Original Article
HIFU ABLATION OF RENAL TISSUE
HÄCKER
et al.
Authors from Germany describe
the use of percutaneously applied
high-intensity focused ultrasound
for non-invasive tissue ablation.
They found that the lessons they
learned from the use of this
technology in animals could be
transferred to its use in humans,
both of which are described. They
indicate that refinements in the
technology are essential before
this treatment can be used outside
the departmental stage.
The use of endoluminal
ultrasonography is discussed by
authors from the Netherlands, for
preventing significant bleeding
during endopyelotomy. In a
prospective study, they evaluate
this technology against helical CT.
Extracorporeally induced ablation of
renal tissue by high-intensity focused
ultrasound
AXEL HÄCKER, MAURICE S. MICHEL, ERNST MARLINGHAUS*,
KAI U. KÖHRMANN† and PETER ALKEN
Department of Urology, University Hospital Mannheim, Faculty of Clinical Medicine Mannheim,
Ruprecht-Karls-University of Heidelberg, Germany, *Storz Medical AG, Kreuzlingen, Switzerland,
and †Theresienkrankenhaus Mannheim, Germany
Accepted for publication 31 October 2005
OBJECTIVE
To investigate the safety and the effects on
healthy renal tissue of high-intensity focused
ultrasound (HIFU) applied extracorporeally.
PATIENTS, MATERIALS AND METHODS
Ultrasound waves (1.04 MHz) created by a
cylindrical piezo-ceramic element were
focused by a parabolic reflector to a physical
focus size of 32 × 4 mm (−6 dB). For an in
vivo study, HIFU was applied to the healthy
tissue of 24 kidneys, monitored by
ultrasonography, with a maximum power of
400 W and a spatially averaged intensity
(ISAL) in the focus of 1192 W/cm2. Fourteen
kidneys were removed immediately after
ablation to evaluate the side-effects and the
effects in the focal zone, and 10 kidneys were
removed delayed after 1, 7 and 10 days. The
clinical study consisted of 19 patients
requiring radical nephrectomy for a renal
tumour. HIFU was applied to the healthy
tissue of 19 kidneys (up to 1600 W,
ISAL = 4768 W/cm2) before proceeding with
the radical nephrectomy.
RESULTS
There were no major complications after
applying HIFU to the 43 kidneys. Side-effects
included skin burns (grade 3) in two patients.
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2 0 0 6 B J U I N T E R N A T I O N A L | 9 7 , 7 7 9 – 7 8 5 | doi:10.1111/j.1464-410X.2006.06037.x
During the follow-up there were no further
HIFU-specific side-effects. In one case (in vivo
study) there was a thermal lesion of the small
intestine, which was due to mis-focusing.
HIFU effects in the focal zone immediately
after application were: interstitial
haemorrhages, fibre rupture, shrinking of the
collagen fibres, and coagulation necrosis.
These effects occurred sporadically, and their
number and size did not correspond to the
number of HIFU pulses applied. After 7 and
10 days, there was a well-demarcated
coagulation necrosis in vivo.
CONCLUSION
Using this device, extracorporeally applied
HIFU can ablate healthy kidney tissue in vivo
in combination with diagnostic online
ultrasonography. The technique is safe and
resulted only in minor complications (skin
burns). Refinements in the technology are
essential to establish HIFU as a noninvasive
treatment option that allows complete and
reliable tissue ablation.
KEYWORDS
kidney, ultrasonography, ultrasonic therapy,
surgery, minimally invasive, high-intensity
focused ultrasound
779
H Ä C K E R ET AL.
FIG. 1. A schematic diagram of the generator for
HIFU application.
FIG. 2.
The principle of extracorporeal
kidney tissue ablation by HIFU
(clinical device).
Focal point 32 × 4 mm
1 MHz
ultrasound field
Focal
distance
100 mm
Piezoelectric
cylinder
Paraboloid
reflector
investigated in a pilot clinical study in
humans.
B-mode
Aperture diameter 100 mm
INTRODUCTION
The widespread application of CT and
abdominal ultrasonography increases the
dilemma of how to manage small (<4 cm),
incidentally discovered, solid or complex renal
masses [1]. Their slow growth, low metastatic
risk and the difficulty of differentiating
between benign and malignant lesions
preoperatively make the clinical significance
of such lesions unclear. Depending on the
individual clinical situation, the treatment
options currently available include
surgical excision by radical/partial open
or laparoscopic nephrectomy, watchful
waiting, or energy-based ablation (e.g.
radiofrequency ablation, cryoablation,
microwave thermoablation or interstitial laser
ablation). As an extracorporeal technique,
high-intensity focused ultrasound (HIFU)
delivers thermal energy without needing to
insert a probe into the tumour and thus has
the potential to become a fully noninvasive
ablation technique.
Our group developed an extracorporeal
flexible HIFU device for kidney tissue ablation.
We described the system technically [2] and
reported that, in perfused ex vivo kidney
tissue, HIFU lesions can be induced with
precision and are sharply demarcated from
the surrounding tissue; lesion size can be
controlled by the amount of generator power
and pulse duration [3]. The present study
investigated the safety of this extracorporeal
HIFU device in vivo and its effects on the
tissue. The safety of the technique was then
780
PATIENTS, MATERIALS AND METHODS
The Storz UTT system (Storz Medical AG,
Kreuzlingen, Switzerland) was used for HIFU
treatment, as previously described in detail
[2]. Briefly, a cylindrical piezo-ceramic
element creates ultrasound waves at an
excitation frequency of 1.04 MHz and the
waves are focused by a parabolic reflector
(Fig. 1). The field distribution results in a
physical cigar-shaped focus size of
32 × 4 mm (−6 dB) [3]. The aperture diameter
and focal distance were both 100 mm. The
dimensions of the applicator and focus were
identical for both the in vivo and clinical
applications. The maximum power (Pel) of
the generator was up to 400 W for in vivo
application (Pel = 0–400 W; the spatially
averaged intensity at the focus, ISAL, was
0–1192 W/cm2) and 1600 W for clinical
application (Pel = 0–1600 W; ISAL = 0–4768 W/
cm2). The intensities are calculated with an
efficiency factor of η= 0.5 (determined at
low power settings). A diagnostic 3.5 MHz
ultrasound transducer (B-mode; Kretzt
Technology AG, Zipf, Austria) is positioned in
the centre of the HIFU transducer for in-line
imaging of the focal area. The centre of the
focal zone is indicated on the ultrasonogram
by a cross.
The in vivo study was approved by the local
state government office; 12 male beagle dogs
were used. Under inhalation anaesthesia
(isoflurane), the dog’s skin was shaved and
degreased in the treatment area and was fixed
in an upright position in a basin filled with
degassed water controlled at 37 °C.
Ultrasound waves were coupled to the dog’s
body inside the water-filled basin. The focal
zone was positioned in the centre of the
renal parenchyma. The aim was to ablate
healthy renal tissue by non-overlapping
focal positions with each area generally
subjected to one ultrasound pulse with
ultrasonographic guidance and manual
changes of the focal position. During HIFU
application, ventilation of the dog was
stopped to reduce the respiratory movement
of the kidney. In all, 221 pulses were applied
(mean 10; range 2–23 per kidney) to the
24 kidneys (12 right, 12 left) at 200 W
(ISAL = 596 W/cm2) or 400 W (ISAL = 1192 W/
cm2) and a pulse duration of 1–5 s, with an
exposure separation of ≥ 30 s between each
pulse. The mean focal depth was 53 mm.
The Ethical Committee of the University of
Heidelberg approved the clinical study, and
written informed consent was obtained from
each patient. All patients had malignant renal
tumours requiring radical nephrectomy. The
principle of extracorporeal kidney tissue
ablation by HIFU is shown in Fig. 2. The main
feature of the generator developed for clinical
application is that it allows ultrasound waves
to be directly coupled to the body surface by
means of a flexible cushion (polyurethane)
filled with cooled (16 °C) degassed water. To
adjust the penetration depth individually for
each patient the amount of water inside the
cushion can be controlled electronically.
Under general anaesthesia, the patient was
placed on the operating table in the flank
position. To optimize the contact to the
patient’s skin, ultrasound gel was applied
after shaving and degreasing the skin. An
initial evaluation of the best application route
was made with an external diagnostic
ultrasonography probe (Fig. 3a) before the
therapeutic ultrasound source was coupled to
the patient’s body (Fig. 3b). The cushion was
then filled with water to the required
penetration depth. The integrated in-line
ultrasound transducer was used to locate the
optimum sonic window for coupling the
©
2006 BJU INTERNATIONAL
HIFU ABLATION OF RENAL TISSUE
FIG. 3.
The extracorporeal coupling.
(a) Coupling window between
interfering ribs and iliac crest.
(b) Ultrasound applicator on the
patient’s body surface (flank
position).
50 (41–56) mm and 184 pulses were applied
(mean 9.7/patient).
a
After the HIFU application, the skin in the
flank region was examined to identify thermal
or mechanical injuries. Nephrectomy was
performed immediately (<1 h) afterwards
(14 in vivo kidneys, and after all clinical
applications) during the same anaesthesia
and using standard surgical procedures.
Delayed nephrectomy was performed on one
dog after 1 day, on three after 7 days, and on
one after 10 days. During surgery, the skin, the
tissue along the ultrasound propagation
(muscle, fat) route, and the organs adjacent to
the kidney were investigated carefully. After
nephrectomy, the kidney was examined
macroscopically, sectioned serially in 3-mm
slices, and the maximum lesion diameters
were measured using a sliding calliper. The
tissue was fixed in 10% buffered formalin,
embedded in paraffin wax, stained with
routine haematoxylin and eosin, and
examined by a pathologist. In the clinical
study, the patients were monitored by the
office urologist after discharge.
b
RESULTS
FIG. 4.
The ultrasonographic focus
positioning
water cushion, to position the focus in the
target area, and to ensure that no bone
structures (ribs; Fig. 3a) or air (bowel)
interfered with the propagation of the
ultrasound waves that would result in
absorption and/or reflection (Fig. 4). During
HIFU application, ventilation of the patient
was stopped to reduce the respiratory
movement of the kidney. In all, 19 human
kidneys were sonicated extracorporeally; HIFU
was applied to healthy renal parenchyma that
had not been invaded by the renal tumour.
The pulse duration was 4 s with an interval
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2006 BJU INTERNATIONAL
No systemic adverse effects occurred
during or after HIFU application to 19 human
and 24 dog kidneys up to a Pel of 1600 W
(ISAL = 4768 W/cm2). In particular, there were
no alterations in the muscular wall, or on the
surface of the kidney, no subcapsular or
perirenal haematomas, and no thermal injury
to the ureter, renal pelvis or renal vascular
pedicle. In the in vivo study, there was a
thermal necrosis of the small intestine in one
dog due to mis-focusing.
of ≥30 s between pulses. While evaluating
the side-effects, we increased the treatment
variables over time. Based on the results of
the in vivo study, we started with a Pel of
400 W (ISAL = 1192 W/cm2) and subsequently
increased the number of non-overlapping
pulses up to 10 on each target area in
healthy renal tissue. If no side-effects
were detected we increased Pel stepwise
in 200-W increments up to 1600 W
(ISAL = 4768 W/cm2), starting with one pulse
and ending with a maximum of 10 in one
area. The mean (range) penetration depth was
In the in vivo study the macroscopic lesion in
the renal parenchyma immediately after HIFU
application was characterized by a defect in
the boundary area between the medulla and
cortex, with striped haemorrhages leading
along the centripetal tubules (Fig. 5a). These
effects were detected at irregular intervals
and their number did not correspond to the
number of HIFU pulses applied. In seven
kidneys, we were unable to identify any
lesions immediately after HIFU application
(five kidneys) or after 1 day (two kidneys). The
macroscopically measurable lesions varied
considerably in size, in addition to always
being smaller than the physical focus size. The
maximum lesion diameters of each kidney
unit are summarized in Table 1. At 7 and
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H Ä C K E R ET AL.
10 days after HIFU there were well
demarcated lesions with coagulation necrosis
surrounded by healthy renal parenchyma
(Fig. 5b).
In the human study there was no thermal
injury to other adjacent organs (colon,
duodenum, vena cava). Two patients had a
localized grade III skin burn (3.0 cm × 0.3 cm
and 0.6 cm × 0.6 cm). Both skin burns were
because of incorrect coupling conditions. In
these patients, air bubbles were detected in
the ultrasound gel, and these might have
caused uncontrolled reflection, resulting in a
thermal necrosis in the skin below. One skin
burn occurred at a Pel of 800 W (penetration
depth 55 mm), and the second at the highest
Pel of 1600 W (penetration depth 41 mm).
These were managed conservatively and
healed, leaving a scar. No other HIFU-specific
side-effects occurred during follow-up. As
with the in vivo study, in the human kidneys
macroscopically there were only limited
effects of variable dimensions in the
treatment area immediately after HIFU;
haemorrhages were detected in 15 of the 19
kidneys, a whitish-grey thermal lesion in three
of the 19, and a cystic liquefied necrosis
10 mm in diameter in one kidney.
Histologically, the HIFU effects were
predominantly characterized by minor tissue
necrosis and small interstitial haemorrhages
from fibre ruptures in the walls of small
vessels. Shrinkage of collagen fibres
accompanied by eosinophilic epithelial
necrosis and melting of the nuclei were proof
of a thermal injury in the focal area (Fig. 6).
Using diagnostic in-line ultrasonography
allowed good visualization of all anatomical
areas of the kidney, as well as placing the
focal zone in the target tissue. The
multidirectional flexibility of the water
cushion (clinical device) made it possible to
couple the transducer and place the focal
point in the kidney, allowing for anatomical
differences in the 19 patients. The transducer
had to be moved manually. The path of the
therapeutic ultrasound could be imaged
clearly enough to prevent ultrasound
absorption or reflection by the intestines,
bones or lung. It was not possible to visualize
the development of lesion sizes or changes to
the tissue during sonication. This was partly
because of back-scattering of the HIFU waves
in the tissue that over-modulated the
diagnostic ultrasonography and created a
totally white image in the B-scan. After a
HIFU pulse, a hyperechogenic area appeared
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TABLE 1 The maximum lesion sizes of in vivo dog kidneys after HIFU
Kidney
no.
1
2–14
Power/pulse duration
200 W/1 s
400 W/5 s
Time to nephrectomy
after HIFU
<1 h
<1 h
15–16
17–22
23–24
400 W/5 s
400 W/3 s
400 W/5 s
24 h
7 days
10 days
sporadically in the focal area for a few
seconds.
DISCUSSION
Advances in technology are changing how
renal masses are diagnosed and treated. The
aim of extracorporeal HIFU technology is the
‘contactless’ ablation of defined parts of an
organ by extracorporeally applied ultrasound
energy focused at a selected depth within the
body, to induce a sharply demarcated thermal
lesion. Overlying and surrounding tissues
remain unchanged, as the energy outside the
focal zone decreases sharply. Being able to
treat small renal masses transcutaneously
by ablating the tumour completely, and
noninvasively without needing to touch or
manipulate the tumour by puncture, is an
attractive treatment option. HIFU would
appear to be the ideal minimally invasive
approach. The technology is not new; the first
reports were published around 1940 [4]. To
date, its feasibility has been shown on
malignant and nonmalignant tissue in several
organs (eye, brain, liver, breast, bladder,
uterus, testis, prostate and others) with
several groups reporting no increase in the
rate of tumour-cell dissemination or
metastases [5,6].
The first attempts at extracorporeal HIFU
ablation of renal tissue began in 1992 using a
technology derived from piezo-electric
lithotripters [7,8]. However, focusing with a
large aperture diameter was not suitable for
clinical use. Since then, only a few groups
Maximum lesion size, mm
No lesion
No lesion in 5 kidneys
2×2
3×2
3×2
3×2
4×3
5×2
5×3
5×4
No lesion
20 × 7
8×3
have been working on HIFU ablation of renal
tissue [6,9,10]. To overcome the inflexibility of
a large aperture size, we developed a new
HIFU source with a smaller diameter of 10 cm
for flexible extracorporeal application. With
this, we showed in perfused ex vivo kidney
that HIFU lesions can be induced with
precision and are sharply demarcated from
the surrounding tissue [3]. Lesion size could
be reliably controlled by the power of the
generator and pulse duration.
The present study tested the safety of
this newly developed generator in the
extracorporeal HIFU treatment of kidney
tissue in animal studies in vivo and in humans.
Ultrasound has thermal effects on tissue, and
nonthermal effects (cavitation, acoustic
streaming, oscillatory motion). In the present
study, macroscopic and histological analysis
of the kidneys showed that mechanical
lesions (ruptured tissue and haemorrhages)
prevailed over thermal lesions. However, the
histological findings of acute HIFU lesions are
only indicative, because the morphological
characteristics of the lesions change during
the follow-up period. Vallancien et al. [8]
described histological findings similar to
those in the present study in porcine kidneys
immediately after HIFU application. They
observed an area that was less strongly
stained by periodic acid-Schiff, while
histologically, there was evidence of
tissue laceration with intense congestion,
hyperaemia and marked alterations to
the microcapillaries. Electron microscopic
studies showed complete destruction of the
intracytoplasmic organelles (mitochondria,
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2006 BJU INTERNATIONAL
HIFU ABLATION OF RENAL TISSUE
FIG. 5. The macroscopic appearance of the lesions. (a) Immediately after HIFU: lesion in the boundary area
between medulla/cortex (black arrow) with striped haemorrhage leading along the centripetal tubules (white
arrow) after applying one pulse at 400 W (5 s). (b) 10 days after HIFU in vivo: a well demarcated HIFU lesion
a
Another major drawback was the lack of a
reliable imaging method. With diagnostic
ultrasonography it was impossible to quantify
and image the HIFU effects reliably in terms of
lesion size/morphology and definitive
complete cell death during or after ablation.
Consequently, it was also impossible to
position the lesions exactly side by side.
Ultrasound is also obstructed by bone and airfilled viscera. This drawback can actually be an
advantage for monitoring ultrasonography, as
it is important to identify the position of such
structures in relation to the therapeutic beam.
Possible improvements in the online
monitoring of complete tissue ablation might
be provided by a direct, computer-aided
evaluation of the ultrasound signals, Doppler
ultrasonography or MRI to assess structural
and thermal changes [11]. MRI has better
image quality and the ability to monitor
temperature, but is expensive and has a
poorer spatial resolution. Relevant clinical
experience is lacking, and as yet there is no
device that can treat renal tumours with MRI
guidance. The transducer had to be moved
manually; this was time-consuming, and the
movements were not precise.
b
ribosomes, lysosomes), although
macroscopically the tissue appeared intact [8].
After 2 days, early signs of necrosis were
detected with a persistent zone of hyperaemia
and intense congestion, on day 7 the area was
©
physical focal size. These lesions were of
variable size, depending on the acoustic
intensity and on local variations in the
absorption coefficient of ultrasound in tissue.
Nevertheless, the changes were only apparent
within the targeted area, and the surrounding
structures always appeared normal. In view of
the novelty of the technique, we did not know
how much energy could be delivered to
human kidneys without adverse effects, so
the objective of the present study was to
determine this. Although we know how much
power is emitted from the ultrasound probe,
at present it is impossible to know how much
energy is delivered to the focal zone, which
depends on focal length, target tissue and
intervening tissue characteristics, and, most
importantly, on the perfusion of the kidney.
Only more experiments will enable us to
progress and to ablate clinically relevant
tissue volumes by increasing the number of
pulses and power levels.
2006 BJU INTERNATIONAL
completely necrotic, and by day 90 there was
complete fibrosis of the treated area [8].
In the present study, the measured
macroscopic lesion sizes never reached the
Meanwhile, the clinical device has been
improved by adding a mechanical arm to
stabilize and guide the applicator [10]. Further
technical advances (automatic or robotguided scanning, as is available for transrectal
treatment of prostate cancer) will reduce
treatment time and might make lesion
positioning more precise. Another major
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H Ä C K E R ET AL.
challenge was the respiratory movement of
the kidney. Although the procedures were
performed under general anaesthesia and
attempts were made to reduce the respiratory
movement of the kidney by briefly stopping
ventilation during sonication, it was
impossible to place the lesions precisely next
to each other. Technically, this could be
improved by computer-guided automated
coordination between the organ movement
and HIFU application. Even using a HIFU probe
with an aperture size of 10 cm, as in the
present study, limited the choice of finding a
suitable acoustic window for coupling the
probe to the patient’s body, as bone (ribs) and
air cavities (bowel) in the overlying areas
absorb energy and restrict access to the
affected areas. One solution might be an
approach involving several HIFU probes [12].
As these probes become smaller, it might be
possible to improve coupling conditions and
target access. Another possible advantage of
this approach is its flexibility, in that it enables
focal volumes of various sizes and shapes to
be created by varying the exposure conditions
of the individual probes. In healthy,
homogeneous, ex vivo renal tissue, lesion size
can be controlled by the amount of applied
power and the pulse duration. Identical lesion
sizes and shapes are reliably reproducible [3].
In vivo, the influence of overlying tissue (fat,
muscle, bone, air) combined with absorption
and reflection, and structural heterogeneity
of the tumour tissue can significantly affect
the acoustic peak intensity in the focal zone.
This can result in lesions that are less
consistent in size and shape, or even in
unpredictability in the case of uncontrolled
lesion-to-lesion interaction. A technical
solution to the problem of adapting peak
intensities would be, as mentioned above, a
reliable imaging method for assessing
definitive tissue necrosis during HIFU
application. As no such method is yet
available, the threshold acoustic intensity that
predicts the success of the treatment in terms
of reliable cell death in tumour tissue needs to
be determined in future studies.
In conclusion, using this device,
extracorporeally applied HIFU can ablate
healthy kidney tissue in vivo in combination
with a diagnostic online ultrasonography. In
the present pilot clinical study with few
patients, this technique was safe, resulting in
only minor complications (skin burns).
Refinements in the technology and an
improved knowledge of the correlation
between the applied acoustic energy and
784
FIG. 6. The microscopic appearance of a thermal lesion in the human kidney. Haematoxylin and eosin × 25.
tissue effects are essential to establish HIFU
as a noninvasive treatment option that allows
complete and reliable tissue ablation.
ACKNOWLEDGEMENTS
This project was supported by research grants
from the Faculty of Clinical Medicine
Mannheim of the Ruprecht-Karls-Universität
Heidelberg and from the STORZ-Medical
Company, Kreuzlingen, Switzerland.
CONFLICT OF INTEREST
None declared.
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Correspondence address: Axel Häcker,
Department of Urology, University Hospital
Mannheim, Theodor-Kutzer-Ufer 1–3, 68135
Mannheim, Germany.
e-mail: axel.haecker@chir.ma.uniheidelberg.de
Abbreviations: HIFU, high-intensity focused
ultrasound; Pel, maximum electric power; ISAL,
spatially averaged intensity in the focus.
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