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Resection of noncolorectal liver metastases 219
Table 14.2
Selected studies of noncolorectal liver metastases with at least 20 patients, excluding neuroendocrine tumors.
Study n 5OS Dominant pathology
Harrison 1997 [84] 96 37% Sarcoma, GU
Elias 1998 [85] 120 36%
Lang 1999 [86] 127 16% Breast, sarcoma, GI
Buell 2000 [87] 25 3OS 36% GU
Hamy 2000 [88] 27 27%
Hemming 2000 [89] 37 45% GU, GI, sarcoma
Laurent 2001 [90] 39 35% GI, GU, breast
Van Ruth 2001 [91] 28 35% GU, breast
Yamada 2001 [92] 33 12% GI
Cordera 2005 [93] 64 30% GU, GI, breast
Weitz 2005 [39] 141 CSS 3 y 57% GU, breast, melanoma
Yedibela 2005 [94] 162 27%
Ercolani 2005 [95] 142 34% Breast, GI, GU
Adam 2006 [40] 1452 36% Breast, GI, GU
Earle 2006 [96] 77 31% GU, sarcoma, GI
Lendoire 2007 [97] 106 19% GU, sarcoma, breast
Reddy 2007 [98] 82 37% Breast, sarcoma, GU
O’Rourke 2008 [41] 102 39% Soft tissue, GU, GI
Ercolani 2009 [99] 134 40% (abstract only)
Lehner 2009 [100] 242 28% (non-English language article)
Marudanayagam 2010 [101] 65 26% GU
Schmelze 2010 [102] 44 20% GU, GI, breast
Duan 2011 [103] 62 30% Breast, lung, stomach
Groeschl 2012 [42] 420 31% Breast, sarcoma, GU
Takemura 2013 [104] 145 41% GI, breast
∗
∗
∗
Breast, GU
GI, sarcoma
GI, breast, GU
∗
Survival figures included patients with neuroendocrine tumors.
3OS, three-year overall survival; 5OS, five-year overall survival; CSS, cancer-specific survival; GI, gastrointestinal; GU, genitourinary.
Sixty-day mortality was 1.9% and complications
occurred in 20%. Overall survival rates at three and
five years were 50% and 31%, respectively, with a
median of 49 months. Overall recurrence rate was
66% and was similar across the various cancer types.
Lymphovascular invasion and size of metastases (5 cm)
predicted poorer survival, whereas type of tumor did not.
surgery [45]. Adam et al. reported a series of 85 patients
undergoing liver resection with a five-year overall survival rate of 37%, and median survival of 32 months [46].
Sixty-nine percent of patients recurred after a median of
10 months, with about half of those recurrences in the
liver only. Response to chemotherapy predicted survival,
as did macroscopic residual tumor. In their series of 86
patients, Abbott et al. found a five-year overall survival
14.3.2 Studies of specific tumor types
14.3.2.1 Breast
Distant metastases occur in approximately 50% of breast
cancer patients, of which the liver is involved in 6–25%
cases. With supportive treatment only, median survival is
rate of 44%, and median survival of 57 months [47]. They
found that estrogen receptor negativity and progression
on chemotherapy were signs of poor prognosis.
Table 14.3 summarizes recent studies reporting outcomes
after surgery for breast cancer liver metastases.
<1 month. With systemic treatment using chemotherapy
and/or endocrine therapy, good responders have a
median survival around 13–23 months [43,44].
Most patients have disseminated disease, but about 5%
have isolated liver metastases that may be amenable to
14.3.2.2 Gastrointestinal
The majority of evidence regarding NCNN from gastro-
intestinal (GI) sources comes from gastric cancer series
from Asia. At time of diagnosis of gastric cancer, 35% of
220 Chapter 14
Figure 14.2 Survival curves for 1452 patients in 41 centers after hepatectomy for NCNN. (a) Overall survival. (b) Recurrence-free
survival. Source: Adam et al. [40]. Reproduced with permission of Lippincott, Williams, & Wilkins.
Resection of noncolorectal liver metastases 221
Table 14.3
patients have distant metastases, and 4–14% have liver
metastases. With chemotherapy only, the median survival is in the order of 7–15 months and five-year survival
is rare, around 2% [48,49]. Takamura et al. reported the
largest surgical series to date with 64 patients [50]. After
resection, the overall five-year survival rate was 37%,
Selected contemporary series of breast cancer liver metastases with at least 20 patients.
Study n 5OS Poor prognostic factors
Yoshimoto 2000 [105] 25 27% None
Pocard 2000 [106] 52 3OS 49% Node-positive primary, short disease-free interval
Elias 2003 [45] 54 34% Negative hormonal status
Adam 2006 [46] 85 37% Poor response to pre-op chemotherapy, positive margin, repeat hepatectomy
Thelen 2008 [107] 39 42% Positive margin
Abbott 2012 [47] 86 44% Negative hormonal status, progression on pre-op chemotherapy
Van Walsum 2012 32 37% >1 metastasis
Dittmar 2013 [109] 54 28% Extrahepatic disease, HER2 positivity, age >50
Kostov 2013 [110] 42 38% Negative hormonal status, size >4 cm, positive margin, positive portal nodes,
poor response to preoperative chemotherapy
3OS, three-year overall survival; 5OS, five-year overall survival.
Median survival after surgery was only 6–14 months.
Significantly, Takada et al. found that patients who under-
went synchronous pancreaticoduodenectomy and liver
resection had the same survival as patients who under-
went palliative bypass only and no liver resection, reflect-
ing the unfavorable biology of pancreatic cancer [52].
median 34 months. Presence of metastases >5 cm and
invasion of serosa by the primary tumor were indicators
of poor prognosis. Table 14.4 summarizes recent studies
reporting outcomes after surgery for gastric cancer liver
metastases.
Data for metastatic pancreatic cancer are even more
limited. A systematic review by Michalski et al. found 21
studies with a total of 103 patients over 15 years [51].
14.3.2.3 Gynecological
Most of the data on NCNN of gy necologi cal origin are
drawn from ovarian cancer. Isolated li ver metastases are
rare as ovarian cance r commonly spreads transperito-
neally. However, the biology of this disease lends itself
to cytoreductive surgery, which may include liver resec-
tion, to reduce macroscopic disease to <1cm.
Table 14.4 Selected contemporary series of gastric cancer liver metastases.
Study n 5OS Poor prognostic factors
Sakamoto 2007 [111] 37 11% Size >4 cm, bilobar metastases
Koga 2007 [112] 42 42% >1 metastasis, T3 primary
Thelen 2008 [113] 24 10% Positive margin
Morise 2008 [114] 18 27% T3 primary, LVI
Makino 2010 [115] 16 37%
Tsujimoto 2010 [116] 17 32% Size >6 cm, D1 lymphadenectomy
Schildberg 2012 [117] 31 13% >1 metastasis, positive margin, synchronous
Dittmar 2012 [118] 15 27%
Takemura 2012 [50] 64 37% Size >5 cm, T3 primary
Baek 2013 [119] 12 39%
Qiu 2013 [120] 25 29% >1 metastasis
Vigan 2013 [121] 14 33% Progression on chemotherapy
5OS, five-year overall survival; LVI, lymphovascular invasion.
222 Chapter 14
Table 14.5 Selected contemporary studies of liver resection for gynecological metastases.
Study n Outcome Poor prognostic factors Notes
Yoon 2003 [53] 24 Median OS 62 months Recurrent ovarian cancers
Bosquet 2006 [122] 35 Median DFS 41 months Residual disease (<1 cm better Recurrent ovarian cancers
than >1 cm)
Abood 2008 [123] 10 Median 33 months Size >5 cm, positive margin Ovarian cancers
Lim 2009 [124] 14 5OS 51% Epithelial ovarian cancers only
Kamel 2011 [54] 52 5OS 41% 77% tumors ovarian, 17% tumors uterine
Neumann 2012 [125] 41 Median 42 months Positive margin, ascites, bilobar Epithelial ovarian cancers only
metastases
5OS, five-year overall survival; DFS, disease-free survival; OS, overall survival.
Involvement of the liver with ovarian cancer is most
commonly in the form of capsular implants and, less
often, parenchymal metastases. Even in the presence of
extensive disease, therefore, parenchymal-sparing
resection is often possible.
Yoon et al. from the MSKCC reported a series of 24
patients submitted to hepatic resection, achieving a
median survival of 62 months, with cancer recurring in
75% of patients [53]. The authors noted that these
patients were initially chemosensitive and had experienced prolonged disease-free survival (median 36
months), highlighting the importance of selecting
patients with favorable biology. Kamel et al. reported
their series of 52 patients, resulting in a 75% recurrence
rate at a median of 13 months, with an overall five-year
survival rate of 41%, median 38 months [54]. Table 14.5
summarizes recent studies reporting outcomes after surgery for gynecological liver metastases.
14.3.2.4 Germ cell tumors
Chemotherapy with cisplatin-based regimens is the
mainstay of treatment for metastatic germ cell tumors,
with a cure rate of 60–80%. The presence of liver metastasis worsens the prognosis to a 49% five-year survival
rate, and liver resection has been used as an adjunct to
medical management. Rivoire et al. examined the outcomes of liver resection in 37 patients after chemotherapy
and found an overall survival rate of 62% at five years and
a median survival of 54 months [55]. These authors
identified three negative prognostic factors: presence of
pure embryonal carcinoma in the primary tumor, liver
metastases >30 mm, and presence of viable residual disease. The authors proposed that because germ cell tumors
are generally chemosensitive, liver resection should be
employed selectively. For male patients, they concluded
that metastases between 10 and 29 mm should be
resected, tumors 10 mm should be observed due to
the high probability of them being necrotic, and tumors
30 mm are a poor prognostic group that is unlikely to
benefit from surgery. Female patients fared better, leading the authors to propose that all liver metastases
>10 mm should be considered for resection. Hartmann
et al. reported a series of 43 male patients undergoing
postchemotherapy liver resection with a five-year overall
survival rate of 71% [56]. They found that tumors refractory to chemotherapy had a worse prognosis.
14.3.2.5 Renal cell carcinoma
Livermetastasesdevelopin10–20% of patients with
renalcellcarcinoma(RCC),ofwhich2– 4% are ame-
nable to hepatic resection. Without treatment, only
10% of patients survive more than 1 year. With surgery, five-year survival rates of approximately 25– 60%
have been reported. Thelen et al. reported a series of
31 patients who underwent liver resection and found
an overall five-year survival rate of 39% [57]. Staehler
et al.reportedafive-year survival rate of 62%, median
142 months, in 68 resected patients, compared to 29%
five-year survival and median of 27 months in 20
unresected patients [58]. Tabl e 14.6 summarizes recent
studies reporting outcomes after surgery for renal cell
cancer liver metastases.
14.3.2.6 Melanoma
Liver metastases develop in 10–20% of patients with
metastatic melanoma, with a dismal prognosis of from
two to seven months median survival, and are generally
chemo-resistant with a response rate of 10–30% [59].
Resection of noncolorectal liver metastases 223
Table 14.6
renal cell carcinoma metastases.
Selected contemporary series of liver resection for
Study n 5OS Poor prognostic factors
Aloia 2006 [126] 19 26% Size >5 cm, female sex
Thelen 2007 [57] 31 39% Positive margin
Staehler 2010 [58] 68 62%
Ruys 2011 [127] 29 43% Synchronous metastases,
positive margin
Langan 2012 [128] 10 33% Synchronous metastases
5OS, five-year overall survival.
Ocular melanoma has been reported to have a particularly high propensity to spread to the liver, in up to 95% of
patients [60]. In a review of 1750 melanoma patients with
liver metastases presenting to the John Wayne Cancer
Institute and Sydney Melanoma Unit, Rose et al. reported
a series of 24 patients (1.4%) who underwent curative or
palliative hepatectomy [61]. In this highly selected group,
median survival was 28 months and the five-year overall
survival rate was 29%. In comparison, 10 patients who
were surgically explored but not resected had a median
survival of four months. In addition, 899 patients treated
nonoperatively had a median survival of six months and a
five-year survival rate of 4%.
Pawlik et al. showed that tumor recurred after liver
resection in 75% of patients at a median of eight
months [59]. Ocular melanoma tended to recur more
often within the liver whereas cutaneous melanoma
recurred more often extrahepatically. Five-year survival
rate was also better for ocular primary at 20.5%, compared to no five-year survivors in the cutaneous group.
Aubin et al. conducted a systematic review of 22 studies
involving 579 patients undergoing liver resection for
metastatic melanoma and found an overall five-year
survival rate of 11–36%, median 14–41 months, compared to a median survival of 4–12 months for nonoperative management [62]. The number of metastases and
an R0 versus R1/R2 resection were found to be significant
prognostic factors.
In recent years, a number of new agents have emerged
for treatment of metastatic melanoma. The cytotoxic T
lymphocyte-associated antigen-4 (CTLA-4) blocking
monoclonal antibody ipilimumab has been shown in
two phase III trials to improve overall survival when
used alone or in combination with dacarbazine. Ipilimumab acts as an immune modulator by blocking intrinsic T-
cell inhibition [63,64]. Vemurafenib and trametinib are
inhibitors of the BRAF/MAP-kinase growth pathway that
have been shown in phase III trials to improve overall
survival [65]. They are only effective in patients with
BRAF mutations, present in approximately 50% of melanomas. Finally, trials are ongoing to investigate the role
of imatinib in the subset of melanoma harboring KIT
mutations, with promising phase II results [66]. Through
better systemic control of disease, the number of patients
who become surgical candidates may expand in the
future.
14.3.2.7 Sarcoma
Soft tissue sarcoma (STS) is relatively chemo-resistant.
An early series from the MSKCC showed a 6% partial
response rate to doxorubicin [67].
In 2001, DeMatteo et al. published a 19-year series of
4270 patients with STS from the MSKCC, in which 331
(7.8%) pati ents had liver meta stases, 40% of which
were gastrointestinal stromal tumors (GIST) or intestinal leiomyosarcomas [68]. Liver resection with curative
intent was performed in 56 (17%) patients. There was
recurrence in 84% of patients at a median of 16
months. The five-year disease-free survival rate was
30%, median 39 months, with 10 actual five-year
survivors. In contrast, patients who did not undergo
resection had a five-year disease-free surviv al rate of
4%, median 12 months. Eight patients who underwent
palliative resection (R2) for rel ief from symptoms had
no survival benefit with a median of only eight months.
On multivariate analysis, the only independent predictor of outcome was time interval to liver metas tasis of
>2 years. Neither primary histology, number or size of
metastases, extrahepatic disease, nor microscopic margin predicted survival.
The emergence of imatinib has completely changed the
approach to treatment of GIST. Imatinib is a selective
tyrosine kinase inhibitor that targets GISTs harboring
gain-of-function mutations in cKIT and PDGFR-α
proto-oncogenes, the main pathogenic mechanism in
95% of GISTs. So effective is this drug that it is now
the first-line treatment for liver metastases. However,
response is rarely complete, and most patients will progress after a median of two years due to acquired tumor
resistance. Cytoreductive surgery has been used in addition to imatinib to delay disease progression but the
evidence to support such adjuvant surgery is from retrospective analysis and prone to selection bias.
224 Chapter 14
Figure 14.3 Progression-free and overall survival of patients who underwent surgery for metastatic GIST (including liver, pancreas,
and peritoneal), grouped by preoperative radiological response to six months of imatinib. Source: DeMatteo et al. [69]. Reproduced
with permission of Lippincott, Williams, & Wilkins.
Furthermore, the optimum timing of cytoreduction is
unclear. DeMatteo et al. studied patients who underwent
surgery after six months of imatinib therapy, stratified
according to response [69]. Responders had a two-year
overall survival rate of 100%; patients with focal resistance progressed after a median of 12 months and had an
overall two-year survival of 36%; patients with multifocal
resistance progressed after three months and had an
overall one-year survival of 36% (Figure 14.3). The
authors concluded that patients with responsive disease
cytoreduction (17% of patients underwent hepatectomy) follo wed by imatinib with imatinib alone, and
found no difference in disease progression, need for
salvage surgery or overall survival. They concluded
that initial or “upfront” cytoreduction, despite being
effective in reducing tumor bulk, is not beneficial and
hence imatinib should remain first-line therapy for
metastatic GIST. Table 14.7 summarizes recent studies
reporting outcomes after surgery for sarcoma liver
metastases.
or focal resistance may benefit from surgery, but those
with multifocal resistance do not.
An et al. investigated the reverse approach [70]. In
249 patients, they retrospectively compared
Table 14.7 Selected contemporary series of liver resection for metastatic sarcoma.
Study n 5OS Histology types Poor prognostic factors
DeMatteo 2001 [68] 56 30% 61% GIST, 19% extraintestinal leiomyosarcoma DFI <24 months
Pawlik 2006 [59] 66 27% 55% GIST, 27% leiomyosarcoma
Rehders 2009 [129] 45 49% 30% leiomyosarcoma, 22% GIST DFI <24 months
5OS, five-year overall survival; DFI, disease-free interval; GIST, gastrointestinal stromal tumor.
14.3.3 Laparoscopic resection
There are no published studies to date specifically
addressing the role of laparoscopic resection for NCNN.
Resection of noncolorectal liver metastases 225
Table 14.8
Selected studies and prognostic factors.
Study Disease-free
interval
Cordera 2005 [93] Yes NR No Yes. GI worse than non-GI
Weitz 2005 [39] Yes, 24 months No Yes Yes. Genital better than
Yedibela 2005 [94] NR NR Yes Yes
Ercolani 2005 [95] No Yes, 5 cm NR Yes. GI worst, GU best Total tumor volume
Adam 2006 [40] Yes, 12 months Yes Yes Yes. Nonbreast, squamous, and Extrahepatic disease, age,
Earle 2006 [96] Yes, 24 months NR NR Yes. GI worse than non-GI Synchronous versus
Lendoire 2007 [97] No NR Yes Yes. GU and breast best Synchronous versus
O’Rourke 2008 [41] No Yes, 5 cm Yes No Extrahepatic nodal
Duan 2012 [103] Yes, 12 months Yes, 5 cm NR Yes. Breast and GU best, GI >1metastasis
Groeschl 2012 [42] No Yes, 5 cm No No Primary lymphovascular
GI, gastrointestinal; GU, genitourinary; NR, not reported.
Largest
metastasis
size
R0
versus
R1/R2
Primary tumor type Other
nongenital
melanoma worst 3 segments resected
metachronous, number
of metastases
metachronous
disease
intermediate
invasion
A number of larger series of laparoscopic liver resection
included small numbers of NCNNs in their patient
cohorts [71,72]. As with NELM, selection of NCNN for
laparoscopic resection is based on size, number, and
location of metastases rather than histological type.
There are no documented differences in the outcomes
between NCNN and CRLM attributable to laparoscopic
technique.
14.3.4 Patient selection for surgery
The most important factor to consider when selecting
patients with NCNN for surgery is tumor biology. Most
authors suggest liver resection only if all disease in the
liver and extrahepatic sites can be resected and/or
ablated, with the exception of gynecological metastases
where cytoreduction is proven to be effective treatment,
and in selected GISTs as an adjunct to imatinib to delay
progression. Prognostic factors identified in various series
provide some insight into which patients may benefit
most from surgery: longer disease-free interval, small
metastasis size, solitary metastasis, and good response
to or stability with chemotherapy. Efforts to improve
selection criteria are clearly warranted (Table 14.8,
Figure 14.4, Figure 14.5).
Figure 14.4 Overall survival following hepatic resection for
102 patients with NCNN, grouped by tumor size.
Source: O’Rourke et al. [41]. Reproduced with permission of
Springer.
226 Chapter 14
Figure 14.5 Disease-specific survival for 141 patients with
NCNN, grouped by tumor type. Source: Weitz et al. [39].
Reproduced with permission of Lippincott, Williams, & Wilkins.
KEY POINTS
Neuroendocrine liver metastases (NELM)
14.3.5 Summary
The management of NCNN is controversial, but may
follow that of CRLM and NELM. Evidence is dif ficult to
interpret due to small heterogeneous studies and selec-
tion bias. The majority of patients have unresectable
disease and their prognosis is dismal. The proportion of
patients with limited disease amenable to resection ranges
from 1% (melanoma) to 17% (sarcoma). In highly
selected patients, surgery may result in a long-term sur-
vival rate in the order of 30% at five years, but outcome is
critically dependent on identifying patients with favor-
able tumor biology. It is important to recognize that most
patients submitted to hepatic resection are not cured of
their disease. A multidisciplinary approach is essential for
optimal outcome.
• About 10–20% of patients have limited disease amenable to surgery.
• Aim to completely resect all liver disease, but cytoreduction of >90% can yield similar survival and is effective for palliation of
symptoms of hormonal excess.
• Disease recurs after resection in most patients.
• Overall five-year survival rates of 40–80% with surgery, compared to 30% without.
Noncolorectal, nonneuroendocrine liver metastases (NCNN)
• Most patients have disseminated disease with poor prognosis; only a small percentage of patients are candidat es for liver
resection.
• Careful selection of patients with limited disease and favorable cancer biology can result in five-year survival rates of 25–40%.
• Metastases arising from breast, genitourinary, and sarcoma primaries have better prognosis than those arising from gastro-
intestinal and melanoma primaries.
• Favorable factors to consider include smaller size (<5 cm), solitary metastasis, longer disease-free interval (>24 months), and
good response to chemotherapy.
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