 50, no. 10, pp. 1328-1324, Oct. 2003. distinguish the 3 regions. Fig. 3b exhibits the axial strain for an off-centered slice. The bone is not visible at this position, but the healthy and pathological regions can clearly be