I. Introduction
The American Cancer Society, (2004) estimates over
18,000 cases of primary liver cancer will be diagnosed United States in 2004,
of which over one-half are hepatocellular carcinoma. Hepatocellular carcinoma
(HCC) is one of the most prevalent solid cancers worldwide, especially in East
Asia and South Africa, with over one million new cases annually (Qin and Tang,
2002). The liver also is a common site of metastasis, particularly from
colorectal cancer (Weiss et al, 1986). Surgical resection is remains the
treatment of choice for patients with hepatic malignancies, with contemporary
series demonstrating 5-year survival rates of 25% to 40% for both colorectal
malignancies (Sugihara et al, 1993; Rees et al, 1997; Fong et al, 1999) and HCC
(Vauthey et al, 1995; Hanazaki et al, 2000; Poon et al, 2000; Ercolani et al,
2003). However, the majority of patients with liver tumors are not candidates
for resection due to tumor size, location, multifocality, inadequate liver
reserve, and other health problems (Nagorney et al, 1989).
The treatment options for patients with unresectable
hepatic tumors include systemic chemotherapy, chemoembolization, and locally
ablative techniques (including ethanol ablation, cryoablation, and
radiofrequency, laser or microwave ablation). Results for systemic chemotherapy
have been abysmal for HCC, with short median survivals and low response rates
(Friedman, 1983; Lin et al, 1997; Patt et al, 2003). Additionally, the presence
of cirrhosis often limits the cytotoxic agents available for treatment. Recently,
progress in systemic chemotherapy for metastatic colorectal cancer has resulted
in increased response rates and modest increases in median survival, but still
there are few long-term survivors (Conti et al, 1996; Bajetta et al, 2004;
Cunningham et al, 2004). For HCC or other hypervascular tumors, embolization or
chemoembolization may provide hepatic disease control for patients that are
neither resectable nor appropriate for transplantation (Llovet et al, 2002; Lo
et al, 2002; OÕSuilleabhain et al, 2003).
There are several ablative therapies available for
treatment of unresectable hepatic tumors. Percutaneous ethanol injection (PEI)
can be effective for small HCC tumors, but usually requires multiple treatments
(Lencioni et al, 1997). PEI has been shown to be an effective alternative to
resection, but is most beneficial in patients with adequate hepatic function
and small, well-circumscribed tumors (Mazzanti et al, 2004). PEI has limited
effects on colorectal metastases and non-vascular tumors. PEI may be combined
with other cytotoxic agents to enhance tumor cell kill (Kurokohchi et al,
2004). Cryoablation has been used for a number of malignant liver tumors,
however may be associated with a complication rate that is higher than some
other ablative techniques (Sohn et al, 2003). The Òheat sinkÓ effect may limit
the efficacy of cryoablation of tumor located near large hepatic blood vessels.
The complication rate and the local recurrence rate have made cryoablation less
attractive than other ablative therapies (Adam et al, 2002; Kerkar et al,
2004).
Currently, the most widely
used hepatic ablative strategies are the thermal ablative techniques of
radiofrequency ablation (RFA), laser-induced thermotherapy (LITT), and
microwave ablation (MA). These techniques share a common method for inducing
tumor killing: they heat the tumor resulting in coagulative necrosis. Thermal
ablative techniques result in permanent cellular damage and death by achieving
temperatures above 50¡
to 60¡C
(McGahan et al, 1992; Patterson et al, 1998). These three techniques appear
promising for the future treatment of liver malignancies because they may be
used in a minimally invasive setting, are relatively inexpensive, versatile,
and have acceptably low rates of morbidity and mortality.
II. Radiofrequency ablation
RFA was first mentioned as a treatment for hepatic
malignancies in 1990 by McGahan and Rossi. Since then, the popularity of RFA as
a viable treatment for unresectable HCC and hepatic metastases has increased
exponentially, mainly due to the techniqueÕs versatility and effectiveness. RFA
can be employed in a number of ways: through traditional open surgery,
laparoscopically, or percutaneously under guidance of ultrasound, computed
tomography (CT), or magnetic resonance imaging (MRI). RFA needle electrode
probes release high-frequency (460 kHz) alternating current into the target
tissue. The ions in the tissue are frictionally heated as they attempt to
change direction with the alternating current. After frictional heating rises above
50¡ to 60¡C,
the tissue surrounding the probe forms an area of necrosis as the cells die.
RFA systems include an electrical generator, grounding
pads, and needle electrodes (ranging from 14-gauge to 19-gauge). Three
companies currently market commercially available RFA devices in the United
States: Rita Medical Systems of Mountain View, CA (Mountain View, CA),
Radiotherapeutics (Mountain View, CA) and Radionics (Burlington, MA) (McGhana,
2001; Wong et al, 2001). It is presently unclear whether any system is superior
to another in terms of ablation size, reproducibility, or local tumor control
(de Baere et al, 2001).
Grounding pads are placed on the patientÕs thighs
prior to an RFA procedure. The needle electrode is advanced into the liver
tumor either by an open, laparoscopic, or percutaneous approach, and
ultrasound-guidance is used to position the electrode accurately. The RFA
generator will heat the tissue and maintain the desired temperature by changing
the power output over time. Once the ablation is complete, the electrode is
generally removed slowly while the track is cauterized to prevent tumor seeding
and minimize bleeding. Multiple overlapping ablations may be required for
larger tumors. A successfully ablated lesion should have a region of complete
necrosis encompassing the entire tumor and 1 cm of the surrounding normal
hepatic parenchyma.
The cooling effect of large vessels in close proximity
to the electrode creates a heat sink, which limits the size of the ablation
zone and can cause irregularly shaped ablations. Inflow occlusion during the
ablation may help to mitigate this problem, and can result in larger areas of
ablation, as well as aid in ablating tumors abutting large blood vessels.
Occlusion of the hepatic inflow by the Pringle maneuver has been shown in
several studies to increase the size and regularity of ablations and possibly
to enhance tumor kill (Chinn et al, 2001; Chang et al, 2002; Yamasaki et al,
2002).
In addition to its utility in the initial placement of
the electrode, ultrasonography can be used to monitor the progression of the
ablation during the procedure. Ablated areas become hyperechoic due to gas
bubbles generated by the heated tissue. Gas bubbles generated by an ablation
may interfere with accurate ultrasonography of tissues deep to the electrode,
which can hinder repositioning of the electrode for overlapping ablation zones
when treating larger tumors. Ablating the deepest portions of the tumor first
and re-deploying the electrode serially as it is withdrawn may obviate this
phenomenon. Imaging-related difficulties may be more pronounced with the
percutaneous approach, as transcutaneous ultrasound may not be as accurate as
intra-operative ultrasonography.
Percutaneous RFA is the least invasive mode of
delivery, and can be performed in an outpatient setting, making it an
acceptable alternative for many patients. Laparoscopic RFA has the advantages
of providing more accurate cancer staging using laparoscopy and laparoscopic
ultrasound and minimizing the probability of injury to nearby organs, while
still being minimally invasive. The advantages of an open approach to RFA
include excellent cancer staging, accessibility to all sections of the liver,
ease of intra-operative ultrasound examination, inflow occlusion (Pringle maneuver),
minimal risk to peripheral organs, and the ability to perform a resection in
conjunction with the ablation. The main disadvantage is its invasiveness, which
leads to recovery time, and length of hospital stay (Machi et al, 2001).
Whether RFA should be performed percutaneously,
laparoscopically, or via an open approach should be individualized for each
patient. Percutaneous RFA is well suited for patients who have a limited number
of small tumors and who are not good candidates for more invasive procedures
due to co-morbid conditions. Cirrhotic patients with a small hepatocellular
carcinomas and patients with one or two intrahepatic recurrences following
hepatectomy are good examples of patients who might be best served by the
percutaneous approach. Laparoscopic RFA is a good option for patients with a
small number of tumors for which percutaneous RFA would not be safe, such as
peripherally situated tumors near adjacent organs such as the stomach or colon.
Patients may recover more quickly from a laparoscopic RFA as opposed to an open
RFA, yet substantial surgical judgment must be used in selecting patients for
which the laparoscopic approach is best. Open surgical RFA is preferable for
patients with large tumors, multiple tumors, and tumors near large blood
vessels (because of heat sink effect). Hepatic inflow occlusion diminishes the
heat sink effect from large intrahepatic vessels, and is easier with open
surgery as opposed to laparoscopic surgery. Additionally, the open approach
allows extremely accurate intra-operative ultrasound to be done, which
facilitates ablation of large tumors near blood vessels (Figure 1). Peripherally situated tumors may be safely ablated by
packing the adjacent organs away from the liver, thus providing a layer of
protection difficult to achieve with the other approaches.
Multiple
studies about RFA of hepatic malignancies have been published since 1990;
however, many of these studies are not well controlled in respect to patient
selection, type of cancer, stage of disease, and treatment approach. The high
variability of patients in each study make definitive conclusions difficult,
but the results do point strongly toward RFA being an effective tool against
hepatic malignancies. One concern for all of the ablative techniques has been
local failure. An analysis of several of the larger RFA trials shows local
recurrence per ablated tumor to range from 1.8% to 26.6% and overall recurrence
(outside the ablation zone) to range from 18% to 73.3% (Curley et al, 1999,
2000; Rossi et al, 2000; Bowles et al, 2001; Wong et al, 2001; Kuvshinoff and
Ota, 2002; Jiang et al, 2002; Kosari et al, 2002; Bleicher et al, 2003;
Komorizono et al, 2003) (Table 1). In a large trial conducted at the M.
D. Anderson Cancer Center, Abdalla
Figure 1. (A) CT
demonstrating 2 hepatic metastases from an obstructing right colon
adenocarcinoma. (B) Post-RFA CT
demonstrating complete ablation of metastatic disease.
and
colleagues (Abdalla et al, 2004) compared recurrence and survival between
patients with colorectal cancer metastases treated with resection, resection
and RFA, RFA alone, or chemotherapy alone (including some patients treated with
hepatic infusional therapy). Overall and liver-only recurrences were more
common following RFA compared to resection. Indeed, the liver-only failure rate
was a full four-fold higher for ablated patients as opposed to resected
patients (Abdalla et al, 2004). While this increased recurrence rate likely
reflects the higher risk among unresectable patients because of a greater
number of tumors and other factors, it supports the generally accepted notion
that patients with resectable tumors should undergo resection, rather than
ablation, whenever possible (Machi et al, 2001).
Tumor size has been shown to be an important factor
affecting the rate of local recurrence following RFA (Wood et al, 2000; Machi
et al, 2001; Chan et al, 2002; Kosari et al, 2002; Kuvshinoff and Ota, 2002;
Bleicher et al, 2003). Machi et al, (2001), Kuvshinoff and Ota, (2002) and
Kosari et al, (2002) all noted significantly higher risk for local recurrence
for tumors > 4 cm in greatest diameter. Interestingly, Machi (2001)
also associated higher local recurrence rates with metastatic tumors than with
primary hepatomas. Some studies have also shown that the approach chosen for
delivery of RFA (open, laparoscopic, or percutaneous) may impact local
recurrence. Kuvshinoff and Ota, (2002) and Scaife and Curley, (2003) showed
lower rates of local recurrence for open and laparoscopic RFA versus a
percutaneous approach. The increased access to the liver and use of
intra-operative ultrasound are likely the main reasons for lower local
recurrence rates for operative RFA.
The complication rate associated with RFA is quite
acceptable, ranging from 2.4% to 27% in several trials (Curley et al, 1999,
2000; Bowles et al, 2001; Wong et al, 2001; Jiang et al, 2002; Iannitti et al,
2002; Kosari et al, 2002; Kuvshinoff and Ota, 2002; Bleicher et al, 2003;
Komorizono et al, 2003), (Table 1). In a large review by Scaife and Curley,
(2003) reported an overall mortality rate of 0.5%, a major complication rate of
2%, and a minor complication rate of 6% by combining over 1300 patients from18
different studies. The complications following RFA include wound infections,
intra-abdominal abscess, renal failure, hepatic abscess, biliary injury,
pleural effusion, fever, pain, and minor hemorrhage. RFA-associated morbidity,
mortality, and local recurrence are low enough to justify its use for
unresectable liver tumors.
In non-randomized studies, the available evidence
suggests that RFA extends survival. As with other hepatic directed therapies,
recurrence either in unablated areas of the liver or in other organs is common,
even in the absence of local recurrence (Curley et al, 1999, 2000; Wood et al,
2000; Kosari et al, 2002). Kosari et al, (2002) reported distant failure in 51%
of the patients following RFA and local failure in only 1.8% of the hepatic
malignancies ablated, but new hepatic or systemic disease still developed in
27.6% of patients at a median follow-up of 15 months. These high figures for
distant failure suggest that RFA may best improve long-term survival when
combined with other systemic and
intra-hepatic treatments. Some studies have now reported overall survival
statistics after RFA with moderate follow-up time. Solbiati et al, (2001)
reported overall survival to be 93%, 62%, and 41% at one, two, and three years,
respectively. Iannitti et al, (2002) reported overall survival for patients
with colorectal metastases treated with RFA to be 87%, 77%, and 50% at one,
two, and three years, respectively. They also reported 92%, 75%, and 60%
overall survival rates at one, two, and three years, respectively for patients
with HCC treated with RFA (Iannitti et al, 2002). When compared to liver
resection, however, RFA clearly benefits patients less, with four-year survival
of 22% as compared to 65% for resection (Abdalla et al, 2004). Survival for
unresectable patients with colorectal cancer metastases is better following RFA
than with nonsurgical treatments (Abdalla et al, 2004).
III. Laser-induced thermotherapy
Laser-induced thermotherapy (LITT) is another
non-resectional therapy that has been used to treat liver malignancies. LITT,
like other thermal ablative techniques, kills tumors by raising the temperature
above 55¡ to 60¡
C. LITT uses photons from a low-intensity laser, which are absorbed by natural
molecular chromophores in all human cells and converted into heat (Izzo, 203).
Diode lasers (wavelength 800-980 nm) or N-YAG lasers (wavelength 1064 nm)
operating at low energy generate zones of ablation during LITT (Germer et al,
1998; Muralidharan and Christophi, 2001). Similar to RFA, LITT can be combined
with blood flow occlusion and multiple overlapping laser applications to
increase the volume of ablation (Heisterkamp et al, 1997; Sturesson et al,
1997). Placing multiple laser fibers into the target tissue may create
overlapping zones of ablation (Ivarsson et al, 1998). LITT has the same indications
as RFA: unresectable primary and secondary liver tumors, and like RFA, can be
performed by percutaneous, laparoscopic, or open surgical approaches.
LITT application kits used for percutaneous procedures
include a cannulation needle with a tetragonally sharpened tip, a guide wire,
and a sheath system. The catheter aids in easy removal of the laser fibers and
prevents direct contact between the fibers and the treated tissue. The
applicator has magnetic markers on it that allow the use of MR-guidance for
precise placement. The laser is transmitted via an optical fiber cable that is
placed in the desired treatment area by advancing it through the applicator
system (Vogl et al, 2001).
One of the main advantages of LITT is its
compatibility with MR-guidance. It does not interfere with MR-imaging like RFA
and microwave ablation. Ultrasound or CT may be used for tumor targeting and
placement of the laser fibers, followed by MR imaging of the ablation.
Alternatively, intraoperative MRI can provide precise targeting and ablation in
a single unit. MR imaging provides increased lesion visibility,
three-dimensional laser navigation, and allows monitoring of temperature
changes and tissue coagulation (Vogl et al, 1995; Dick et al 2003a, b).
Real-time temperature monitoring is a notable advantage because it allows the
clinician to assure temperatures are high enough in the tumor for a successful
ablation and low enough in surrounding tissue to minimize collateral damage.
However, present limitations of MRI thermal mapping have precluded this
technique from widespread acceptance.
There have been even fewer large-scale studies of LITT
than of RFA (Heisterkamp et al, 1999). In one large European study, Mack et al,
(2001) treated liver tumors with LITT and demonstrated impressive local control
rates, survival data, and low morbidity. They used MR-guided LITT and reported
results for 1981 lesions in 705 patients, including 97.9% local tumor control
at 6 months, 93% one-year survival, 74% two-year survival, 50% three-year survival,
30% five-year survival, and only a 7.5% rate of complications. In a study of 74
patients with single tumors < 4 cm or one to three tumors <
3 cm in greatest dimension, Pacella et al, (2001) reported a 6% local
recurrence rate and overall survival rates of 99%, 95%, 68%, and 15% at one,
two, three, and five years, respectively. An analysis of the complications
associated with the LITT in 899 patients with 2520 lesions concluded that the
procedure had an acceptably low morbidity (Vogl et al, 2002). It remains to be
seen whether other centers can duplicate these intriguing results; however, the
results of these authors are encouraging and warrant further study.
IV. Microwave ablation
Microwave ablation developed out of technology first
used for hemostasis and coagulation during hepatic resection (Tabuse and
Katsumi, 1981; Tabuse et al, 1986). It has since been adapted and used to treat
small HCC tumors in the liver and has been most extensively studied in Japan
for the treatment of patients with cirrhotic HCC lesions. Microwaves create
dielectric heat in tissue and cells by stimulating tissue water molecules,
which leads to frictional heating and necrosis in a similar manner to RFA and
LITT (Izzo, 2003). MA can be applied percutaneously, laparoscopically, or as an
open surgical procedure. Indications for MA include unresectable hepatic
malignancies and patients not suited for major hepatectomy. The needle
electrode is advanced directly into the tumor under ultrasound guidance and
microwave emission commences. As with the other thermal ablative techniques,
multiple overlapping zones of ablation are created to ablate larger tumors.
Newer antenna designs, including looping coils may allow for more precise
geometric ablation zones to be created with shorter treatment times (Wright et
al, 2003; Shock et al, 2004). Our initial experience in a cohort of 20 patients
with a multiple antennae MA system (Vivant Medical, Mountain View, CA) has been
very favorable; this system allows ablation of multiple tumors at the same
time, large (5 to 7 cm) ablation zones, complete tumor ablation, rapid ablation
times (5 to 10 minutes maximum), and does not require grounding pads that can
potentially result in skin burns such as in RFA systems (Martin et al,
unpublished data).
There are few studies on MA with data on local
recurrence and complications following treatment, and most of the studies that
have been published have reported small numbers of patients. One study
involving 19 patients with 31 tumors (mean tumor size 2.1 cm). reported 9.7%
local recurrence per tumor (Sato et al, 1996). Microwave ablation has been
shown to be a valid treatment option in cirrhotic patients with HCC. Local
failure rates are similar to those seen with the other thermal ablative
techniques (Xu et al, 2004). In a large study by Dong et al, (Dong et al, 2003)
234 patients with 339 HCC tumors were treated percutaneously with MA. Survival
rates of 92% were seen at one year, and long-term survival at five years of
56.7% was reported (Dong et al, 2003). The majority (88.5%) of the patients
were ChildÕs class B cirrhotics. There were no perioperative deaths and very
few minor complications, indicating this is a safe technique, even in patients
with severe comorbid conditions (Dong et al, 2003).
V. Conclusion
The past several years have
seen rapid advances in the treatment of patients with liver tumors. Thermal
ablative techniques have become a valid treatment option for patients with
unresectable liver tumors and for patients whose underlying disease state or
physical condition will not permit a hepatectomy. Resection remains the
treatment of choice for liver malignancies; however, most patients have tumors
that are not resectable. RFA, LITT, and MA appear to be safe, effective
treatments for such patients. The available evidence from non-randomized
studies suggests that, given the limited efficacy of systemic therapy, the
ability to completely ablate liver tumors extends survival. The range of
thermal ablation approaches also permits minimally invasive treatment of
recurrence in the liver following resection or ablation. Further study is
necessary to demonstrate conclusively the survival benefit of thermal ablation,
to aid in patient selection for various approaches, and to determine the most
effective ablation systems and techniques. With improvements in the technology,
it also remains to be determined whether thermal ablation can replace resection
in selected patients.
References
Abdalla EK, Vauthey JN, Ellis
LM, Ellis V, Pollock R, Broglio KR, Hess K, Curley SA (2004)
Recurrence and outcomes following hepatic resection, radiofrequency ablation,
and combined resection/ablation for colorectal liver metastases. Ann Surg 239, 818-825.
Adam R, Hagopian EJ, Linhares
M, Krissat J, Savier E, Azoulay D, Kunstlinger F, Castaing D, Bismuth H (2002) A comparison of percutaneous
cryosurgery and percutaneous radiofrequency for unresectable hepatic
malignancies. Arch Surg 137,
1332-1339.
American Cancer Society.(2004) Cancer Facts and Figures. 1-58. 2004.
Bajetta E, Beretta E, Di
Bartolomeo M, Cortinovis D, Ferrario E, Dognini G, Toffolatti L, Buzzoni R (2004) Efficacy of treatment with
irinotecan and oxaliplatin combination in FU-resistant metastatic colorectal
cancer patients. Oncology 66,
132-137.
Bleicher RJ, Allegra DP, Nora
DT, Wood TF, Foshag LJ, Bilchik AJ (2003)
Radiofrequency ablation in 447 complex unresectable liver tumors, lessons
learned. Ann Surg Oncol 10, 52-58.
Bowles BJ, Machi J, Limm WM,
Severino R, Oishi AJ, Furumoto NL, Wong LL, Oishi RH (2001) Safety and efficacy of radiofrequency thermal ablation in
advanced liver tumors. Arch Surg
136, 864-869.
Chan RP, Asch M, Kachura J,
Ho CS, Greig P, Langer B, Sherman M, Wong F, Feld R, Gallinger S (2002) Radiofrequency ablation of
malignant hepatic neoplasms. Can Assoc
Radiol J 53, 272-278.
Chang CK, Hendy MP, Smith JM,
Recht MH, Welling RE (2002) Radiofrequency
ablation of the porcine liver with complete hepatic vascular occlusion. Ann Surg Oncol 9, 594-598.
Chinn SB, Lee FT, Jr.,
Kennedy GD, Chinn C, Johnson CD, Winter TC, III, Warner TF, Mahvi DM (2001) Effect of vascular occlusion on
radiofrequency ablation of the liver, results in a porcine model. AJR Am J Roentgenol 176, 789-795.
Conti JA, Kemeny NE, Saltz
LB, Huang Y, Tong WP, Chou TC, Sun M, Pulliam S, Gonzalez C (1996) Irinotecan is an active agent in
untreated patients with metastatic colorectal cancer. J Clin Oncol 14, 709-715.
Cunningham D, Humblet Y,
Siena S, Khayat D, Bleiberg H, Santoro A, Bets D, Mueser M, Harstrick A,
Verslype C, Chau I, Van Cutsem E (2004) Cetuximab
monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic
colorectal cancer. N Engl J Med 351,
337-345.
Curley SA, Izzo F, Delrio P,
Ellis LM, Granchi J, Vallone P, Fiore F, Pignata S, Daniele B, Cremona F (1999) Radiofrequency ablation of
unresectable primary and metastatic hepatic malignancies, results in 123
patients. Ann Surg 230, 1-8.
Curley SA, Izzo F, Ellis LM,
Nicolas Vauthey J, Vallone P (2000) Radiofrequency
ablation of hepatocellular cancer in 110 patients with cirrhosis. Ann Surg 232, 381-91.
de Baere T, Denys A, Wood BJ,
Lassau N, Kardache M, Vilgrain V, Menu Y, Roche A.(2001) Radiofrequency liver ablation, experimental comparative
study of water-cooled versus expandable systems. AJR Am J Roentgenol 176, 187-192.
Dick EA, Joarder R, de Jode
M, Taylor-Robinson SD, Thomas HC, Foster GR, Gedroyc WM (2003a) MR-guided laser thermal ablation of primary and secondary
liver tumours. Clin Radiol 58,
112-120.
Dick EA, Wragg P, Joarder R,
de Jode M, Lamb G, Gould S, Gedroyc WM (2003b)
Feasibility of abdomino-pelvic T1-weighted real-time thermal mapping of
laser ablation. J Magn Reson Imaging
17, 197-205.
Dong B, Liang P, Yu X, Su L,
Yu D, Cheng Z, Zhang J (2003) Percutaneous
sonographically guided microwave coagulation therapy for hepatocellular
carcinoma, results in 234 patients. AJR
Am J Roentgenol 180, 1547-1555.
Ercolani G, Grazi GL,
Ravaioli M, Del Gaudio M, Gardini A, Cescon M, Varotti G, Cetta F, Cavallari A
(2003) Liver resection for
hepatocellular carcinoma on cirrhosis, univariate and multivariate analysis of
risk factors for intrahepatic recurrence. Ann
Surg 237, 536-543.
Fong Y, Fortner J, Sun RL,
Brennan MF, Blumgart LH (1999) Clinical
score for predicting recurrence after hepatic resection for metastatic colorectal
cancer, analysis of 1001 consecutive cases. Ann Surg 230, 309-18.
Friedman MA (1983) Primary hepatocellular
cancer--present results and future prospects. Int J Radiat Oncol Biol Phys 9, 1841-1850.
Germer CT, Albrecht D, Roggan
A, Buhr HJ (1998) Technology for in
situ ablation by laparoscopic and image-guided interstitial laser hyperthermia.
Semin Laparosc Surg 5, 195-203.
Hanazaki K, Kajikawa S,
Shimozawa N, Mihara M, Shimada K, Hiraguri M, Koide N, Adachi W, Amano J (2000) Survival and recurrence after
hepatic resection of 386 consecutive patients with hepatocellular carcinoma. J Am Coll Surg 191, 381-388.
Heisterkamp J, van
Hillegersberg R, Mulder PG, Sinofsky EL, IJzermans JN (1997) Importance of eliminating portal flow to produce large
intrahepatic lesions with interstitial laser coagulation. Br J Surg 84, 1245-1248.
Heisterkamp J, van
Hillegersberg R, IJzermans JN (1999)
Interstitial laser coagulation for hepatic tumours. Br J Surg 86, 293-304.
Iannitti DA, Dupuy DE,
Mayo-Smith WW, Murphy B (2002) Hepatic
radiofrequency ablation. Arch Surg
137, 422-426.
Ivarsson K, Olsrud J,
Sturesson C, Moller PH, Persson BR, Tranberg KG (1998) Feedback interstitial diode laser (805 nm) thermotherapy
system, ex vivo evaluation and mathematical modeling with one and four-fibers. Lasers Surg Med 22, 86-96.
Izzo F (2003) Other thermal ablation techniques, microwave and interstitial
laser ablation of liver tumors. Ann Surg
Oncol 10, 491-497.
Jiang HC, Liu LX, Piao DX, Xu
J, Zheng M, Zhu AL, Qi SY, Zhang WH, Wu LF (2002) Clinical short-term results of radiofrequency ablation in
liver cancers. World J Gastroenterol 8,
624-630.
Kerkar S, Carlin AM, Sohn RL,
Steffes C, Tyburski J, Littrup P, Weaver D (2004) Long-term follow up and prognostic factors for cryotherapy of
malignant liver tumors. Surgery 136,
770-779.
Komorizono Y, Oketani M, Sako
K, Yamasaki N, Shibatou T, Maeda M, Kohara K, Shigenobu S, Ishibashi K, Arima T
(2003) Risk factors for local
recurrence of small hepatocellular carcinoma tumors after a single session, single
application of percutaneous radiofrequency ablation. Cancer 97, 1253-1262.
Kosari K, Gomes M, Hunter D,
Hess DJ, Greeno E, Sielaff TD (2002) Local,
intrahepatic, and systemic recurrence patterns after radiofrequency ablation of
hepatic malignancies. J Gastrointest
Surg 6, 255-263.
Kurokohchi K, Masaki T,
Miyauchi Y, Funaki T, Yoneyama H, Miyoshi H, Yoshida S, Himoto T, Morishita A,
Uchida N, Watanabe S, Kuriyama S (2004) Percutaneous
ethanol and lipiodol injection therapy for hepatocellular carcinoma. Int J Oncol 24, 381-387.
Kuvshinoff BW, Ota DM (2002) Radiofrequency ablation of liver
tumors, influence of technique and tumor size. Surgery 132, 605-611.
Lencioni R, Pinto F,
Armillotta N, Bassi AM, Moretti M, Di Giulio M, Marchi S, Uliana M, Della CS,
Lencioni M, Bartolozzi C (1997)
Long-term results of percutaneous ethanol injection therapy for hepatocellular
carcinoma in cirrhosis, a European experience. Eur Radiol 7, 514-519.
Lin DY, Lin SM, Liaw YF (1997) Non-surgical treatment of
hepatocellular carcinoma. J
Gastroenterol Hepatol 12, S319-S328.
Llovet JM, Real MI, Montana
X, Planas R, Coll S, Aponte J, Ayuso C, Sala M, Muchart J, Sola R, Rodes J,
Bruix J (2002) Arterial embolisation
or chemoembolisation versus symptomatic treatment in patients with unresectable
hepatocellular carcinoma, a randomised controlled trial. Lancet 359, 1734-1739.
Lo CM, Ngan H, Tso WK, Liu
CL, Lam CM, Poon RT, Fan ST, Wong J (2002)
Randomized controlled trial of transarterial lipiodol chemoembolization for
unresectable hepatocellular carcinoma. Hepatology
35, 1164-1171.
Machi J, Uchida S, Sumida K,
Limm WM, Hundahl SA, Oishi AJ, Furumoto NL, Oishi RH (2001) Ultrasound-guided radiofrequency thermal ablation of liver
tumors, percutaneous, laparoscopic, and open surgical approaches. J Gastrointest Surg 5, 477-489.
Mack MG, Straub R, Eichler K,
Engelmann K, Zangos S, Roggan A, Woitaschek D, Bottger M, Vogl TJ (2001) Percutaneous MR imaging-guided
laser-induced thermotherapy of hepatic metastases. Abdom Imaging 26, 369-374.
Mazzanti R, Arena U, Pantaleo
P, Antonuzzo L, Cipriani G, Neri B, Giordano C, Lanini F, Marchetti S,
Gentilini P (2004) Survival and
prognostic factors in patients with hepatocellular carcinoma treated by
percutaneous ethanol injection, A 10-year experience. Can J Gastroenterol 18, 611-618.
McGahan JP, Browning PD,
Brock JM, Tesluk H (1990) Hepatic
ablation using radiofrequency electrocautery. Invest Radiol 25, 267-270.
McGahan JP, Brock JM, Tesluk
H, Gu WZ, Schneider P, Browning PD (1992)
Hepatic ablation with use of radio-frequency electrocautery in the animal
model. J Vasc Interv Radiol 3,
291-297.
McGhana JP, Dodd GD, III (2001) Radiofrequency ablation of the
liver, current status. AJR Am J
Roentgenol 176, 3-16.
Muralidharan V, Christophi C
(2001) Interstitial laser
thermotherapy in the treatment of colorectal liver metastases. J Surg Oncol 76, 73-81.
Nagorney DM, Van Heerden JA,
Ilstrup DM, Adson MA (1989) Primary
hepatic malignancy, surgical management and determinants of survival. Surgery 106, 740-748.
O'Suilleabhain CB, Poon RT,
Yong JL, Ooi GC, Tso WK, Fan ST (2003) Factors
predictive of 5-year survival after transarterial chemoembolization for
inoperable hepatocellular carcinoma. Br
J Surg 90, 325-331.
Pacella CM, Bizzarri G,
Magnolfi F, Cecconi P, Caspani B, Anelli V, Bianchini A, Valle D, Pacella S,
Manenti G, Rossi Z (2001) Laser
thermal ablation in the treatment of small hepatocellular carcinoma, results in
74 patients. Radiology 221, 712-720.
Patt YZ, Hassan MM, Lozano
RD, Brown TD, Vauthey JN, Curley SA, Ellis LM (2003) Phase II trial of systemic continuous fluorouracil and
subcutaneous recombinant interferon Alfa-2b for treatment of hepatocellular
carcinoma. J Clin Oncol 21, 421-7.
Patterson EJ, Scudamore CH,
Owen DA, Nagy AG, Buczkowski AK (1998) Radiofrequency
ablation of porcine liver in vivo, effects of blood flow and treatment time on
lesion size. Ann Surg 227, 559-565.
Poon RT, Fan ST, Ng IO, Lo
CM, Liu CL, Wong J (2000) Different
risk factors and prognosis for early and late intrahepatic recurrence after
resection of hepatocellular carcinoma. Cancer
89, 500-507.
Qin LX, Tang ZY (2002) The prognostic significance of
clinical and pathological features in hepatocellular carcinoma. World J Gastroenterol 8, 193-199.
Rees M, Plant G, Bygrave S (1997) Late results justify resection
for multiple hepatic metastases from colorectal cancer. Br J Surg 84, 1136-1140.
Rossi S, Fornari F, Pathies
C, Buscarini L (1990) Thermal
lesions induced by 480 KHz localized current field in guinea pig and pig liver.
Tumori 76, 54-57.
Rossi S, Garbagnati F,
Lencioni R, Allgaier HP, Marchiano A, Fornari F, Quaretti P, Tolla GD, Ambrosi
C, Mazzaferro V, Blum HE, Bartolozzi C (2000)
Percutaneous radio-frequency thermal ablation of nonresectable
hepatocellular carcinoma after occlusion of tumor blood supply. Radiology 217, 119-126.
Sato M, Watanabe Y, Ueda S,
Iseki S, Abe Y, Sato N, Kimura S, Okubo K, Onji M (1996) Microwave coagulation therapy for hepatocellular carcinoma. Gastroenterology 110, 1507-1514.
Scaife CL, Curley SA (2003) Complication, local recurrence,
and survival rates after radiofrequency ablation for hepatic malignancies. Surg Oncol Clin N Am 12, 243-255.
Shock SA, Meredith K, Warner
TF, Sampson LA, Wright AS, Winter TC, III, Mahvi DM, Fine JP, Lee FT, Jr (2004) Microwave ablation with loop
antenna, in vivo porcine liver model. Radiology
231, 143-149.
Sohn RL, Carlin AM, Steffes
C, Tyburski JG, Wilson RF, Littrup PJ, Weaver DW (2003) The extent of cryosurgery increases the complication rate
after hepatic cryoablation. Am Surg
69, 317-322.
Solbiati L, Livraghi T,
Goldberg SN, Ierace T, Meloni F, Dellanoce M, Cova L, Halpern EF, Gazelle GS (2001) Percutaneous radio-frequency
ablation of hepatic metastases from colorectal cancer, long-term results in 117
patients. Radiology 221, 159-166.
Sturesson C, Liu DL, Stenram
U, Andersson-Engels S (1997) Hepatic
inflow occlusion increases the efficacy of interstitial laser-induced
thermotherapy in rat. J Surg Res 71,
67-72.
Sugihara K, Hojo K, Moriya Y,
Yamasaki S, Kosuge T, Takayama T (1993) Pattern
of recurrence after hepatic resection for colorectal metastases. Br J Surg 80, 1032-1035.
Tabuse K, Katsumi M (1981) Application of a microwave tissue
coagulator to hepatic surgery the hemostatic effects on spontaneous rupture of
hepatoma and tumor necrosis. Nippon Geka
Hokan 50, 571-579.
Tabuse K, Katsumi M,
Kobayashi Y, Noguchi H, Egawa H, Aoyama O, Kim H, Nagai Y, Yamaue H, Mori K (1985) Microwave surgery, hepatectomy
using a microwave tissue coagulator. World
J Surg 9, 136-143.
Vauthey JN, Klimstra D,
Franceschi D, Tao Y, Fortner J, Blumgart L, Brennan M (1995) Factors affecting long-term outcome after hepatic resection
for hepatocellular carcinoma. Am J Surg
169, 28-34.
Vogl TJ, Muller PK,
Hammerstingl R, Weinhold N, Mack MG, Philipp C, Deimling M, Beuthan J, Pegios
W, Riess H (1995) Malignant liver
tumors treated with MR imaging-guided laser-induced thermotherapy, technique
and prospective results. Radiology
196, 257-265.
Vogl TJ, Eichler K, Straub R,
Engelmann K, Zangos S, Woitaschek D, Bottger M, Mack MG (2001) Laser-induced thermotherapy of malignant liver tumors,
general principals, equipment(s), procedure(s)--side effects, complications and
results. Eur J Ultrasound 13,
117-127.
Vogl TJ, Straub R, Eichler K,
Woitaschek D, Mack MG (2002) Malignant
liver tumors treated with MR imaging-guided laser-induced thermotherapy,
experience with complications in 899 patients (2,520 lesions). Radiology 225, 367-377.
Weiss L, Grundmann E,
Torhorst J, Hartveit F, Moberg I, Eder M, Fenoglio-Preiser CM, Napier J, Horne
CH, Lopez MJ (1986) Haematogenous
metastatic patterns in colonic carcinoma, an analysis of 1541 necropsies. J Pathol 150, 195-203.
Wong SL, Edwards MJ, Chao C,
Simpson D, McMasters KM (2001) Radiofrequency
ablation for unresectable hepatic tumors. Am
J Surg 182, 552-557.
Wood TF, Rose DM, Chung M,
Allegra DP, Foshag LJ, Bilchik AJ (2000)
Radiofrequency ablation of 231 unresectable hepatic tumors, indications,
limitations, and complications. Ann Surg
Oncol 7, 593-600.
Wright AS, Lee FT, Jr., Mahvi
DM (2003) Hepatic microwave ablation
with multiple antennae results in synergistically larger zones of coagulation
necrosis. Ann Surg Oncol 10,
275-283.
Xu HX, Xie XY, Lu MD, Chen
JW, Yin XY, Xu ZF, Liu GJ (2004) Ultrasound-guided
percutaneous thermal ablation of hepatocellular carcinoma using microwave and
radiofrequency ablation. Clin Radiol
59, 53-61.
Yamasaki T, Kurokawa F,
Shirahashi H, Kusano N, Hironaka K, Okita K (2002) Percutaneous radiofrequency ablation therapy for patients
with hepatocellular carcinoma during occlusion of hepatic blood flow.
Comparison with standard percutaneous radiofrequency ablation therapy. Cancer 95, 2353-2360.
Charles
R. Scoggins