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    Diagnostic and Interventional Imaging (2012) 93, 246261

    CONTINUING EDUCATION PROGRAM: FOCUS. . .

    Radiologically-guided thermal ablation ofrenal

    tumours

    F. Cornelisa,,b, P. Balageas a, Y. Le Bras a, G. Rigoua,J.-R. Boutaulta, M. Bouzgarrou a, N. Greniera

    aDepartment ofdiagnostic imaging andtherapeutics, hpital Pellegrin, CHUde Bordeaux,

    place Amlie-Raba-Lon, 33076 Bordeaux, Franceb Institut Bergoni, 229, cours de lArgonne, 33076 Bordeaux, France

    KEYWORDS

    Kidney;Radiofrequency;Focused ultrasound;Technique;Therapy

    Abstract Thermal ablation techniques for renal tumours have become the norm in surgicallyat-risk patients. These percutaneous treatments are locally effective, particularly for tumoursmeasuring less than 4 cm. Larger tumours may be treated by adapting the technique and strat-egy. Multidisciplinary discussion is essential before any decision, in order to decide on the mostappropriate technique. Radiofrequency is simple, effective and inexpensive. Cryotherapy ismore complex and should be preferred when the tumour is large or there is vascular or uri-

    nary tract contact. Microwaves can be used to treat larger tumours. Morbidity is low, but goodknowledge of these techniques and of dissection is required to avoid injury to neighbouringdigestive or urinary structures. 2012 ditions franaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.

    Over the last few decades, the increasing use of imaging in many diseases has profoundlyaltered the natural history of kidney cancer. Nearly 50% of kidney cancers diagnosed arecurrently discovered by chance [1]. This has meant earlier detection of often small, renaltumours, and in 70 to 80% of cases, while they are still in a non-metastatic stage [2,3].These changes in presentation and prognosis have considerably modified the managementof renal cell carcinomas (RCC), particularly over the last ten years, with the development

    of nephron-sparing techniques replacing open surgery. The initial technique of laparo-scopic partial nephrectomy has been supplemented by the techniques of laparoscopicthermal ablation, including the use of radiofrequency (RF) and cryoablation. However,some patients with small kidney cancers cannot tolerate a surgical procedure, because ofadvanced physiological age, comorbidities, or already precarious renal function. For thesepatients, a percutaneous approach using thermal ablation is gradually predominating,

    Corresponding author.E-mail address: [email protected] (F. Cornelis).

    2211-5684/$ see front matter 2012 ditions franaises de radiologie. Published by Elsevier Masson SAS. All rights reserved.doi:10.1016/j.diii.2012.02.001

    http://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001http://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001http://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001http://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001mailto:[email protected]://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001http://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001mailto:[email protected]://localhost/var/www/apps/conversion/tmp/scratch_6/dx.doi.org/10.1016/j.diii.2012.02.001
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    Radiologically-guided thermal ablation of renal tumours 247

    particularly because the equipment and techniques havedeveloped to be ever more efficient in terms of sparing renalfunction and being less invasive for these fragile patients.This review does not set out to explain the principles ofthe various thermal ablation techniques (RF, cryoablation,microwaves, laser and focused ultrasound), already widelydescribed in the literature, but aims rather to give the ben-efits, limitations, complications and performance reported,

    and the principles of post-treatment monitoring.

    Guidance methods

    A percutaneous approach is required in the majority ofthermal ablation indications and techniques. However, thelaparoscopic route, which is effective in oncological terms[4], is still suggested for tumours at risk due to theirtopography, particularly in an anterior position and there-fore difficult to access via a posterior approach, justifyingdirect visual control during thermal ablation. Apart fromits less invasive character, the advantages of the percuta-neous approach are less pain, immediate verification, which

    is possible using CT, MRI or ultrasound, a shorter periodof hospitalisation [5] and reduced overall cost [6]. In hismeta-analysis of 46 studies from 1996 to 2006, Hui et al. [5]concluded that percutaneous radiofrequency is safer and aseffective as laparoscopic radiofrequency, with complicationrates of 3.1 and 7.4% respectively, for identical secondaryefficacy of 92% at 5 years.

    CT guidance is currently best for localising the tumourand controlling the procedure. The limits and relationshipsof the tumour to be treated can be precisely deter-mined, but nevertheless it can be adversely affected by thepatients breathing movements, which justifies positioningthe applicators during apnoea. At the end of the procedure,it can help in looking for immediate complications before

    the patient is transferred to the recovery room. However,because of the risks of using iodinated contrast agents andthe frequent need for an injection of contrast agent beforethermal ablation, to identify the relationships of the lesion,identifying enhancement of tumour remnants at the endof the session can be difficult. This may prevent any fur-ther treatment during the same period of anaesthesia. Asan alternative, or associated with CT, ultrasound guidancehas proved to be feasible and to provide good procedu-ral safety [7,8] and can be an effective aid for fast andaccurate positioning of the applicators. It is neverthelesslimited by the generally narrow acoustic window; in thesame way, the formation of hyperechoic gas microbubblesat the treatment site alters the ultrasound window [9] inradiofrequency therapy, and the formation of ice is a sourceof reflection during cryotherapy. Finally, MRI guidance pro-vides real-time monitoring of the ablation site, either byconventional T1-weighted sequences with or without con-trast, by T2 sequences or by thermometry sequences [9].This technique is however limited by restricted accessibilityand MRI compatible equipment.

    Performing biopsies

    At the time when surgery was the only therapeutic option fora solid renal mass, biopsies were limited to lesions suspected

    of being renal metastases, lymphomas or abscesses, orwhen histological analysis was needed because of metastaticdevelopment of a cancer or tumour which could notbe immediately resected [10]. Heilbrun argued that pre-operative biopsies did not provide additional information forconfirming the malignancy of lesions when the character-istics of malignancy were typical in pre-operative imaging[11].

    When thermal ablation treatment is to be undertaken,on the other hand, pre-treatment biopsy seems to be justi-fied, firstly because there will be no postoperative surgicalspecimen, secondly because nearly 20% of T1 tumours areestimated to be benign (particularly when less than 3 cm[12], with up to 44% of tumours less than 1 cm being benign[13]) and thirdly because of the value of grading the lesionand obtaining a molecular analysis for determining a prog-nosis. This is all the more justified now that the rate offalse-negative biopsies is in the order of 1%, with an inci-dence of symptomatic complications of less than 2% [14].In certain special cases (e.g. von Hippel Lindau disease,a recent history of RCC), a biopsy is not essential. Simi-larly, for cystic tumours, the risk of malignancy can currently

    be evaluated using Bosniaks classification and the resultingtherapeutic choices assessed [2].

    Two approaches should be discussed if it is decided thata biopsy is indicated. A biopsy performed during the samesession as the ablation certainly has the advantage of savingtime and being more comfortable for the patient. However,due to the significant proportion of biopsies that have provednegative or shown a benign lesion and have led to treat-ment without any histological evidence or even treatmentthat was unnecessary, biopsy is now proposed during a pro-cedure prior to thermal ablation. This provides a samplecontributing to the decision before treatment [15] but canput constraints on patients who may require adjustment to

    their anticoagulant or antiplatelet medication.

    Clinical results

    Thermal ablation using radiofrequency

    Since Zlotta et al. [16], many studies have reported the effi-cacy of radiofrequency ablation (Fig. 1) on RCC, even thoughlong-term studies are not yet available. Local recurrence-free survival at 5 years is in the order of 89 to 92% [17,18]and most authors agree on the fact that most recurrencesappear during the first year [19]. However, recurrences canoccur several years after what was considered to have been

    complete treatment of the lesion [20], although after threeyears they are still rare [21]. In a long-term follow-up of amean of 61.6 months in a population of 31 patients, Levinsondescribes only three in situ recurrences, all occurring before31 months, and no metastatic development [22]. Primaryefficacy is 67 to 100% [1719,23]. This wide heterogene-ity of results can be explained particularly by very variablefollow-up times and tumour sizes. Nevertheless, the pro-portion of conversions to surgery is low, with a mean of1.6% in the literature, because repeating radiofrequencyprocedures is not described as a technical challenge; itis used in a mean of 8.5% of cases [24]. The secondaryefficacy of radiofrequency treatment seems much more

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    248 F. Cornelis et al.

    Figure 1. Radiofrequency thermal ablation of an exophytic left renal tumour (histologically demonstrated clear cell carcinoma) locatedon the lower pole: a: localising CT acquisition with injection of contrast agent, in an axial slice; b: radiofrequency treatment using adeployable antenna guide: post-injection axial CT scan; c: immediate postoperative control shows classic changes (gas, interstitial oedema,perirenal infiltration); d: MRI control in an axial slice, 2 months after the procedure, showing the typical sequelae of post-ablation necrotic-haemorrhagic changes as a T2 hyposignal; e: spontaneous T1 hypersignal on the MRI control in an axial slice at the same level; f: no

    enhancement following injection of gadolinium chelate on the control MRI in an axial slice.

    informative and representative of the contribution of thetechnique to oncological control, with values between 90and 100% [17,21,22,25,26]. In a small series, comparing 37patients treated by partial nephrectomy with 40 patientstreated by percutaneous or laparoscopic radiofrequency,Stern found no significant difference in recurrence-free sur-vival at 3 years for T1a tumours, with respective levels of95.8% and 93.4% [27]. In radiofrequency thermal ablation,the size and sinus extension of the tumour to be treatedcan increase the risk of technical failure [25]. In a seriesof 104 patients and 125 tumours, Zagoria was able to treat

    all cancers measuring less than 3.7 cm completely. The sur-vival rate without recurrence fell to only 47% for tumoursover 3.7 cm in size. For tumours larger than 3.6 cm, thisauthor described a risk of recurrence increased by a factorof 2.19 for each additional centimetre. The recurrence-freesurvival rate was not however influenced by sex, the sideor cranio-caudal topography of the tumour. Zagoria foundno significant difference whether the site of the lesion wasexophytic, parenchymal, central or mixed [19]. Gervais, ina series of 85 patients and 100 tumours, identified tumoursize of less than 3 cm and a non-central location as inde-pendent factors of primary efficacy. Only the non-centralsite of lesions is described as an independent factor of

    secondary efficacy. Gervais emphasised that the choice ofa size limit for treatment is not unequivocal. In his series, acut-off at 4 cm produced treatment that was 90% complete,while excluding 15% of patients who could have benefitedfrom effective treatment. A cut-off at 5.8 cm would mean99% of patients could be treated completely, but with ashort-term success rate of 63% [17]. At present, these resultsneed to be confirmed in series with long-term follow-up.

    Cryotherapy

    The first use of cryoablation to treat renal tumours (Fig. 2)was reported in 1995 [28] and was initially performed bylaparoscopy (65%) [29]. The percutaneous approach hasonly developed recently owing to a reduction in the sizeof cryoprobes. The basis of this ablation technique is thedestruction of tumour cells using freeze/thaw cycles. Dur-ing the freeze part of the cycle, the formation of ice crystalsdenatures the intracellular proteins, breaks up cell struc-tures and modifies cell membrane function. Subsequently,after increasing the intracellular osmotic pressure, an inflowof water occurs during thawing resulting in the tumour cellsbursting [30]. A major advantage of cryoablation is the abil-ity to monitor the ablation zone in real time [31,32] by

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    Radiologically-guided thermal ablation of renal tumours 249

    Figure 2. Cryoablation of a left renal papillary tumour in an anterior exophytic location, near the tail of the pancreas, in a patient witha history of contralateral nephrectomy: a: left anterior renal tumour in a CT axial slice with injection (arterial phase); b: renal mass in asagittal slice with injection (cortical phase); c: cryotherapy with visualisation of a needle and dissection with CO2 to displace the digestivesstructures: axial CT without injection; d: cryotherapy: the 3 cryoprobes and the CO2 dissection are visible on this oblique coronal CT scan; e:controlafter the procedure, in an axial slice comparable to figure c; f: controlin an oblique coronal slice showing the hypodenseextension ofthe ice after removal of the cryoprobes, comparable to figure d; g: MRI control at 6 months showing the post-ablation necrotic-haemorrhagicchanges, with a typical T2 hyposignal halo in this axial slice; h: absence of enhancement on this T1-weighted axial MRI with injection.

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    250 F. Cornelis et al.

    Figure 2. (Continued).

    Figure 3. Microwave thermal ablation of an upper polar tumour (clear cell carcinoma) of the left kidney: a: CT axial slice with injectionof contrast agent in the arterial phase; b: comparative coronal slice with injection of contrast agent in the arterial phase; c: comparativesagittal slice, with injection of contrast agent in the arterial phase: d: treatment with microwaves, with an applicator positioned in themass: CT axial scan without injection; e: applicator positioned in the centre of the lesion on this coronal scan; f: control CT axial scan, withinjection (arterial phase) at 6 months, showing neither recurrence nor any remnant; g: control CT scan with injection: comparative coronalslice. (Acknowledgements to Dr Rgis Hubrecht, centre hospitalier de Pau, France.)

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    Radiologically-guided thermal ablation of renal tumours 251

    Figure 3. (Continued).

    visualising the physical changes caused by freezing, whetherusing CT, MRI or ultrasound. This is particularly useful whenthe lesion to be treated is close to sensitive organs or struc-tures. Another advantage is that there is no denaturing ofprotein, as in hyperthermic treatment, in the architectureof supporting tissues, particularly urothelial tissue, whichis therefore conserved. In Kunkles meta-analysis [29], theprimary efficacy of cryotherapy was better than that of RFtreatment, with a reoperation rate of 8.5% for RF versus1.3% for cryotherapy (P< 0.0001). The local tumour progres-sion rate was significantly higher for RF (12.9% as against5.2% (P< 0.0001) for cryoablation. Moreover, the frequency

    of metastases was reported to be lower for cryoablation(1.0%) than for RF (2.5%, P= 0.06) during monitoring.

    Microwave thermal ablation

    Microwave ablation is a thermal ablation technique that iscurrently used for the treatment of hepatocellular carci-noma or lung carcinoma [33], but its use in kidney cancer isstill being evaluated (Fig. 3). The potential benefit of thistechnique [34] is ablation that is not limited by desiccation,carbonisation or thermal convection [35]. As a consequence,the temperature obtained is high, and can result in a largerablation zone being treated in less time.

    After adjusting the technique, Clark et al. [36] gave 10patients microwave treatment before nephrectomy. Histo-logical analysis showed uniform cell death in the ablationzone. Liang et al. [33] recently reported the results of afeasibility study in which 12 patients were treated with noremnant or recurrence at a mean follow-up of 11 months.Carrafiello et al. [37] also performed 12 successful proce-dures, with a mean follow-up of 6 months [314]. It ishowever necessary to analyse complications, tolerance andefficacy in the medium term.

    Focused ultrasound ablation

    Many experimental studies have been performed on the kid-ney in animals (Fig. 4). In contrast, clinical applications arestill in the very early stages and no recent review of clinicalstudies has been published. Nevertheless, such applicationswere initiated very early on because of the totally non-invasive character of this technique. In the 1990s, a study[38] including eight patients treated pre-operatively showedthermal ablation lesions. More recently, Marberger et al.[39] treated 16 patients, again pre-operatively, but consid-erably underestimating the volume of the lesion induced(only 15 to 35% of the target volume). The results wereonly analysed for the 10 of the 13 patients treated by

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    252 F. Cornelis et al.

    Figure 4. Focused ultrasound thermal ablation performed during a large animal experimental procedure: a: positioning the transducer,with the red triangle showing the focusing cone. The transducer is visible at the bottom of the image (arrow), on a T1-weighted axial MRimage; b: determination of the focal point (arrow) on the T1-weighted sagittal MR image; c: temperature MRI (proton resonance frequency(PRF) method) controlling heating at the focal point in real time, merged with a sagittal T1-weighted gradient echo MR image; d: thermaldose mapping merged with a sagittal T1 gradient echo MR image; e: control following ablation at the same level by T1-weighted MRI (sagittalslice) after injection, showing the ablation area which is not enhanced; f: control T2-weighted TSE MRI (sagittal slice) showing necrotic-haemorrhagic changes as a T2 hyposignal; g: apparent diffusion coefficient (ADC) mapping in a sagittal slice showing diffusion restriction ofthe treated area.

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    Radiologically-guided thermal ablation of renal tumours 253

    Figure 5. Digestive complications of the ablation procedures: a: left renal mass on the only kidney (arrow) in a patient with a history ofipsilateral ablation (dotted arrow); b: radiofrequency with deployable needle: CT axial scan without injection; c: enhancement within theablation zone (hyposignal), corresponding to leakage of excreted contrast medium on this T1-weighted MRI with injection and subtraction;d: fistulation of the colon shown by a hypersignal in the intestinal tract in the later phases after injection, in T1-weighting with subtraction.Secondary infection of the ablation zone led to nephrectomy and dialysis for this patient.

    Wu et al. [40] who were being given palliative treat-ment. In the Oxford group series, complete treatment wasdemonstrated, in five cases out of 10 [41], only when thetumour was completely accessible via the subcostal route,which further emphasises the problem of acoustic inter-faces. These issues have been discussed in a recent generalreview [42]. This author also highlights the problems ofpositioning the focus during respiration, since, even if theshots are made during apnoea, each shot must be reposi-tioned relative to the others to the nearest millimetre, toavoid leaving intervals of untreated tissue. Technical solu-

    tions have nevertheless recently been proposed [4345] toimprove control of the energy applied, thus opening up newprospects.

    Complications

    In addition to its oncological efficacy, the low morbidity ofpercutaneous thermal ablation is a major asset for the treat-ment of kidney cancer in patients who are poor candidatesfor surgery because of their comorbidities [46]. The rates ofcomplications for thermal ablations reported in the litera-ture are very variable, between 4 and 37%, because of an

    absence of standardisation in grading the side effects [47],which have mainly been described for radiofrequency andcryotherapy techniques.

    Bleeding

    A perirenal haematoma is the most common complication,in 0 to 30% of cases depending on the series [17,48,49],and particularly concerns procedures performed usingcryotherapy, even if more evidence must be obtained fromlarge series. These haemorrhages are usually minor and

    asymptomatic and do not justify special monitoring. Therisk of major bleeding with a fall in erythrocyte count andthe need for transfusion is rare, in the order of 0 to 2% inthe literature [17,19]. The risk of bleeding is increased inpatients receiving non-interrupted antiplatelet therapy or ifthe lesion is close to a vascular pedicle. It can be preventedby good vascular screening before the procedure and withrapid, optimal positioning of the electrode. Gross haema-turia, at the end of the procedure, is a rare event occurringin 0 to 2.5% of cases [50]. This should not be considered analarm signal, especially if the urine gradually clears within12 hours [51]; this risk will be greater in the case of a centraltumour [51,52].

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    Figure 6. Urinary tract complications after thermal ablation in two different patients: a: radiofrequency thermal ablation of a left renalmass on a solitary kidney: CT axial slice with injection; b: procedure complicated by a retroperitoneal urinoma from calyceal leakage, easilyidentified on late CT acquisitions; c: radiofrequency thermal ablation of a central right renal tumour: late CT axial slice with injection; d:procedure complicated by stenosis of the upper urinary tract, identified by T2-weighted MRI (axial slice).

    Pain and neuromuscular weakness

    This is usually temporary [19] and uncommon, beingdescribed in 4.5% of cases [20,26], and results from lesionsof the lumbar plexus, subcostal or genitofemoral nerves,which pass close to the lower pole of the kidney and thepsoas muscle [9,51,53]. Posterior approaches passing closeto the anterior surface of the psoas muscle are most at risk.

    Pneumothorax

    The incidence of pneumothorax is 1 to 2% [19,50]. In most

    cases, these pneumothorax are minor, well tolerated and donot justify drainage [54]. Approach through a pleural recessis sometimes anticipated and unavoidable for tumours whichare difficult to access [54].

    Risk factors

    The rate of major complications is generally in the range of 0to 6% [7,1719,25]. In a meta-analysis of minimally invasiveradiofrequency and percutaneous cryotherapy procedures,Hui et al. reported 3.1% of serious complications [5]. Thevarious studies in the literature describe variable statisticalratios between the different tumour parameters and the risk

    of major complications, which can be explained by their lowincidence. In a series of 71 patients with 87 tumours and arate of major complications of 4.6%, Velti et al. found thatan exophytic location played a protective role [25]. Zago-ria et al., in a series of 104 patients with 125 tumours anda rate of major complications of 2.9%, did not report anychanges in the rate of complications related to the loca-tion of the tumour, the patients sex or even the size ofthe lesion [19]. In a series of 24 patients with 32 tumoursand a rate of major complications of 16.6%, Weizer foundthat this rate increased when several tumours were treatedduring the same session [55].

    Thermal lesions ofthe digestive tract

    A major complication to be feared, and specific to hyper-thermic ablation treatments, is the result of thermal injuryto adjacent organs, including the digestive tract. It is rare,with a mean of between 0 and 1% in the series [17,20,48],and can appear with a free interval of several days, threat-ening the life of the patient and requiring emergencysurgical management because of the risk of perforation andseptic complications. The colon, particularly exposed in thecase of upper pole and anterior tumours [55], seems to bemost at risk of thermal injury (Fig. 5). The stomach, probably

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    Radiologically-guided thermal ablation of renal tumours 255

    Figure 7. Infectious complications of thermal ablation: a: radiofrequency ablation of a left lower pole renal mass: pre-treatment coronal

    T1-weighted MRI with injection; b: secondary infection of the ablation zone: CT coronal slice with injection; c: control examination 2 monthsafter antibiotic treatment: T2-weighted MRI (axial slice); d: control examination 2 months after antibiotic treatment: T1-weighted MRI withinjection of contrast agent (comparative axial slice); e: control examination 6 months after antibiotic treatment: T2-weighted MRI (axialslice) showing regression of the infected ablation zone; f: control examination 6 months after antibiotic treatment: T1-weighted MRI withinjection of contrast agent (comparative axial slice).

    because of the thickness of its wall, and the small intes-tine, because of its mobility, are less sensitive to thermaldamage [51]. Preventing thermal injury to adjacent organsis based on the presence of a fatty safety area of at least5 mm [52] which can be artificially increased by reposition-ing the patient or using hydrodissection (exclusively glucoseor sterile water) and/or CO2 dissection [56,57]. In contrast,thermal damage to the liver and spleen is often minor andof no consequence for the patient [51].

    Lesions ofthe urinary tract

    The upper urinary tract is particularly exposed duringtreatment of central tumours by hyperthermic ablationtechniques (Fig. 6), in contrast to cryotherapy, but thesecomplications are rare [51], less than 4% in the litera-ture [17,19,50,55]. In the acute phase, a ureteral injurymay appear as a perforation with formation of a urinoma.The symptoms may appear several months later as ureteralstenosis, with the risk of recurrent urinary tract infections,

    hydronephrosis and impaired renal function, necessitatingfitting of a double J stent, a nephrostomy or a ureteralstent [58]. It is necessary to prevent these complications,particularly for central and lower pole tumours, where theminimum safety distance from the ureter is less than 15 mm,and often requires the use of cryotherapy. However, pre-operative fitting of a ureteral catheter with per-operativepyelocaliceal irrigation using a non-ionic 5% glucose/sterilewater mixture [58] which is not modified by the RF wavescan be discussed. The corollary to preventing pyeloureteralthermal injury by this way is the possible decrease inthe efficacy of the thermal ablation by the heat-sinkeffect.

    Infection

    Despite taking aseptic measures, the risk of infection(Fig. 7) is not negligible, being in the order of 0 to 2%in the series [7,25]. Diabetes increases the risk of sepsis[51].

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    Figure8. Typical appearance in T1-weighted MRI of necrotic-haemorrhagic post-ablation changes: a: spontaneous T1 hypersignal (coronalslice); b: no detectable enhancement after injection in the arterial phase (axial slice); c: no detectable enhancement after injectionin the cortico-medullary phase (axial slice); d: no enhancement on the subtracted sequence (coronal slice). Subtraction sequences arerecommended to detect remnants and in situ recurrences.

    Tumour dissemination

    Studied in radiofrequency ablation, tumour disseminationalong the applicator path is exceptional, as only two cases

    have been reported in the literature [59]. To minimise thisrisk, the electrode must be positioned optimally in a directpath, and the path of the needle should be treated at the endof the procedure; this can also reduce the risk of bleeding[51].

    Surveillance and follow-up imaging

    It is essential for patients to be monitored for remnants orrecurrences. Although a biopsy is the gold standard, it isan invasive procedure, the usefulness of which is controver-sial.

    Normal appearance in imaging

    Monitoring by imaging is nowadays essential. The appear-ance of an ablation site evolves with time in a normal and

    relatively predictable way. Several changes occur, particu-larly the size of the site: a clear increase in the volumeof the site treated by heat ablation appears early in thefollowing week and the first 2 months after the proce-dure, particularly for small tumours of less than 3 cm3

    [60]. Then, the scar volume gradually decreases over 1 to2 years.

    In a CT scan, the density of the treated area, the site ofcoagulation necrosis, is and remains spontaneously denserthan the adjacent renal parenchyma. No contrast uptakecan be identified. However, in a series of 36 radiofrequency-treated tumours, Javadi described significant homoge-neous enhancement, greater than 10 HU, visible in the

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    Radiologically-guided thermal ablation of renal tumours 257

    Figure 9. Typical appearance in a T2-weighted MRI of necrotic-haemorrhagic post-ablation changes: a: exophytic right renal tumour inT1-weighted MRI with injection (axial slice); b: radiofrequency thermal ablation with deployable needle: CT axial scan without injection; c:absence of contrast uptake after injection in the cortical phase in the 2-month control on MRI subtracted sequences; d: absence of contrastuptake after injection in the cortico-medullary phase in the 6-month control on MRI subtracted sequences; e: typical hyposignal from theablation zone, associated with the zones peripheral halo, including the tumour and surrounding treated tissue, defining the therapeutic

    borders during this axial T2 MRI follow-up; f: coronal T2-weighted hyposignal from the ablation zone and peripheral halo.

    parenchymal phase, on a control on D0 of the radiofrequencysites, which improved over time in 78% cases [61].

    In MRI, the treated site is heterogeneous, generally with aT1 hypersignal and a T2 hyposignal without contrast uptake(Figs. 8 and 9). A thin ring of peripheral enhancement canbe seen on late acquisitions throughout follow-up, withno suspicious character, probably related to inflammatorychanges.

    In both CT and MRI, infiltration of peripheral fat is almostsystematic, especially with exophytic tumours [53]. A spon-taneously dense peripheral halo with a T1 hyposignal has

    been reported in nearly 75% of cases; it appears during thefirst months and often persists [62]. Fat invagination into thescar is less common and occurs later [60]. MRI has no partic-ular advantage over CT apart from not requiring injection ofan iodinated contrast agent; it should therefore be preferredin cases of renal impairment.

    As for cryotherapy, there is no precise description of theablation zone, the volume of which tends to decrease overtime; MRI shows a clear T2 hyposignal ring [63].

    Tumour residue and local recurrence

    The presence of focal nodular contrast enhancement is stillthe only validated marker of living residual or recurrent

    tumour tissue and involves acquisition first without injectionof contrast agent and then with this injection.

    In the CT scan, enhancement is evaluated qualita-tively and quantitatively. Any contrast enhancement of theradiofrequency site of more than 10 HU [19] or 15 HU [64]must be considered significant, suggestive of a residual orrecurrent local tumour. Any complication due to local infec-tion may make this analysis difficult.

    In MRI, because of the T1 hypersignal from the ablationsite, subtraction techniques must be widely used to detector eliminate focal enhancement. Quantitatively, enhance-

    ment is considered significant if it exceeds 15% on thedynamic sequence [19,65].Some authors have evaluated the feasibility of contrast-

    enhanced ultrasound (SonoVue, Bracco, Milan, Italy) duringmonitoring, instead of CT or MRI [66], with a possible limitfor hypovascularised and/or deep tumours for which thisexamination may be found wanting as regards detectingliving tumour tissue. This technique is to be preferred inpatients with severe renal impairment, in whom injectionof iodinated or gadolinium chelate contrast agent is con-traindicated.

    There is no recommendation on follow-up in terms ofexamination dates, but there is some consensus in the liter-ature. Follow-up is generally frequent during the first year

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    Figure 10. CT axial slice with injection in the cortical phase. Axial CT scan after injection in the late phase (a) with the deployableradiofrequency needle positioned within the tumour (b). Axial T2-weighted (c) and T1-weighted MRI with injection and subtraction (d),

    during follow-up.following the ablation [67], with three to four examinationsgradually more widely spaced: at 2, 6 and 12 months or at1, 3, 6 and 12 months. An annual follow-up is then recom-mended for 5 years or even longer.

    Nephron-sparing measures

    Sparing the kidney is the objective at the forefront of RCCmanagement. Besides in familial diseases, such as von HippelLindau disease, in which the high frequency of synchronousand metachronous cancer sites requires multiple treatmentwith progressive reduction in kidney reserves, it has been

    shown that progression towards chronic renal disease is asso-ciated with increased mortality [68].

    Many studies agree in demonstrating the absence of sig-nificant impairment of renal function at 1 month and 1year for patients treated for a single tumour [22,25,69].In a series of 242 patients, Lucas observed preservation ofrenal function after radiofrequency and partial nephrectomywhich was significantly higher than for total nephrectomysurgical techniques, with a rate without appearance ofchronic renal impairment after 3 years of 95.2%, 70.7% and39.9% respectively [70].

    Raman compared 47 patients who had had a solitarykidney treated by radiofrequency with 42 treated by open

    partial nephrectomy, with mean tumour sizes of 2.8 and3.9 cm respectively, mean renal function of 46.5 mL/min and55.9 mL/min respectively and mean follow-up of 18.1 and 30months. Decline in renal function was significantly higher inpatients treated with conservative surgery than in patientstreated by radiofrequency, both soon after the procedure(15.8% versus 7.1%), at 12 months (24.5% versus 10.4%) andat the last follow-up (28.6% versus 11.4%; P< 0.001). Theproportion of patients who, during follow-up, developedmoderate (CrCl < 60 mL/min) and severe (CrCl < 30 mL/min)renal impairment was 0% and 7% respectively for patientstreated with radiofrequency as against 35% and 17% where

    treatment had been surgical [71].A recent study [53], reviewing 24 thermal ablations(radiofrequency and cryoablation) on kidney, transplantsshowed no change in renal function following the proce-dures.

    Conclusion

    Apart from the need for large-scale validation of newlydeveloping techniques such as microwaves and focusedultrasound, the long-term results of radiofrequency andcryotherapy ablations need to be confirmed. Nevertheless,

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    Radiologically-guided thermal ablation of renal tumours 259

    given the low morbidity of these techniques and the excel-lent oncological efficacy reported in the management ofkidney tumours of less than 4 cm, enlarging the indicationsto a wider population can be envisaged. Prospective studiescomparing thermal ablation with the reference treatment,which is still surgery, must now be undertaken.

    TAKE-HOMEMESSAGES

    General points on the thermal ablation of renal tumours Thermal ablation techniques can be proposed for

    renal tumours as an alternative to surgery. These techniques are effective, with results

    comparable to those of partial nephrectomy, andthey preserve kidney capital.

    Morbidity is low if precautionary rules are followed,particularly concerning adjacent organs (thedigestive or urinary tract).

    Radiofrequency thermal ablation is simple, effectiveand economical.

    Cryotherapy allows the ablation zone to be

    controlled and appears to be particularly useful fortreating central tumours, as it does not damage thesupporting urothelial tissue.

    Microwave ablation allows larger ablation zones tobe treated.

    The use of focused ultrasound is still to be defined.

    Follow-up after thermal ablation Regular follow-up is necessary (at 2, 6 and 12 months

    during the first year). This may be with ultrasound, CT or MRI. Injection of a contrast agent is required to detect

    remnants or recurrences that are hypervascularised. Interpretation may be hindered by necrotic-

    haemorrhagic changes that give a T1 hypersignaland T2 hyposignal in MRI, and are spontaneouslydense in a CT scan. The T1 hypersignal requiressubtraction sequences to be undertaken afterinjection of a contrast agent in order to detect earlycontrast uptake.

    Clinical case

    This 86-year-old woman presented a 32 mm left renal

    tumour (Fuhrman 2 clear cell carcinoma) (Fig. 10a). Con-sidering the age and general condition of the patient,radiofrequency thermal ablation was decided in a multidis-ciplinary meeting.

    The procedure was performed under CT guidance andgeneral anaesthesia (Fig. 10b) without complication. Thepatient was reassessed by MRI some time after the procedure(Fig. 10c: 1, 2).

    Questions

    1. What follow-up should be proposed after this thermaltreatment?

    2. Is an injection at the time of the examination needed forthis surveillance?

    3. What is your diagnosis and what management, if neces-sary, do you recommend?

    Answers

    1. Follow-up using imaging should be offered systemati-

    cally. The technique used must be adapted to each case,using ultrasound, CT or MRI particularly depending onthe contraindications (especially renal impairment). Ide-ally, the examinations will be performed at 2, 6 and 12months during the first year, then annually if there is norecurrence.

    2. Injection of a contrast agent is essential for identifying aresidual tumour or an in situ recurrence, because imagescontain artefacts due to necrotic- haemorrhagic changessecondary to thermal ablation.

    3. The control MRI shows a T2 hypersignal and above allperipheral uptake of contrast, corresponding to tumourremnants, and not recurrence, for this was detected dur-ing the first follow-up examination and was secondary

    to incomplete treatment (due to the size of the lesionor the technique used). Primary efficacy was not good,therefore, in this case. A new procedure had to be pro-posed as a first course of action, in order to completethe treatment, taking into account the limits of thefirst technique used. Cryotherapy treatment was pro-posed and performed in this patient. Given the efficacyof this second procedure on the control examinations,the secondary efficacy of the thermal treatment over-all (radiofrequency then cryotherapy) was, in the end,good.

    Disclosure of interestThe authors declare that they have no conflicts of interestconcerning this article.

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