Skip to main content
Erschienen in: Radiation Oncology 1/2014

Open Access 01.12.2014 | Review

Oligometastasis and oligo-recurrence: more than a mirage

verfasst von: Fang Huang, Gang Wu, Kunyu Yang

Erschienen in: Radiation Oncology | Ausgabe 1/2014

Abstract

The standard treatment choice for cancer metastasis has been systemic management, including cytotoxic chemotherapy, hormonal manipulation, and targeted therapy. Emerging evidence has shown an oligometastatic state, an intermediate state between limited primary cancer and polymetastatic cancer, in which local therapy for metastatic lesions results in satisfactory survival comparable to non-metastatic disease. We provide a comprehensive introduction of evidence from experimental and clinical studies in favor of the oligometastatic phenotype, we review the efficacy and safety of surgery and stereotactic body radiotherapy in the treatment of oligometastases, and finally, we discuss the way to differentiate the oligometastatic state from polymetastasis.
Hinweise

Competing interests

The authors declare that they have no competing interests.
Abkürzungen
SBRT
Stereotactic body radiotherapy
OS
Overall survival
NET
Neuroendocrine tumors
PFS
Progression-free survival
DFI
Disease-free interval
NSCLC
Non-small cell lung cancer

Introduction

Cancer is widely regarded as a systemic disease. Previously, cancer with metastasis has been considered stage IV, an end-stage disease, with the goal of palliative management. The standard treatment choice for metastatic cancer has been systemic management, including cytotoxic chemotherapy, hormonal manipulation, and targeted therapy. Despite recent advances in systemic therapy, prognosis remains poor. Within the population of cancer metastasis, emerging evidence has shown that a fraction of patients have an oligometastatic state, in which local therapy for metastatic lesions results in satisfactory survival comparable to non-metastatic disease. The concept of an oligometastatic state was first proposed by Hellman et al. as an intermediate state (≤5 metastases) between limited primary and polymetastatic cancers in which local therapy could achieve long-term survival or cure, with no restrictions on primary lesions [1],[2]. In 2006, the concept of oligo-recurrence was defined by Niibe et al. as the state that cancer patients have ≤5 metastatic or recurrent lesions with controlled primary lesions [3]. Recently, the concept of sync-oligometastasis was proposed as the state that cancer patients have ≤5 metastatic or recurrent lesions with active primary lesions [4]. The major difference among oligometastasis, oligo-recurrence and sync-oligometastasis was the status of the primary lesion, which is the most important prognostic factor of oligometastasis, and oligo-recurrence showed better prognosis compared with sync-oligometastasis.
Despite the accumulating knowledge on this state, the existence of oligometastasis remains debatable. Although oligometastatic clones are not identified directly, some clonal areas with modest metastatic capacities might lead to oligometastasis, at least in a fraction of all metastatic cases. During the past decades, a large amount of data has shown excellent 5-year survival rates after aggressive local treatment of metastatic disease for many patients, including those with a limited number of metastases, certain primary tumor types, and early T- and N-stage primary tumors. However, many oncologists believe oligometastasis is more like a mirage than a reality. In this review, we provide a comprehensive introduction of evidence favoring the oligometastatic phenotype, we review the efficacy and safety of two methods to treat metastatic lesions [surgery and stereotactic body radiotherapy (SBRT)], and finally, we discuss the manner in which oligometastasis can be differentiated from polymetastasis.

Review

Biological basis of the oligometastatic phenotype

Metastasis occurs when genetically unstable cancer cells colonize a tissue microenvironment distant from the primary tumor. With advances in genomic research techniques, including next-generation sequencing and high-resolution genome-wide SNP and copy number analyses, emerging evidence indicates that clones with selective advantages within the primary tumor give rise to distant metastasis. Navin et al. applied single-nucleus sequencing to investigate the genetic relationship between a primary breast cancer tumor and its liver metastasis [5], they found that copy number profiles from the primary tumor were highly similar to those from the metastases, indicating that metastatic cells emerge from a main advanced expansion rather than from an earlier intermediate or a completely different subpopulation.
Primary tumors are composed of heterogeneous cell populations, and evidence over the years has shown that tumor clones are not equally able to metastasize. Fidler et al. identified a wide range of metastatic ability of B16F1 melanoma cells to colonize the lung [6], supporting the notion of clonal heterogeneity within the primary tumor. Various cell lines with high and low metastatic potential have also been reported in PC-14 human lung adenocarcinoma cells [7] and MHCC97 hepatocellular carcinoma cells [8], and these results have been expanded upon by investigators using KHT sarcoma cells [9].
Further important evidence implying the existence of oligometastasis was proposed by Yachida et al. who used next-generation sequencing techniques to analyze the genomes of seven patients with pancreatic cancer metastases in order to evaluate the clonal relationships between the primary and metastatic cancers [10]. Quantitative analysis of the genetic evolution of pancreatic cancer indicated at least a decade between the initiating mutation and the birth of the cancer cell, another five years were required for acquisition of metastatic ability. This temporal nature emphasizes that oligometastastic clones might develop before polymetastatic clones during tumorigenesis.
During this time, intensive research on metastasis-regulating genes has also advanced. Although the genes responsible for the oligometastastic phenotype remain elusive, DNA array analysis has provided important information to distinguish oligometastasis from polymetastasis. Wuttig et al. used samples from patients with renal cell carcinoma to identify genes that characterized `few’ (<8) or `many’ (>16) pulmonary metastases [11]. Analysis of fresh samples from resection of pulmonary metastases revealed 135 genes that were differentially expressed between the `few’ and `many’ metastasis groups. Furthermore, polymetastatic tumors were enriched by genes that regulate the cell cycle. Based on a meta-analysis of these data and previously published data, an 11-gene classifier was established to predict the number of metastases in patients with renal cell carcinoma. These data provide evidence at the molecular level for the existence of an oligometastastic state, but further work is essential to clarify mechanisms that generate the oligometastastic phenotype.

Clinical supporting evidence and treatment options for oligometastases

Liver oligometastases

The liver is frequently involved in cancer metastasis, especially in cancers from the gastrointestinal tract. This susceptibility is attributed to venous drainage of the gastrointestinal tract via the portal vein and to the liver-specific microenvironment suitable for colonization by certain types of tumor. Local therapy, including surgery and SBRT of liver metastatic lesions, has significantly improved survival in these patients. Much evidence exists showing the efficacy of surgical resection of hepatic metastases from colorectal cancer, with 10-year overall survival (OS) rates of 17-28%, which is far better than those of patients treated with systemic therapy [12].
Long-term survival after resection for non-colorectal cancer liver metastases has also been documented. A systematic review of >1000 patients with breast cancer and liver metastasis showed 2-, 3- and 5-year survival rates of 58-86%, 35-79% and 21-61%, respectively [13]. Liver metastasectomy of neuroendocrine tumors (NET) has also been shown to benefit most patients (95%) and prolong survival [14]. A systematic review of NET liver metastasectomy reported median 5- and 10-year OS rates of 70.5% and 42%, respectively, and median 1-, 3- and 5-year progression free survival (PFS) rates of 63%, 32% and 29%, respectively, which are much better than those from other tumor origins. Hepatectomy of metastases from melanoma also nearly doubles survival, with a median OS of 14 months after surgery increased to 27 months with R0 resection [15]. Summary of hepatic metastasectomy from selected studies were listed in Table 1.
Table 1
Summary of hepatic metastasectomy from selected studies
Primary tumor type
Year
No. patients
5-year survival (%)
10-year survival (%)
References
Noncolorectal
2005
142
26
/
[16]
Noncolorectal Nonendocrine liver metastases
2006
1452
36
23
[17]
Noncolorectal nonneuroendocrine liver metastases
2007
360
37
/
[18]
Breast cancer
2010
41
48
/
[19]
Soft-tissue sarcoma
2009
45
49
/
[20]
Although surgical resection is the optimal choice for patients with liver oligometastases, unfortunately, only some patients are eligible for metastasectomy at diagnosis [21]. It is difficult to eradicate gross tumors using conventional radiotherapeutic techniques without accompanied radiation-induced liver disease because of the relative radiosensitivity of the liver [22]. Stereotactic body radiotherapy allows delivery of ablative doses of radiation to metastatic lesions. The efficacy and tolerability of SBRT for liver metastasis has been confirmed by retrospective studies [23]-[26] showing local control rates around 80% or higher [27]. At Centre Oscar Lambret, 42 patients with 62 liver metastases were treated with SBRT at 40 Gy in 4 fractions and 45 Gy in 3 fractions. 1- and 2-year local control rates were 90% and 86%, respectively, and 1- and 2-year OS rates were 94% and 48%, respectively. In all, 38% of patients suffered grade 1 or 2 toxicity, and one patient had grade 3 epidermitis. Summary of SBRT for liver metastasis from selected studies were listed in Table 2.
Table 2
Summary of SBRT for liver metastasis from selected studies
Primary tumor type
Year
No. patients
Local control
Toxicity
References
Mixed (Most colorectal cancer)
2001
37
81% at 18 month
not mentioned
[28]
Mixed
2006
36
93% at 18 months
one case of grade 3 soft tissue toxicity
[29]
Mixed (Most colorectal cancer)
2009
68
1-year local control rate was 71%
9% acute grade 3 toxicities and 1% grade 4 toxicity
[30]
Mixed (Most colorectal cancer)
2006
25
1- and 2-year local control rates were 94% and 82%
4 cases of grade ≥3 toxicity
[31]
Mixed (Most colorectal cancer)
2011
27
30-, 50-, and 60-Gy cohorts were 56%, 89%, and 100% at 24 months respectively
one case of grade 3 toxicity
[32]
Mixed
2009
47
1- and 2-year local control rates were 95% and 92%
actuarial rate of grade ≥3 toxicity was 2%
[33]
Although many reports on SBRT for liver metastases are retrospective, prospective trials have been initiated as well. In phase I trials, maximum tolerated doses of SBRT were determined using a range of therapeutic doses in various fractions. In all, 60 Gy was well tolerated and safe and was commonly used as the therapeutic dose in phase II clinical trials. 1- and 2-year local control rates in prospective studies ranged 71-95% and 82-92%, respectively, with no grade 4–5 liver toxicity and few grade 3 toxicities [28]-[34]. Preliminary reports from a 2013 phase II trial of 61 patients with 3 or more lesions receiving 75 Gy on 3 consecutive days showed a 94% in-field local response rate at 1-year, median OS of 19 months and actuarial survival of 83.5% at 12 months. Grade 3 late toxicity occurred in one patient, with no grade 3 or higher acute toxicity. SBRT offers an alternative, noninvasive approach for patients with liver metastases. The outcomes of serial studies confirm that it is a promising treatment modality with efficacy and safety, bringing benefit to patients with unresectable lesions.

Lung oligometastases

Lung metastasis is also a major cause of cancer death, and the lung is the primary venous drainage organ for the entire body except the gastrointestinal tract. The lung is the most extensively studied organ for cancer microenvironment because of its susceptibility to metastasis. Local therapy for patients with lung oligometastases is not new and significantly prolongs survival. Many retrospective surgical studies have shown that patients with limited metastases can have a long-term survival, indicating that limited metastasis may be eliminated in these patients [35]-[41]. The particular study by Pastorino et al. (1997) is of great importance [35]. They assessed the long-term results of 5206 cases of lung metastases from different origins treated with surgery included in the International Registry of Lung Metastases. The 5-year OS rate of patients with complete metastasectomy was 36%, but it was only 13% for those with incomplete resection. A prospective study including 1720 patients with pulmonary metastatic melanoma showed that metastasectomy is a strong predictor of survival with the hazard ratio of 0.5 (95% CI: 0.4-0.6) [40]. Summary of pulmonary metastasectomy from selected studies were listed in Table 3.
Table 3
Summary of pulmonary metastasectomy from selected studies
Primary tumor type
Year
No. patients
5-year survival (%)
10-year survival (%)
References
Melanoma
2007
1720
21
/
[40]
Many types
2011
575
46
/
[37]
Colorectal carcinoma
2002
165
39.6
37.2
[41]
Colorectal carcinoma
2007
175
53.8
20.6
[42]
Renal cell carcinoma
2002
191
41.5
/
[38]
Renal cell carcinoma
2011
202
39
/
[43]
Testicular germ cell tumors
1998
157
68
/
[44]
Malignant fibrous histiocytoma
2005
103
21
/
[45]
Gynecologic cancers
2006
103
46.8
34.3
[46]
Bone sarcoma
2010
52
31
/
[47]
SBRT has been shown to prolong OS or even induce a cure in lung oligometastases, which is especially attractive for patients who refuse or are unsuitable for resection. Results of retrospective studies have shown 2-year local control rates ranging 80-90% and 2-year OS rates ranging 66-84% [48]-[52]. These results were repeated in a 2010 systematic review involving 334 patients, in which the 2-year weighted local control rate was 77.9%, and the 2-year weighted OS rate was 53.7%. Recently, Takahashi et al. conducted a retrospective analysis of 42 patients with lung oligo-recurrence who underwent SBRT, 2-year local control rate and 2-year OS rate were 87% and 65% respectively [53]. Interestingly, the efficacy and feasibility of carbon ion radiotherapy for lung oligo-recurrence were evaluated in a retrospective study, 3-year local control rate was 85.4% and 3-year OS rate was 50.1%, without any grade 3–5 toxicity [54]. The safety and efficacy of SBRT for lung oligometastases has been confirmed by prospective phase I and II trials. In one multi-institutional phase I/II trial, use of SBRT at 48–60 Gy in 3 fractions showed no dose-limiting toxicities. In all, 60 Gy was delivered in phase II, and 1- and 2-year actuarial local control rates were 100% and 96%, respectively. The median survival was 19 months. Grade 3 toxicity occurred in 8% of patients with no grade 4 or higher toxicity [55]. Other prospective studies have shown similar results [56],[57], which are comparable to survival after surgery. In summary, increasing evidence proves that SBRT is efficacious and well tolerated in patients with lung metastases. Summary of SBRT for lung metastasis from selected studies were listed in Table 4.
Table 4
Summary of SBRT for lung metastasis from selected studies
Primary tumor type
Year
No. patients
Local control
Toxicity
References
Mixed
2006
50
3-year local control rate 83%
35% Grade 1 toxicity, 6.1% grade 2 toxicity, 2% grade 3 toxicity
[51]
Mixed (Most NSCLC)
2009
124
3-year local control rate 83%
17.8% Grade 2 toxicity, 1.2% grade 3 toxicity
[48]
Mixed (Most colorectal cancer)
2010
10
1- and 2-year local control rates were 48% and 25%
Not mentioned
[58]
Mixed (Most colorectal cancer)
2011
44
1- and 2-year local control rates in colorectal cancers were 80% and 72%
2 cases of Grade 2 radiation pneumonitis, 1 case of Grade 3 pneumonitis, No Grades 4 radiation pneumonitis
[59]
Mixed (Most NSCLC)
2012
61
2- and 3- year local control rates were 89% and 83.5%
one case of grade 3 radiation pneumonitis
[52]
Mixed (Most colorectal cancer)
2013
32
1-, 2- and 3- year local control rates were 97%, 92% and 85%
no grade 4 toxicity, 3 cases of grade 3 toxicities, 1 case of grade 2 radiation pneumonitis
[60]

Adrenal oligometastases

Adrenal metastases, mostly lung and renal in origin, are reported to occur in 13-27% of disseminated malignancies at autopsy [61]. Although debates exist on adrenal metastasectomy, several retrospective studies have shown that both open and laparoscopic adrenalectomy prolongs survival [62],[63]. In a 2012 retrospective study by Zheng et al., 31/47 patients had adrenal metastasectomy, and survival rates were significantly higher in patients with surgery than in patients without surgery (34.2 ± 4.7 vs. 6.3 ± 2.7 months, respectively). Data on SBRT for treating adrenal metastases is limited. Several studies show that it is an invasive but effective and safe option [64],[65]. Casamassima et al. studied 48 patients with adrenal metastases who were treated with SBRT at 36 Gy/3 fractions. Actuarial 1- and 2-year local control rates were 90%, and actuarial OS rates at 1 and 2 years were 39.7% and 14.5%, respectively.

Spinal oligometastases

Bone metastases account for 20% of patients with metastatic tumors, and the most common site is the axial skeleton. Spinal metastases often cause pain and diminished quality of life. Palliative surgery benefit patients with spinal metastasis by improving quality of life [66],[67]. SBRT has emerged as a novel, promising and non-invasive treatment modality for isolated spinal metastasis [68],[69]. In a phase I/II trail, 149 patients with 166 non-cord compressing spinal metastases were treated with 27–30 Gy SBRT, generally in 3 fractions. Actuarial survival rates at 1 and 2 years were 71.9% and 48.8%, respectively. The actuarial local control rates at 1 and 2 years after SBRT were 80.5% and 72.4%, respectively. Few grade 3 and no grade 4 or higher toxicities were observed. Compared to surgery, SBRT may better benefit patients with prolong survival, pain relief and safety. However, it should be noted that SBRT is associated with vertebral compression fractures [70],[71].

Long-term follow-up data of oligometastases treated by SBRT

Although there are no prospective randomized studies comparing the long-term survival of SBRT and metastasectomy, the recent prospective study by Widder et al. found that the long-term survival of patients with pulmonary oligometastases treated with SBRT is not inferior to that of metastasectomy. In this study, the 5-year OS rates were 41% for metastasectomy and 49% for SBRT (p =0.43) [72].
Several studies have shown better prognosis in long-term survivors who had been treated with SBRT. Recently, de Vin et al. retrospectively studied 309 oligometastatic cancer patients treated with SBRT. They showed a 5-year OS rate of 32%, and they identified a subgroup of long-term survivors with a median survival of 40 (24–63) months [73]. Moreover, a prospective study by Milano et al. of 121 patients with oligometastases treated with SBRT showed a 6-year OS rate of 20%, and they identified selected long-term breast cancer survivors with a 6-year OS rate of 47% [74]. Clearly, the key issue for prospective randomized trials to verify the promising benefit of SBRT in patients with oligometastases will be how to identify the most suitable population for radical local treatment.

Clinical factors in selecting patients with oligometastases

The satisfactory outcomes of local therapy for oligometastases strongly suggest the existence of an oligometastatic phenotype, but the frequency of oligometastases in various cancer types is unknown, and there are no standard criteria used to identify these patients. However, several clinical prognostic factors have been identified which strongly suggest the oligometastatic state and aid in selecting patients for aggressive local therapies.

Colorectal cancer

Liver is the most common site of metastasis from colorectal cancer, and more than half of patients with colorectal cancer will develop liver metastases during the disease course. As early as the 1980s, a subpopulation of patients with isolated liver metastases and a better prognosis was identified [75], and hepatic resection has become the standard treatment for resectable liver metastases from colorectal cancer. Recent data on the efficacy of this surgical resection has demonstrated a 5-year OS rate of 39-47% and a 10-year OS rate of 17-28%, which is far better than for those who received systemic therapy [76],[77]. These long-term survivors strongly support the biological distinction of oligometastases in colorectal cancer. Simmonds et al. performed a review of 529 independent studies evaluating the benefit of hepatic resection of oligometastases from colorectal cancer and found a majority of retrospective studies and an absence of prospective randomized trials [78], indicating the need for further studies of this population.
Approximately 10-15% of patients with colorectal cancer will develop lung metastases, and pulmonary metastasectomy is the standard treatment for resectable lesions. Evidence suggests that patients with isolated lung metastases have a better prognosis after resection, with a 5-year OS rate of 40-61% [79],[80]. Salah et al. reviewed 8 retrospective studies of pulmonary metastasectomy in 988 colorectal cancer patients, and the 5-year OS rate was 54.3% following the first lung resection [81]. Moreover, after further stratification into the population into good, intermediate, and high-risk groups according to three independent prognostic factors (CEA, disease free interval and lesion numbers), the 5-year OS were 68.2%, 46.4% and 26.1%, respectively; in this, the good and intermediate groups had OS comparable to patients with stage III colorectal cancer.
Although there is a lack of randomized controlled data on local therapy for metastases from colorectal cancer, the promising long-term survival suggests a potential cure in the oligometastatic population, while this survival is rare in patients with extensive metastases.

Breast cancer

The survival benefit of pulmonary metastasectomy for patients with breast cancer has been reported in retrospective studies, but until recently, no prospective randomized trials have been available to validate the existence of oligometastases in breast cancer and to explore the impact of local therapy. Recently, Meimarakis et al. studied the role of metastasectomy in breast cancer patients with oligometastases, at least partially [82]. They reported 5- and 10-year OS rates of 59.6% and 43.0%, respectively, which were significantly higher than those of patients treated regularly.
Liver metastases of breast cancer are usually part of generalized metastases and indicate a poor prognosis with a median OS of 4–12 months, but selected (<5%) patients with isolated liver metastases have shown good long-term survival after metastasectomy of liver lesions. A systematic review by Bergenfeldt et al. analyzed patients with breast cancer and liver oligometastases who had undergone metastasectomy and patients who had received local ablation therapy such as SBRT, they showed that surgical resection led to 5-year OS rates of 25-42%, that local ablation therapy had similar survival results, and R0 resection was a strong prognostic factor for survival [13].

Non-small cell lung cancer (NSCLC)

A systematic review by Ashworth et al. analyzed 49 retrospective studies of 2176 patients with NSCLC treated with metastasectomy and found highly variable survival outcomes, with 5-year OS rates of 10-80% and more than half of oligometastatic lesions progressing within 12 months after metastasectomy [83]. Interestingly, two randomized controlled trials, primarily of patients with NSCLC, have provided compelling evidence in support of an oligometastatic state. In 1990, Patchell et al. reported that patients with a single brain metastasis who had undergone metastasectomy plus radiotherapy had longer survival than those who had received radiotherapy alone [84]. In a randomized multi-institutional trial, 333 patients (64% NSCLC) with brain metastases received whole-brain radiation therapy with or without an SBRT boost; results for patients with a single brain metastases showed that the combination therapy group had a survival advantage compared to the whole-brain radiation group (median OS 6.5 vs 4.9 months, p =0.039) [85].

Other tumor origins

The different histology of tumors greatly influences prognosis, and this fact should be taken into account when determining patient treatment. Studies have shown that tumors from particular origins have a better prognosis after local therapy. Pulmonary metastases from germ cell tumors, hepatic metastases from neuroendocrine tumors (NET), and breast cancer oligometastases all have relatively prolonged survival, while hepatic metastasis from gastric cancer has a worse prognosis. A 2011 retrospective study of 575 patients and 708 lesions by Casiraghi et al. showed that tumor origin predicts prognosis after pulmonary metastasectomy, with 5-year survival rates of 46%, 39%, 37% and 90% for epithelial, sarcoma, melanoma and germ cell cancers, respectively.

Number of metastases in selecting patients with oligometastases

The number of metastatic lesions is known to influence prognosis, but the concrete number of lesions has not been determined. Several important studies confirmed that 4 metastases is a critical value. A systematic review of 15 studies by Spelt et al. demonstrated that number of metastases was a prognostic factor in all prospective studies and in 8/11 retrospective studies, and that number of metastases correlated best with survival [86].

DFI in selecting patients with oligometastases

DFI has generally been considered a prognostic factor in lung metastases other than liver metastases. The value of DFI has not been standardized, however, and varies between 12, 23 and 36 months in different studies. Kanzaki et al. studied patients with pulmonary metastasectomy from renal cell carcinoma and demonstrated that a DFI ≥2 years was associated with a 5-year survival of 58% but that the survival of patients with DFI <2 years decreased to 26% [87]. DFI has also been found to be a prognostic factor after pulmonary local therapy. Pfannschmidt et al. demonstrated a 5-year survival rate of 24.7% in patients with DFI <23 months compared to 47% for those with DFI >23 months [33].

N stage in selecting patients with oligometastases

Involvement of lymph nodes, also termed N staging, is a risk factor in several tumor types, particularly in liver metastases other than pulmonary metastases. Negative lymph node status predicts a better prognosis than positive status after local therapy. In a study of 925 patients by Rees et al. to evaluate factors associated with prognosis after liver metastasectomy for colorectal cancer, primary lymph node status was identified as a prognostic factor, and 5-year survival was 42.2% with lymph node-negative status and 31.8% with lymph-node-positive status [88].

Scoring systems in selecting patients with oligometastases

Scoring systems, which aim to predict prognosis before local therapy, are useful because individual patients have different prognostic factors. Myrddin et al. performed a prospective study of 929 patients to identify prognostic factors after hepatic resection for metastatic colorectal cancer [88], and the Basingstoke Predictive Index was created based on the following prognostic factors: primary lymph node status, primary tumor differentiation, CEA level at hepatectomy, metastatic number, largest tumor diameter and extrahepatic metastatic disease. Patients were given a total score based on the prognostic factors and were divided into the following groups: 0, 5, 10, 15, 20, 25, and 30. Five-year survival in patients with the lowest scores was 66%, decreasing to only 2% in patients with the highest scores. Similar results have been observed in other scoring systems, including Risk score, the Memorial Sloan Kettering Cancer Center clinical risk score and simplified cancer staging systems [89]-[91].

MiroRNA signature in selecting patients with oligometastases

MicroRNA is known to regulate proliferation and apoptosis in cancer development, and microRNA expression profiles may be better able to classify cancer subtypes than coding gene profiles. Emerging evidence indicates that microRNA profiles could be a useful tool to distinguish oligometastasis from polymetastasis. Recently, Lussier et al. analyzed microRNA expression patterns from lung metastasis samples of patients with 1–5 metastatic tumors resected with curative intent [92] and identified distinct microRNA profiles between patients with the highest and lowest rates of recurrence. Another clinical/pathologic correlation study indicated that microRNA-200c expression was able accurately to characterize patients with clinically limited metastases into two phenotypes-those whose disease progressed to widespread, polymetastatic recurrence and those with clinically limited disease or oligometastatic recurrence [92].

Conclusions

Given the abundant clinical and biological evidence supporting the oligometastatic state, we infer that oligometastasis is more than a mirage. As understanding of the biology of metastases increases, improved biomarkers to accurately identify patients with oligometastases will be generated, allowing better selection for locally ablative therapies. Furthermore, prospective trials will be needed to clarify the criteria for selecting patients with oligometastases from each specific cancer type, and randomized trials comparing the efficacy and safety of different treatment modalities including SBRT or surgery will also be needed to generate guidelines for the treatment of oligometastasis. With the advance of molecular and clinical medicine, the oligometastasis mirage might be converted to a paradigm of cancer treatment.

Authors’ contributions

HF carried out the literature searching and manuscript drafting, WG carried out the sequence alignment and revision of the manuscript, YKY proposed the whole idea of the paper and context editing. All authors read and approved the final manuscript.

Acknowledgments

This work was supported by grants from the Natural Science Foundation of China (No. 81101507) to Fang Huang, and Natural Science Foundation of China (No. 81172121) to Kunyu Yang.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
The Creative Commons Public Domain Dedication waiver (https://​creativecommons.​org/​publicdomain/​zero/​1.​0/​) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Competing interests

The authors declare that they have no competing interests.
Literatur
1.
Zurück zum Zitat Weichselbaum RR, Hellman S: Oligometastases revisited. Nat Rev Clin Oncol. 2011, 8: 378-382.PubMed Weichselbaum RR, Hellman S: Oligometastases revisited. Nat Rev Clin Oncol. 2011, 8: 378-382.PubMed
2.
Zurück zum Zitat Hellman S, Weichselbaum RR: Oligometastases. J Clin Oncol. 1995, 13: 8-10.PubMed Hellman S, Weichselbaum RR: Oligometastases. J Clin Oncol. 1995, 13: 8-10.PubMed
3.
Zurück zum Zitat Niibe Y, Hayakawa K: Oligometastases and oligo-recurrence: the new era of cancer therapy. Jpn J Clin Oncol. 2010, 40: 107-111. 10.1093/jjco/hyp167.PubMedCentralCrossRefPubMed Niibe Y, Hayakawa K: Oligometastases and oligo-recurrence: the new era of cancer therapy. Jpn J Clin Oncol. 2010, 40: 107-111. 10.1093/jjco/hyp167.PubMedCentralCrossRefPubMed
4.
Zurück zum Zitat Niibe Y, Chang JY: Novel insights of oligometastases and oligo-recurrence and review of the literature. Pulm Med. 2012, 2012: 261096-10.1155/2012/261096.PubMedCentralCrossRefPubMed Niibe Y, Chang JY: Novel insights of oligometastases and oligo-recurrence and review of the literature. Pulm Med. 2012, 2012: 261096-10.1155/2012/261096.PubMedCentralCrossRefPubMed
5.
Zurück zum Zitat Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, Muthuswamy L, Krasnitz A, McCombie R, Wigler M: Tumour evolution inferred by single-cell sequencing. Nature. 2011, 472: 90-94. 10.1038/nature09807.PubMedCentralCrossRefPubMed Navin N, Kendall J, Troge J, Andrews P, Rodgers L, McIndoo J, Cook K, Stepansky A, Levy D, Esposito D, Muthuswamy L, Krasnitz A, McCombie R, Wigler M: Tumour evolution inferred by single-cell sequencing. Nature. 2011, 472: 90-94. 10.1038/nature09807.PubMedCentralCrossRefPubMed
6.
Zurück zum Zitat Fidler IJ, Kripke ML: Metastasis results from preexisting variant cells within a malignant tumor. Science (New York, NY). 1977, 197: 893-895. 10.1126/science.887927.CrossRef Fidler IJ, Kripke ML: Metastasis results from preexisting variant cells within a malignant tumor. Science (New York, NY). 1977, 197: 893-895. 10.1126/science.887927.CrossRef
7.
Zurück zum Zitat Shindo-Okada N, Takeuchi K, Nagamachi Y: Establishment of cell lines with high- and low-metastatic potential from PC-14 human lung adenocarcinoma. Jpn J Cancer Res. 2001, 92: 174-183. 10.1111/j.1349-7006.2001.tb01080.x.CrossRefPubMed Shindo-Okada N, Takeuchi K, Nagamachi Y: Establishment of cell lines with high- and low-metastatic potential from PC-14 human lung adenocarcinoma. Jpn J Cancer Res. 2001, 92: 174-183. 10.1111/j.1349-7006.2001.tb01080.x.CrossRefPubMed
8.
Zurück zum Zitat Li Y, Tang ZY, Ye SL, Liu YK, Chen J, Xue Q, Chen J, Gao DM, Bao WH: Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J Gastroenterol. 2001, 7: 630-636.PubMedCentralPubMed Li Y, Tang ZY, Ye SL, Liu YK, Chen J, Xue Q, Chen J, Gao DM, Bao WH: Establishment of cell clones with different metastatic potential from the metastatic hepatocellular carcinoma cell line MHCC97. World J Gastroenterol. 2001, 7: 630-636.PubMedCentralPubMed
9.
Zurück zum Zitat Chambers AF, Hill RP, Ling V: Tumor heterogeneity and stability of the metastatic phenotype of mouse KHT sarcoma cells. Cancer Res. 1981, 41: 1368-1372.PubMed Chambers AF, Hill RP, Ling V: Tumor heterogeneity and stability of the metastatic phenotype of mouse KHT sarcoma cells. Cancer Res. 1981, 41: 1368-1372.PubMed
10.
Zurück zum Zitat Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA: Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010, 467: 1114-1117. 10.1038/nature09515.PubMedCentralCrossRefPubMed Yachida S, Jones S, Bozic I, Antal T, Leary R, Fu B, Kamiyama M, Hruban RH, Eshleman JR, Nowak MA, Velculescu VE, Kinzler KW, Vogelstein B, Iacobuzio-Donahue CA: Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010, 467: 1114-1117. 10.1038/nature09515.PubMedCentralCrossRefPubMed
11.
Zurück zum Zitat Wuttig D, Baier B, Fuessel S, Meinhardt M, Herr A, Hoefling C, Toma M, Grimm MO, Meye A, Rolle A, Wirth MP: Gene signatures of pulmonary metastases of renal cell carcinoma reflect the disease-free interval and the number of metastases per patient. Int J Cancer. 2009, 125: 474-482. 10.1002/ijc.24353.CrossRefPubMed Wuttig D, Baier B, Fuessel S, Meinhardt M, Herr A, Hoefling C, Toma M, Grimm MO, Meye A, Rolle A, Wirth MP: Gene signatures of pulmonary metastases of renal cell carcinoma reflect the disease-free interval and the number of metastases per patient. Int J Cancer. 2009, 125: 474-482. 10.1002/ijc.24353.CrossRefPubMed
12.
Zurück zum Zitat Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, Kemeny N, Brennan MF, Blumgart LH, D’Angelica M: Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007, 25: 4575-4580. 10.1200/JCO.2007.11.0833.CrossRefPubMed Tomlinson JS, Jarnagin WR, DeMatteo RP, Fong Y, Kornprat P, Gonen M, Kemeny N, Brennan MF, Blumgart LH, D’Angelica M: Actual 10-year survival after resection of colorectal liver metastases defines cure. J Clin Oncol. 2007, 25: 4575-4580. 10.1200/JCO.2007.11.0833.CrossRefPubMed
13.
Zurück zum Zitat Bergenfeldt M, Jensen BV, Skjoldbye B, Nielsen D: Liver resection and local ablation of breast cancer liver metastases-a systematic review. Eur J Surg Oncol. 2011, 37: 549-557. 10.1016/j.ejso.2011.04.013.CrossRefPubMed Bergenfeldt M, Jensen BV, Skjoldbye B, Nielsen D: Liver resection and local ablation of breast cancer liver metastases-a systematic review. Eur J Surg Oncol. 2011, 37: 549-557. 10.1016/j.ejso.2011.04.013.CrossRefPubMed
14.
Zurück zum Zitat Saxena A, Chua TC, Perera M, Chu F, Morris DL: Surgical resection of hepatic metastases from neuroendocrine neoplasms: a systematic review. Surg Oncol. 2012, 21: e131-141. 10.1016/j.suronc.2012.05.001.CrossRefPubMed Saxena A, Chua TC, Perera M, Chu F, Morris DL: Surgical resection of hepatic metastases from neuroendocrine neoplasms: a systematic review. Surg Oncol. 2012, 21: e131-141. 10.1016/j.suronc.2012.05.001.CrossRefPubMed
15.
Zurück zum Zitat Mariani P, Piperno-Neumann S, Servois V, Berry MG, Dorval T, Plancher C, Couturier J, Levy-Gabriel C, Lumbroso-Le Rouic L, Desjardins L, Salmon RJ: Surgical management of liver metastases from uveal melanoma: 16 years’ experience at the Institut Curie. Eur J Surg Oncol. 2009, 35: 1192-1197. 10.1016/j.ejso.2009.02.016.CrossRefPubMed Mariani P, Piperno-Neumann S, Servois V, Berry MG, Dorval T, Plancher C, Couturier J, Levy-Gabriel C, Lumbroso-Le Rouic L, Desjardins L, Salmon RJ: Surgical management of liver metastases from uveal melanoma: 16 years’ experience at the Institut Curie. Eur J Surg Oncol. 2009, 35: 1192-1197. 10.1016/j.ejso.2009.02.016.CrossRefPubMed
16.
Zurück zum Zitat Ercolani G, Grazi GL, Ravaioli M, Ramacciato G, Cescon M, Varotti G, Del Gaudio M, Vetrone G, Pinna AD: The role of liver resections for noncolorectal, nonneuroendocrine metastases: experience with 142 observed cases. Ann Surg Oncol. 2005, 12: 459-466. 10.1245/ASO.2005.06.034.CrossRefPubMed Ercolani G, Grazi GL, Ravaioli M, Ramacciato G, Cescon M, Varotti G, Del Gaudio M, Vetrone G, Pinna AD: The role of liver resections for noncolorectal, nonneuroendocrine metastases: experience with 142 observed cases. Ann Surg Oncol. 2005, 12: 459-466. 10.1245/ASO.2005.06.034.CrossRefPubMed
17.
Zurück zum Zitat Adam R, Chiche L, Aloia T, Elias D, Salmon R, Rivoire M, Jaeck D, Saric J, Le Treut YP, Belghiti J, Mantion G, Mentha G: Hepatic resection for noncolorectal nonendocrine liver metastases: analysis of 1,452 patients and development of a prognostic model. Ann Surg. 2006, 244: 524-535. 10.1097/01.sla.0000246847.02058.1b.PubMedCentralCrossRefPubMed Adam R, Chiche L, Aloia T, Elias D, Salmon R, Rivoire M, Jaeck D, Saric J, Le Treut YP, Belghiti J, Mantion G, Mentha G: Hepatic resection for noncolorectal nonendocrine liver metastases: analysis of 1,452 patients and development of a prognostic model. Ann Surg. 2006, 244: 524-535. 10.1097/01.sla.0000246847.02058.1b.PubMedCentralCrossRefPubMed
18.
Zurück zum Zitat Reddy SK, Barbas AS, Marroquin CE, Morse MA, Kuo PC, Clary BM: Resection of noncolorectal nonneuroendocrine liver metastases: a comparative analysis. J Am Coll Surg. 2007, 204: 372-382. 10.1016/j.jamcollsurg.2006.12.019.CrossRefPubMed Reddy SK, Barbas AS, Marroquin CE, Morse MA, Kuo PC, Clary BM: Resection of noncolorectal nonneuroendocrine liver metastases: a comparative analysis. J Am Coll Surg. 2007, 204: 372-382. 10.1016/j.jamcollsurg.2006.12.019.CrossRefPubMed
19.
Zurück zum Zitat Hoffmann K, Franz C, Hinz U, Schirmacher P, Herfarth C, Eichbaum M, Buchler MW, Schemmer P: Liver resection for multimodal treatment of breast cancer metastases: identification of prognostic factors. Ann Surg Oncol. 2010, 17: 1546-1554. 10.1245/s10434-010-0931-5.CrossRefPubMed Hoffmann K, Franz C, Hinz U, Schirmacher P, Herfarth C, Eichbaum M, Buchler MW, Schemmer P: Liver resection for multimodal treatment of breast cancer metastases: identification of prognostic factors. Ann Surg Oncol. 2010, 17: 1546-1554. 10.1245/s10434-010-0931-5.CrossRefPubMed
20.
Zurück zum Zitat Rehders A, Peiper M, Stoecklein NH, Alexander A, Boelke E, Knoefel WT, Rogiers X: Hepatic metastasectomy for soft-tissue sarcomas: is it justified?. World J Surg. 2009, 33: 111-117. 10.1007/s00268-008-9777-4.CrossRefPubMed Rehders A, Peiper M, Stoecklein NH, Alexander A, Boelke E, Knoefel WT, Rogiers X: Hepatic metastasectomy for soft-tissue sarcomas: is it justified?. World J Surg. 2009, 33: 111-117. 10.1007/s00268-008-9777-4.CrossRefPubMed
21.
Zurück zum Zitat Small R, Lubezky N, Ben-Haim M: Current controversies in the surgical management of colorectal cancer metastases to the liver. Isr Med Assoc J. 2007, 9: 742-747.PubMed Small R, Lubezky N, Ben-Haim M: Current controversies in the surgical management of colorectal cancer metastases to the liver. Isr Med Assoc J. 2007, 9: 742-747.PubMed
22.
Zurück zum Zitat Lawrence TS, Robertson JM, Anscher MS, Jirtle RL, Ensminger WD, Fajardo LF: Hepatic toxicity resulting from cancer treatment. Int J Radiat Oncol Biol Phys. 1995, 31: 1237-1248. 10.1016/0360-3016(94)00418-K.CrossRefPubMed Lawrence TS, Robertson JM, Anscher MS, Jirtle RL, Ensminger WD, Fajardo LF: Hepatic toxicity resulting from cancer treatment. Int J Radiat Oncol Biol Phys. 1995, 31: 1237-1248. 10.1016/0360-3016(94)00418-K.CrossRefPubMed
23.
Zurück zum Zitat Mendez Romero A, Hoyer M: Radiation therapy for liver metastases. Curr Opin Support Palliat Care. 2012, 6: 97-102. 10.1097/SPC.0b013e32834de6d8.CrossRefPubMed Mendez Romero A, Hoyer M: Radiation therapy for liver metastases. Curr Opin Support Palliat Care. 2012, 6: 97-102. 10.1097/SPC.0b013e32834de6d8.CrossRefPubMed
24.
Zurück zum Zitat Wada H, Takai Y, Nemoto K, Yamada S: Univariate analysis of factors correlated with tumor control probability of three-dimensional conformal hypofractionated high-dose radiotherapy for small pulmonary or hepatic tumors. Int J Radiat Oncol Biol Phys. 2004, 58: 1114-1120. 10.1016/j.ijrobp.2003.08.012.CrossRefPubMed Wada H, Takai Y, Nemoto K, Yamada S: Univariate analysis of factors correlated with tumor control probability of three-dimensional conformal hypofractionated high-dose radiotherapy for small pulmonary or hepatic tumors. Int J Radiat Oncol Biol Phys. 2004, 58: 1114-1120. 10.1016/j.ijrobp.2003.08.012.CrossRefPubMed
25.
Zurück zum Zitat Sawrie SM, Fiveash JB, Caudell JJ: Stereotactic body radiation therapy for liver metastases and primary hepatocellular carcinoma: normal tissue tolerances and toxicity. Cancer Control. 2010, 17: 111-119.PubMed Sawrie SM, Fiveash JB, Caudell JJ: Stereotactic body radiation therapy for liver metastases and primary hepatocellular carcinoma: normal tissue tolerances and toxicity. Cancer Control. 2010, 17: 111-119.PubMed
26.
Zurück zum Zitat Lanciano R, Lamond J, Yang J, Feng J, Arrigo S, Good M, Brady L: Stereotactic body radiation therapy for patients with heavily pretreated liver metastases and liver tumors. Front Oncol. 2012, 2: 23-10.3389/fonc.2012.00023.PubMedCentralCrossRefPubMed Lanciano R, Lamond J, Yang J, Feng J, Arrigo S, Good M, Brady L: Stereotactic body radiation therapy for patients with heavily pretreated liver metastases and liver tumors. Front Oncol. 2012, 2: 23-10.3389/fonc.2012.00023.PubMedCentralCrossRefPubMed
27.
Zurück zum Zitat Katz AW, Carey-Sampson M, Muhs AG, Milano MT, Schell MC, Okunieff P: Hypofractionated stereotactic body radiation therapy (SBRT) for limited hepatic metastases. Int J Radiat Oncol Biol Phys. 2007, 67: 793-798. 10.1016/j.ijrobp.2006.10.025.CrossRefPubMed Katz AW, Carey-Sampson M, Muhs AG, Milano MT, Schell MC, Okunieff P: Hypofractionated stereotactic body radiation therapy (SBRT) for limited hepatic metastases. Int J Radiat Oncol Biol Phys. 2007, 67: 793-798. 10.1016/j.ijrobp.2006.10.025.CrossRefPubMed
28.
Zurück zum Zitat Herfarth KK, Debus J, Lohr F, Bahner ML, Rhein B, Fritz P, Hoss A, Schlegel W, Wannenmacher MF: Stereotactic single-dose radiation therapy of liver tumors: results of a phase I/II trial. J Clin Oncol. 2001, 19: 164-170.PubMed Herfarth KK, Debus J, Lohr F, Bahner ML, Rhein B, Fritz P, Hoss A, Schlegel W, Wannenmacher MF: Stereotactic single-dose radiation therapy of liver tumors: results of a phase I/II trial. J Clin Oncol. 2001, 19: 164-170.PubMed
29.
Zurück zum Zitat Kavanagh BD, Schefter TE, Cardenes HR, Stieber VW, Raben D, Timmerman RD, McCarter MD, Burri S, Nedzi LA, Sawyer TE, Gaspar LE: Interim analysis of a prospective phase I/II trial of SBRT for liver metastases. Acta Oncol. 2006, 45: 848-855. 10.1080/02841860600904870.CrossRefPubMed Kavanagh BD, Schefter TE, Cardenes HR, Stieber VW, Raben D, Timmerman RD, McCarter MD, Burri S, Nedzi LA, Sawyer TE, Gaspar LE: Interim analysis of a prospective phase I/II trial of SBRT for liver metastases. Acta Oncol. 2006, 45: 848-855. 10.1080/02841860600904870.CrossRefPubMed
30.
Zurück zum Zitat Lee MT, Kim JJ, Dinniwell R, Brierley J, Lockwood G, Wong R, Cummings B, Ringash J, Tse RV, Knox JJ, Dawson LA: Phase I study of individualized stereotactic body radiotherapy of liver metastases. J Clin Oncol. 2009, 27: 1585-1591. 10.1200/JCO.2008.20.0600.CrossRefPubMed Lee MT, Kim JJ, Dinniwell R, Brierley J, Lockwood G, Wong R, Cummings B, Ringash J, Tse RV, Knox JJ, Dawson LA: Phase I study of individualized stereotactic body radiotherapy of liver metastases. J Clin Oncol. 2009, 27: 1585-1591. 10.1200/JCO.2008.20.0600.CrossRefPubMed
31.
Zurück zum Zitat Mendez Romero A, Wunderink W, Hussain SM, De Pooter JA, Heijmen BJ, Nowak PC, Nuyttens JJ, Brandwijk RP, Verhoef C, Ijzermans JN, Levendag PC: Stereotactic body radiation therapy for primary and metastatic liver tumors: A single institution phase i-ii study. Acta Oncol. 2006, 45: 831-837. 10.1080/02841860600897934.CrossRefPubMed Mendez Romero A, Wunderink W, Hussain SM, De Pooter JA, Heijmen BJ, Nowak PC, Nuyttens JJ, Brandwijk RP, Verhoef C, Ijzermans JN, Levendag PC: Stereotactic body radiation therapy for primary and metastatic liver tumors: A single institution phase i-ii study. Acta Oncol. 2006, 45: 831-837. 10.1080/02841860600897934.CrossRefPubMed
32.
Zurück zum Zitat Rule W, Timmerman R, Tong L, Abdulrahman R, Meyer J, Boike T, Schwarz RE, Weatherall P, Chinsoo Cho L: Phase I dose-escalation study of stereotactic body radiotherapy in patients with hepatic metastases. Ann Surg Oncol. 2011, 18: 1081-1087. 10.1245/s10434-010-1405-5.CrossRefPubMed Rule W, Timmerman R, Tong L, Abdulrahman R, Meyer J, Boike T, Schwarz RE, Weatherall P, Chinsoo Cho L: Phase I dose-escalation study of stereotactic body radiotherapy in patients with hepatic metastases. Ann Surg Oncol. 2011, 18: 1081-1087. 10.1245/s10434-010-1405-5.CrossRefPubMed
33.
Zurück zum Zitat Rusthoven KE, Kavanagh BD, Cardenes H, Stieber VW, Burri SH, Feigenberg SJ, Chidel MA, Pugh TJ, Franklin W, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for liver metastases. J Clin Oncol. 2009, 27: 1572-1578. 10.1200/JCO.2008.19.6329.CrossRefPubMed Rusthoven KE, Kavanagh BD, Cardenes H, Stieber VW, Burri SH, Feigenberg SJ, Chidel MA, Pugh TJ, Franklin W, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for liver metastases. J Clin Oncol. 2009, 27: 1572-1578. 10.1200/JCO.2008.19.6329.CrossRefPubMed
34.
Zurück zum Zitat Schefter TE, Kavanagh BD, Timmerman RD, Cardenes HR, Baron A, Gaspar LE: A phase I trial of stereotactic body radiation therapy (SBRT) for liver metastases. Int J Radiat Oncol Biol Phys. 2005, 62: 1371-1378. 10.1016/j.ijrobp.2005.01.002.CrossRefPubMed Schefter TE, Kavanagh BD, Timmerman RD, Cardenes HR, Baron A, Gaspar LE: A phase I trial of stereotactic body radiation therapy (SBRT) for liver metastases. Int J Radiat Oncol Biol Phys. 2005, 62: 1371-1378. 10.1016/j.ijrobp.2005.01.002.CrossRefPubMed
35.
Zurück zum Zitat Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. The International Registry of Lung Metastases.J Thorac Cardiovasc Surg 1997, 113:37–49, Long-term results of lung metastasectomy: prognostic analyses based on 5206 cases. The International Registry of Lung Metastases.J Thorac Cardiovasc Surg 1997, 113:37–49,
36.
Zurück zum Zitat Choong PF, Pritchard DJ, Rock MG, Sim FH, Frassica FJ: Survival after pulmonary metastasectomy in soft tissue sarcoma Prognostic factors in 214 patients. Acta Orthop Scand. 1995, 66: 561-568. 10.3109/17453679509002316.CrossRefPubMed Choong PF, Pritchard DJ, Rock MG, Sim FH, Frassica FJ: Survival after pulmonary metastasectomy in soft tissue sarcoma Prognostic factors in 214 patients. Acta Orthop Scand. 1995, 66: 561-568. 10.3109/17453679509002316.CrossRefPubMed
37.
Zurück zum Zitat Casiraghi M, De Pas T, Maisonneuve P, Brambilla D, Ciprandi B, Galetta D, Borri A, Gasparri R, Petrella F, Tessitore A, Guarize J, Donghi SM, Veronesi G, Solli P, Spaggiari L: A 10-year single-center experience on 708 lung metastasectomies: the evidence of the “international registry of lung metastases”. J Thorac Oncol. 2011, 6: 1373-1378. 10.1097/JTO.0b013e3182208e58.CrossRefPubMed Casiraghi M, De Pas T, Maisonneuve P, Brambilla D, Ciprandi B, Galetta D, Borri A, Gasparri R, Petrella F, Tessitore A, Guarize J, Donghi SM, Veronesi G, Solli P, Spaggiari L: A 10-year single-center experience on 708 lung metastasectomies: the evidence of the “international registry of lung metastases”. J Thorac Oncol. 2011, 6: 1373-1378. 10.1097/JTO.0b013e3182208e58.CrossRefPubMed
38.
Zurück zum Zitat Pfannschmidt J, Hoffmann H, Muley T, Krysa S, Trainer C, Dienemann H: Prognostic factors for survival after pulmonary resection of metastatic renal cell carcinoma. Ann Thorac Surg. 2002, 74: 1653-1657. 10.1016/S0003-4975(02)03803-1.CrossRefPubMed Pfannschmidt J, Hoffmann H, Muley T, Krysa S, Trainer C, Dienemann H: Prognostic factors for survival after pulmonary resection of metastatic renal cell carcinoma. Ann Thorac Surg. 2002, 74: 1653-1657. 10.1016/S0003-4975(02)03803-1.CrossRefPubMed
39.
Zurück zum Zitat Kanemitsu Y, Kato T, Hirai T, Yasui K: Preoperative probability model for predicting overall survival after resection of pulmonary metastases from colorectal cancer. Br J Surg. 2004, 91: 112-120. 10.1002/bjs.4370.CrossRefPubMed Kanemitsu Y, Kato T, Hirai T, Yasui K: Preoperative probability model for predicting overall survival after resection of pulmonary metastases from colorectal cancer. Br J Surg. 2004, 91: 112-120. 10.1002/bjs.4370.CrossRefPubMed
40.
Zurück zum Zitat Petersen RP, Hanish SI, Haney JC, Miller CC, Burfeind WR, Tyler DS, Seigler HF, Wolfe W, D’Amico TA, Harpole DH: Improved survival with pulmonary metastasectomy: an analysis of 1720 patients with pulmonary metastatic melanoma. J Thorac Cardiovasc Surg. 2007, 133: 104-110. 10.1016/j.jtcvs.2006.08.065.CrossRefPubMed Petersen RP, Hanish SI, Haney JC, Miller CC, Burfeind WR, Tyler DS, Seigler HF, Wolfe W, D’Amico TA, Harpole DH: Improved survival with pulmonary metastasectomy: an analysis of 1720 patients with pulmonary metastatic melanoma. J Thorac Cardiovasc Surg. 2007, 133: 104-110. 10.1016/j.jtcvs.2006.08.065.CrossRefPubMed
41.
Zurück zum Zitat Saito Y, Omiya H, Kohno K, Kobayashi T, Itoi K, Teramachi M, Sasaki M, Suzuki H, Takao H, Nakade M: Pulmonary metastasectomy for 165 patients with colorectal carcinoma: A prognostic assessment. J Thorac Cardiovasc Surg. 2002, 124: 1007-1013. 10.1067/mtc.2002.125165.CrossRefPubMed Saito Y, Omiya H, Kohno K, Kobayashi T, Itoi K, Teramachi M, Sasaki M, Suzuki H, Takao H, Nakade M: Pulmonary metastasectomy for 165 patients with colorectal carcinoma: A prognostic assessment. J Thorac Cardiovasc Surg. 2002, 124: 1007-1013. 10.1067/mtc.2002.125165.CrossRefPubMed
42.
Zurück zum Zitat Welter S, Jacobs J, Krbek T, Krebs B, Stamatis G: Long-term survival after repeated resection of pulmonary metastases from colorectal cancer. Ann Thorac Surg. 2007, 84: 203-210. 10.1016/j.athoracsur.2007.03.028.CrossRefPubMed Welter S, Jacobs J, Krbek T, Krebs B, Stamatis G: Long-term survival after repeated resection of pulmonary metastases from colorectal cancer. Ann Thorac Surg. 2007, 84: 203-210. 10.1016/j.athoracsur.2007.03.028.CrossRefPubMed
43.
Zurück zum Zitat Meimarakis G, Angele M, Staehler M, Clevert DA, Crispin A, Ruttinger D, Lohe F, Preissler G, Hatz RA, Winter H: Evaluation of a new prognostic score (Munich score) to predict long-term survival after resection of pulmonary renal cell carcinoma metastases. Am J Surg. 2011, 202: 158-167. 10.1016/j.amjsurg.2010.06.029.CrossRefPubMed Meimarakis G, Angele M, Staehler M, Clevert DA, Crispin A, Ruttinger D, Lohe F, Preissler G, Hatz RA, Winter H: Evaluation of a new prognostic score (Munich score) to predict long-term survival after resection of pulmonary renal cell carcinoma metastases. Am J Surg. 2011, 202: 158-167. 10.1016/j.amjsurg.2010.06.029.CrossRefPubMed
44.
Zurück zum Zitat Liu D, Abolhoda A, Burt ME, Martini N, Bains MS, Downey RJ, Rusch VW, Bosl GJ, Ginsberg RJ: Pulmonary metastasectomy for testicular germ cell tumors: a 28-year experience. Ann Thorac Surg. 1998, 66: 1709-1714. 10.1016/S0003-4975(98)00940-0.CrossRefPubMed Liu D, Abolhoda A, Burt ME, Martini N, Bains MS, Downey RJ, Rusch VW, Bosl GJ, Ginsberg RJ: Pulmonary metastasectomy for testicular germ cell tumors: a 28-year experience. Ann Thorac Surg. 1998, 66: 1709-1714. 10.1016/S0003-4975(98)00940-0.CrossRefPubMed
45.
Zurück zum Zitat Suri RM, Deschamps C, Cassivi SD, Nichols FC, Allen MS, Schleck CD, Pairolero PC: Pulmonary resection for metastatic malignant fibrous histiocytoma: an analysis of prognostic factors. Ann Thorac Surg. 2005, 80: 1847-1852. 10.1016/j.athoracsur.2005.05.004.CrossRefPubMed Suri RM, Deschamps C, Cassivi SD, Nichols FC, Allen MS, Schleck CD, Pairolero PC: Pulmonary resection for metastatic malignant fibrous histiocytoma: an analysis of prognostic factors. Ann Thorac Surg. 2005, 80: 1847-1852. 10.1016/j.athoracsur.2005.05.004.CrossRefPubMed
46.
Zurück zum Zitat Clavero JM, Deschamps C, Cassivi SD, Allen MS, Nichols FC, Barrette BA, Larson DR, Pairolero PC: Gynecologic cancers: factors affecting survival after pulmonary metastasectomy. Ann Thorac Surg. 2006, 81: 2004-2007. 10.1016/j.athoracsur.2006.01.068.CrossRefPubMed Clavero JM, Deschamps C, Cassivi SD, Allen MS, Nichols FC, Barrette BA, Larson DR, Pairolero PC: Gynecologic cancers: factors affecting survival after pulmonary metastasectomy. Ann Thorac Surg. 2006, 81: 2004-2007. 10.1016/j.athoracsur.2006.01.068.CrossRefPubMed
47.
Zurück zum Zitat Garcia Franco CE, Torre W, Tamura A, Guillen-Grima F, San-Julian M, Martin-Algarra S, Pardo FJ: Long-term results after resection for bone sarcoma pulmonary metastases. Eur J Cardiothorac Surg. 2010, 37: 1205-1208. 10.1016/j.ejcts.2009.11.026.CrossRefPubMed Garcia Franco CE, Torre W, Tamura A, Guillen-Grima F, San-Julian M, Martin-Algarra S, Pardo FJ: Long-term results after resection for bone sarcoma pulmonary metastases. Eur J Cardiothorac Surg. 2010, 37: 1205-1208. 10.1016/j.ejcts.2009.11.026.CrossRefPubMed
48.
Zurück zum Zitat Guckenberger M, Wulf J, Mueller G, Krieger T, Baier K, Gabor M, Richter A, Wilbert J, Flentje M: Dose-response relationship for image-guided stereotactic body radiotherapy of pulmonary tumors: relevance of 4D dose calculation. Int J Radiat Oncol Biol Phys. 2009, 74: 47-54. 10.1016/j.ijrobp.2008.06.1939.CrossRefPubMed Guckenberger M, Wulf J, Mueller G, Krieger T, Baier K, Gabor M, Richter A, Wilbert J, Flentje M: Dose-response relationship for image-guided stereotactic body radiotherapy of pulmonary tumors: relevance of 4D dose calculation. Int J Radiat Oncol Biol Phys. 2009, 74: 47-54. 10.1016/j.ijrobp.2008.06.1939.CrossRefPubMed
49.
Zurück zum Zitat Hamamoto Y, Kataoka M, Yamashita M, Nogami N, Sugawara Y, Kozuki T, Sawada S, Suehisa H, Shinohara S, Nakajima N, Shinkai T: Factors affecting the local control of stereotactic body radiotherapy for lung tumors including primary lung cancer and metastatic lung tumors. Jpn J Radiol. 2012, 30: 430-434. 10.1007/s11604-012-0071-x.CrossRefPubMed Hamamoto Y, Kataoka M, Yamashita M, Nogami N, Sugawara Y, Kozuki T, Sawada S, Suehisa H, Shinohara S, Nakajima N, Shinkai T: Factors affecting the local control of stereotactic body radiotherapy for lung tumors including primary lung cancer and metastatic lung tumors. Jpn J Radiol. 2012, 30: 430-434. 10.1007/s11604-012-0071-x.CrossRefPubMed
50.
Zurück zum Zitat Norihisa Y, Nagata Y, Takayama K, Matsuo Y, Sakamoto T, Sakamoto M, Mizowaki T, Yano S, Hiraoka M: Stereotactic body radiotherapy for oligometastatic lung tumors. Int J Radiat Oncol Biol Phys. 2008, 72: 398-403. 10.1016/j.ijrobp.2008.01.002.CrossRefPubMed Norihisa Y, Nagata Y, Takayama K, Matsuo Y, Sakamoto T, Sakamoto M, Mizowaki T, Yano S, Hiraoka M: Stereotactic body radiotherapy for oligometastatic lung tumors. Int J Radiat Oncol Biol Phys. 2008, 72: 398-403. 10.1016/j.ijrobp.2008.01.002.CrossRefPubMed
51.
Zurück zum Zitat Okunieff P, Petersen AL, Philip A, Milano MT, Katz AW, Boros L, Schell MC: Stereotactic Body Radiation Therapy (SBRT) for lung metastases. Acta Oncol. 2006, 45: 808-817. 10.1080/02841860600908954.CrossRefPubMed Okunieff P, Petersen AL, Philip A, Milano MT, Katz AW, Boros L, Schell MC: Stereotactic Body Radiation Therapy (SBRT) for lung metastases. Acta Oncol. 2006, 45: 808-817. 10.1080/02841860600908954.CrossRefPubMed
52.
Zurück zum Zitat Ricardi U, Filippi AR, Guarneri A, Ragona R, Mantovani C, Giglioli F, Botticella A, Ciammella P, Iftode C, Buffoni L, Ruffinie E, Scagliottif GV: Stereotactic body radiation therapy for lung metastases. Lung Cancer. 2012, 75: 77-81. 10.1016/j.lungcan.2011.04.021.CrossRefPubMed Ricardi U, Filippi AR, Guarneri A, Ragona R, Mantovani C, Giglioli F, Botticella A, Ciammella P, Iftode C, Buffoni L, Ruffinie E, Scagliottif GV: Stereotactic body radiation therapy for lung metastases. Lung Cancer. 2012, 75: 77-81. 10.1016/j.lungcan.2011.04.021.CrossRefPubMed
53.
Zurück zum Zitat Takahashi W, Yamashita H, Niibe Y, Shiraishi K, Hayakawa K, Nakagawa K: Stereotactic body radiotherapy for metastatic lung cancer as oligo-recurrence: an analysis of 42 cases. Pulmonary medicine. 2012, 2012: 454107-10.1155/2012/454107.PubMedCentralCrossRefPubMed Takahashi W, Yamashita H, Niibe Y, Shiraishi K, Hayakawa K, Nakagawa K: Stereotactic body radiotherapy for metastatic lung cancer as oligo-recurrence: an analysis of 42 cases. Pulmonary medicine. 2012, 2012: 454107-10.1155/2012/454107.PubMedCentralCrossRefPubMed
54.
Zurück zum Zitat Takahashi W, Nakajima M, Yamamoto N, Yamada S, Yamashita H, Nakagawa K, Tsuji H, Kamada T: Carbon ion radiotherapy for oligo-recurrent lung metastases from colorectal cancer: a feasibility study. Radiat Oncol. 2014, 9: 68-10.1186/1748-717X-9-68.PubMedCentralCrossRefPubMed Takahashi W, Nakajima M, Yamamoto N, Yamada S, Yamashita H, Nakagawa K, Tsuji H, Kamada T: Carbon ion radiotherapy for oligo-recurrent lung metastases from colorectal cancer: a feasibility study. Radiat Oncol. 2014, 9: 68-10.1186/1748-717X-9-68.PubMedCentralCrossRefPubMed
55.
Zurück zum Zitat Rusthoven KE, Kavanagh BD, Burri SH, Chen C, Cardenes H, Chidel MA, Pugh TJ, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for lung metastases. J Clin Oncol. 2009, 27: 1579-1584. 10.1200/JCO.2008.19.6386.CrossRefPubMed Rusthoven KE, Kavanagh BD, Burri SH, Chen C, Cardenes H, Chidel MA, Pugh TJ, Kane M, Gaspar LE, Schefter TE: Multi-institutional phase I/II trial of stereotactic body radiation therapy for lung metastases. J Clin Oncol. 2009, 27: 1579-1584. 10.1200/JCO.2008.19.6386.CrossRefPubMed
56.
Zurück zum Zitat Hof H, Hoess A, Oetzel D, Debus J, Herfarth K: Stereotactic single-dose radiotherapy of lung metastases. Strahlenther Onkol. 2007, 183: 673-678. 10.1007/s00066-007-1724-z.CrossRefPubMed Hof H, Hoess A, Oetzel D, Debus J, Herfarth K: Stereotactic single-dose radiotherapy of lung metastases. Strahlenther Onkol. 2007, 183: 673-678. 10.1007/s00066-007-1724-z.CrossRefPubMed
57.
Zurück zum Zitat Fritz P, Kraus HJ, Muhlnickel W, Hammer U, Dolken W, Engel-Riedel W, Chemaissani A, Stoelben E: Stereotactic, single-dose irradiation of stage I non-small cell lung cancer and lung metastases. Radiat Oncol. 2006, 1: 30-10.1186/1748-717X-1-30.PubMedCentralCrossRefPubMed Fritz P, Kraus HJ, Muhlnickel W, Hammer U, Dolken W, Engel-Riedel W, Chemaissani A, Stoelben E: Stereotactic, single-dose irradiation of stage I non-small cell lung cancer and lung metastases. Radiat Oncol. 2006, 1: 30-10.1186/1748-717X-1-30.PubMedCentralCrossRefPubMed
58.
Zurück zum Zitat Hamamoto Y, Kataoka M, Yamashita M, Shinkai T, Kubo Y, Sugawara Y, Inoue T, Sakai S, Aono S, Takahashi T, Semb T, Uwatsu K: Local control of metastatic lung tumors treated with SBRT of 48 Gy in four fractions: in comparison with primary lung cancer. Jpn J Clin Oncol. 2010, 40: 125-129. 10.1093/jjco/hyp129.CrossRefPubMed Hamamoto Y, Kataoka M, Yamashita M, Shinkai T, Kubo Y, Sugawara Y, Inoue T, Sakai S, Aono S, Takahashi T, Semb T, Uwatsu K: Local control of metastatic lung tumors treated with SBRT of 48 Gy in four fractions: in comparison with primary lung cancer. Jpn J Clin Oncol. 2010, 40: 125-129. 10.1093/jjco/hyp129.CrossRefPubMed
59.
Zurück zum Zitat Takeda A, Kunieda E, Ohashi T, Aoki Y, Koike N, Takeda T: Stereotactic body radiotherapy (SBRT) for oligometastatic lung tumors from colorectal cancer and other primary cancers in comparison with primary lung cancer. Radiother Oncol. 2011, 101: 255-259. 10.1016/j.radonc.2011.05.033.CrossRefPubMed Takeda A, Kunieda E, Ohashi T, Aoki Y, Koike N, Takeda T: Stereotactic body radiotherapy (SBRT) for oligometastatic lung tumors from colorectal cancer and other primary cancers in comparison with primary lung cancer. Radiother Oncol. 2011, 101: 255-259. 10.1016/j.radonc.2011.05.033.CrossRefPubMed
60.
Zurück zum Zitat Baschnagel AM, Mangona VS, Robertson JM, Welsh RJ, Kestin LL, Grills IS: Lung metastases treated with image-guided stereotactic body radiation therapy. Clin Oncol. 2013, 25: 236-241. 10.1016/j.clon.2012.12.005.CrossRef Baschnagel AM, Mangona VS, Robertson JM, Welsh RJ, Kestin LL, Grills IS: Lung metastases treated with image-guided stereotactic body radiation therapy. Clin Oncol. 2013, 25: 236-241. 10.1016/j.clon.2012.12.005.CrossRef
61.
Zurück zum Zitat Muth A, Persson F, Jansson S, Johanson V, Ahlman H, Wangberg B: Prognostic factors for survival after surgery for adrenal metastasis. Eur J Surg Oncol. 2010, 36: 699-704. 10.1016/j.ejso.2010.04.002.CrossRefPubMed Muth A, Persson F, Jansson S, Johanson V, Ahlman H, Wangberg B: Prognostic factors for survival after surgery for adrenal metastasis. Eur J Surg Oncol. 2010, 36: 699-704. 10.1016/j.ejso.2010.04.002.CrossRefPubMed
62.
Zurück zum Zitat Zheng QY, Zhang GH, Zhang Y, Guo YL: Adrenalectomy may increase survival of patients with adrenal metastases. Oncology letters. 2012, 3: 917-920.PubMedCentralPubMed Zheng QY, Zhang GH, Zhang Y, Guo YL: Adrenalectomy may increase survival of patients with adrenal metastases. Oncology letters. 2012, 3: 917-920.PubMedCentralPubMed
63.
Zurück zum Zitat Suzuki H: Laparoscopic adrenalectomy for adrenal carcinoma and metastases. Curr Opin Urol. 2006, 16: 47-53. 10.1097/01.mou.0000193378.14694.9b.CrossRefPubMed Suzuki H: Laparoscopic adrenalectomy for adrenal carcinoma and metastases. Curr Opin Urol. 2006, 16: 47-53. 10.1097/01.mou.0000193378.14694.9b.CrossRefPubMed
64.
Zurück zum Zitat Chawla S, Chen Y, Katz AW, Muhs AG, Philip A, Okunieff P, Milano MT: Stereotactic body radiotherapy for treatment of adrenal metastases. Int J Radiat Oncol Biol Phys. 2009, 75: 71-75. 10.1016/j.ijrobp.2008.10.079.CrossRefPubMed Chawla S, Chen Y, Katz AW, Muhs AG, Philip A, Okunieff P, Milano MT: Stereotactic body radiotherapy for treatment of adrenal metastases. Int J Radiat Oncol Biol Phys. 2009, 75: 71-75. 10.1016/j.ijrobp.2008.10.079.CrossRefPubMed
65.
Zurück zum Zitat Torok J, Wegner RE, Burton SA, Heron DE, Torok J, Wegner RE, Burton SA, Heron DE: Stereotactic body radiation therapy for adrenal metastases: a retrospective review of a noninvasive therapeutic strategy. Future Oncol. 2011, 7: 145-151. 10.2217/fon.10.165.CrossRefPubMed Torok J, Wegner RE, Burton SA, Heron DE, Torok J, Wegner RE, Burton SA, Heron DE: Stereotactic body radiation therapy for adrenal metastases: a retrospective review of a noninvasive therapeutic strategy. Future Oncol. 2011, 7: 145-151. 10.2217/fon.10.165.CrossRefPubMed
66.
Zurück zum Zitat Chamberlain MC: Spinal metastases from lung cancer-who benefits from decompression surgery?. Nat Clin Pract Neurol. 2007, 3: 188-189. 10.1038/ncpneuro0428.CrossRefPubMed Chamberlain MC: Spinal metastases from lung cancer-who benefits from decompression surgery?. Nat Clin Pract Neurol. 2007, 3: 188-189. 10.1038/ncpneuro0428.CrossRefPubMed
67.
Zurück zum Zitat Choi D, Morris S, Crockard A, Albert T, Bunger C, Fehlings M, Harrop J, Kawahara N, Martin JA, Massicotte EM, Mazel C, Oner FC, Peul W, Tomita K, Wang M: Assessment of quality of life after surgery for spinal metastases: position statement of the Global Spine Tumour Study Group. World Neurosurg. 2013, 80: e175-179. 10.1016/j.wneu.2013.02.054.CrossRefPubMed Choi D, Morris S, Crockard A, Albert T, Bunger C, Fehlings M, Harrop J, Kawahara N, Martin JA, Massicotte EM, Mazel C, Oner FC, Peul W, Tomita K, Wang M: Assessment of quality of life after surgery for spinal metastases: position statement of the Global Spine Tumour Study Group. World Neurosurg. 2013, 80: e175-179. 10.1016/j.wneu.2013.02.054.CrossRefPubMed
68.
Zurück zum Zitat Lo SS, Sahgal A, Wang JZ, Mayr NA, Sloan A, Mendel E, Chang EL: Stereotactic body radiation therapy for spinal metastases. Discov Med. 2010, 9: 289-296.PubMed Lo SS, Sahgal A, Wang JZ, Mayr NA, Sloan A, Mendel E, Chang EL: Stereotactic body radiation therapy for spinal metastases. Discov Med. 2010, 9: 289-296.PubMed
69.
Zurück zum Zitat Lopes JC, Navarro A, Sole JM, Martinez M, Guedea F: Stereotactic body radiation therapy for spinal metastases. Clin Transl Oncol. 2010, 12: 639-642. 10.1007/s12094-010-0570-0.CrossRefPubMed Lopes JC, Navarro A, Sole JM, Martinez M, Guedea F: Stereotactic body radiation therapy for spinal metastases. Clin Transl Oncol. 2010, 12: 639-642. 10.1007/s12094-010-0570-0.CrossRefPubMed
70.
Zurück zum Zitat Cunha MV, Al-Omair A, Atenafu EG, Masucci GL, Letourneau D, Korol R, Yu E, Howard P, Lochray F, da Costa LB, Fehlings MG, Sahgal A: Vertebral compression fracture (VCF) after spine stereotactic body radiation therapy (SBRT): analysis of predictive factors. Int J Radiat Oncol Biol Phys. 2012, 84: e343-349. 10.1016/j.ijrobp.2012.04.034.CrossRefPubMed Cunha MV, Al-Omair A, Atenafu EG, Masucci GL, Letourneau D, Korol R, Yu E, Howard P, Lochray F, da Costa LB, Fehlings MG, Sahgal A: Vertebral compression fracture (VCF) after spine stereotactic body radiation therapy (SBRT): analysis of predictive factors. Int J Radiat Oncol Biol Phys. 2012, 84: e343-349. 10.1016/j.ijrobp.2012.04.034.CrossRefPubMed
71.
Zurück zum Zitat Boehling NS, Grosshans DR, Allen PK, McAleer MF, Burton AW, Azeem S, Rhines LD, Chang EL: Vertebral compression fracture risk after stereotactic body radiotherapy for spinal metastases. J Neurosurg Spine. 2012, 16: 379-386. 10.3171/2011.11.SPINE116.CrossRefPubMed Boehling NS, Grosshans DR, Allen PK, McAleer MF, Burton AW, Azeem S, Rhines LD, Chang EL: Vertebral compression fracture risk after stereotactic body radiotherapy for spinal metastases. J Neurosurg Spine. 2012, 16: 379-386. 10.3171/2011.11.SPINE116.CrossRefPubMed
72.
Zurück zum Zitat Widder J, Klinkenberg TJ, Ubbels JF, Wiegman EM, Groen HJ, Langendijk JA: Pulmonary oligometastases: metastasectomy or stereotactic ablative radiotherapy?. Radiother Oncol. 2013, 107: 409-413. 10.1016/j.radonc.2013.05.024.CrossRefPubMed Widder J, Klinkenberg TJ, Ubbels JF, Wiegman EM, Groen HJ, Langendijk JA: Pulmonary oligometastases: metastasectomy or stereotactic ablative radiotherapy?. Radiother Oncol. 2013, 107: 409-413. 10.1016/j.radonc.2013.05.024.CrossRefPubMed
73.
Zurück zum Zitat de Vin T, Engels B, Gevaert T, Storme G, De Ridder M: Stereotactic radiotherapy for oligometastatic cancer: a prognostic model for survival. Ann Oncol. 2014, 25: 467-471. 10.1093/annonc/mdt537.CrossRefPubMed de Vin T, Engels B, Gevaert T, Storme G, De Ridder M: Stereotactic radiotherapy for oligometastatic cancer: a prognostic model for survival. Ann Oncol. 2014, 25: 467-471. 10.1093/annonc/mdt537.CrossRefPubMed
74.
Zurück zum Zitat Milano MT, Katz AW, Zhang H, Okunieff P: Oligometastases treated with stereotactic body radiotherapy: long-term follow-up of prospective study. Int J Radiat Oncol Biol Phys. 2012, 83: 878-886. 10.1016/j.ijrobp.2011.08.036.CrossRefPubMed Milano MT, Katz AW, Zhang H, Okunieff P: Oligometastases treated with stereotactic body radiotherapy: long-term follow-up of prospective study. Int J Radiat Oncol Biol Phys. 2012, 83: 878-886. 10.1016/j.ijrobp.2011.08.036.CrossRefPubMed
75.
Zurück zum Zitat Goslin R, Steele G, Zamcheck N, Mayer R, MacIntyre J: Factors influencing survival in patients with hepatic metastases from adenocarcinoma of the colon or rectum. Dis Colon Rectum. 1982, 25: 749-754. 10.1007/BF02553304.CrossRefPubMed Goslin R, Steele G, Zamcheck N, Mayer R, MacIntyre J: Factors influencing survival in patients with hepatic metastases from adenocarcinoma of the colon or rectum. Dis Colon Rectum. 1982, 25: 749-754. 10.1007/BF02553304.CrossRefPubMed
76.
Zurück zum Zitat Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL: Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002, 235: 759-766. 10.1097/00000658-200206000-00002.PubMedCentralCrossRefPubMed Choti MA, Sitzmann JV, Tiburi MF, Sumetchotimetha W, Rangsin R, Schulick RD, Lillemoe KD, Yeo CJ, Cameron JL: Trends in long-term survival following liver resection for hepatic colorectal metastases. Ann Surg. 2002, 235: 759-766. 10.1097/00000658-200206000-00002.PubMedCentralCrossRefPubMed
77.
Zurück zum Zitat Giuliante F, Ardito F, Vellone M, Ranucci G, Federico B, Giovannini I, Nuzzo G: Role of the surgeon as a variable in long-term survival after liver resection for colorectal metastases. J Surg Oncol. 2009, 100: 538-545. 10.1002/jso.21393.CrossRefPubMed Giuliante F, Ardito F, Vellone M, Ranucci G, Federico B, Giovannini I, Nuzzo G: Role of the surgeon as a variable in long-term survival after liver resection for colorectal metastases. J Surg Oncol. 2009, 100: 538-545. 10.1002/jso.21393.CrossRefPubMed
78.
Zurück zum Zitat Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M: Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006, 94: 982-999. 10.1038/sj.bjc.6603033.PubMedCentralCrossRefPubMed Simmonds PC, Primrose JN, Colquitt JL, Garden OJ, Poston GJ, Rees M: Surgical resection of hepatic metastases from colorectal cancer: a systematic review of published studies. Br J Cancer. 2006, 94: 982-999. 10.1038/sj.bjc.6603033.PubMedCentralCrossRefPubMed
79.
Zurück zum Zitat Suemitsu R, Takeo S, Kusumoto E, Hamatake M, Ikejiri K, Saitsu H: Results of a pulmonary metastasectomy in patients with colorectal cancer. Surg Today. 2011, 41: 54-59. 10.1007/s00595-009-4244-x.CrossRefPubMed Suemitsu R, Takeo S, Kusumoto E, Hamatake M, Ikejiri K, Saitsu H: Results of a pulmonary metastasectomy in patients with colorectal cancer. Surg Today. 2011, 41: 54-59. 10.1007/s00595-009-4244-x.CrossRefPubMed
80.
Zurück zum Zitat Inoue M, Ohta M, Iuchi K, Matsumura A, Ideguchi K, Yasumitsu T, Nakagawa K, Fukuhara K, Maeda H, Takeda S, Minami M, Ohno Y, Matsuda H: Benefits of surgery for patients with pulmonary metastases from colorectal carcinoma. Ann Thorac Surg. 2004, 78: 238-244. 10.1016/j.athoracsur.2004.02.017.CrossRefPubMed Inoue M, Ohta M, Iuchi K, Matsumura A, Ideguchi K, Yasumitsu T, Nakagawa K, Fukuhara K, Maeda H, Takeda S, Minami M, Ohno Y, Matsuda H: Benefits of surgery for patients with pulmonary metastases from colorectal carcinoma. Ann Thorac Surg. 2004, 78: 238-244. 10.1016/j.athoracsur.2004.02.017.CrossRefPubMed
81.
Zurück zum Zitat Salah S, Watanabe K, Welter S, Park JS, Park JW, Zabaleta J, Ardissone F, Kim J, Riquet M, Nojiri K, Gisabella M, Kim SY, Tanaka K, Ali BA: Colorectal cancer pulmonary oligometastases: pooled analysis and construction of a clinical lung metastasectomy prognostic model. Ann Oncol. 2012, 23: 2649-2655. 10.1093/annonc/mds100.CrossRefPubMed Salah S, Watanabe K, Welter S, Park JS, Park JW, Zabaleta J, Ardissone F, Kim J, Riquet M, Nojiri K, Gisabella M, Kim SY, Tanaka K, Ali BA: Colorectal cancer pulmonary oligometastases: pooled analysis and construction of a clinical lung metastasectomy prognostic model. Ann Oncol. 2012, 23: 2649-2655. 10.1093/annonc/mds100.CrossRefPubMed
82.
Zurück zum Zitat Meimarakis G, Ruttinger D, Stemmler J, Crispin A, Weidenhagen R, Angele M, Fertmann J, Hatz RA, Winter H: Prolonged overall survival after pulmonary metastasectomy in patients with breast cancer. Ann Thorac Surg. 2013, 95: 1170-1180. 10.1016/j.athoracsur.2012.11.043.CrossRefPubMed Meimarakis G, Ruttinger D, Stemmler J, Crispin A, Weidenhagen R, Angele M, Fertmann J, Hatz RA, Winter H: Prolonged overall survival after pulmonary metastasectomy in patients with breast cancer. Ann Thorac Surg. 2013, 95: 1170-1180. 10.1016/j.athoracsur.2012.11.043.CrossRefPubMed
83.
Zurück zum Zitat Ashworth A, Rodrigues G, Boldt G, Palma D: Is there an oligometastatic state in non-small cell lung cancer? A systematic review of the literature. Lung Cancer. 2013, 82: 197-203. 10.1016/j.lungcan.2013.07.026.CrossRefPubMed Ashworth A, Rodrigues G, Boldt G, Palma D: Is there an oligometastatic state in non-small cell lung cancer? A systematic review of the literature. Lung Cancer. 2013, 82: 197-203. 10.1016/j.lungcan.2013.07.026.CrossRefPubMed
84.
Zurück zum Zitat Patchell RA, Tibbs PA, Walsh JW, Dempsey RJ, Maruyama Y, Kryscio RJ, Markesbery WR, Macdonald JS, Young B: A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med. 1990, 322: 494-500. 10.1056/NEJM199002223220802.CrossRefPubMed Patchell RA, Tibbs PA, Walsh JW, Dempsey RJ, Maruyama Y, Kryscio RJ, Markesbery WR, Macdonald JS, Young B: A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med. 1990, 322: 494-500. 10.1056/NEJM199002223220802.CrossRefPubMed
85.
Zurück zum Zitat Andrews DW, Scott CB, Sperduto PW, Flanders AE, Gaspar LE, Schell MC, Werner-Wasik M, Demas W, Ryu J, Bahary JP, Souhami L, Rotman M, Mehta MP, Curran WJ: Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial. Lancet. 2004, 363: 1665-1672. 10.1016/S0140-6736(04)16250-8.CrossRefPubMed Andrews DW, Scott CB, Sperduto PW, Flanders AE, Gaspar LE, Schell MC, Werner-Wasik M, Demas W, Ryu J, Bahary JP, Souhami L, Rotman M, Mehta MP, Curran WJ: Whole brain radiation therapy with or without stereotactic radiosurgery boost for patients with one to three brain metastases: phase III results of the RTOG 9508 randomised trial. Lancet. 2004, 363: 1665-1672. 10.1016/S0140-6736(04)16250-8.CrossRefPubMed
86.
Zurück zum Zitat Spelt L, Andersson B, Nilsson J, Andersson R: Prognostic models for outcome following liver resection for colorectal cancer metastases: A systematic review. Eur J Surg Oncol. 2012, 38: 16-24. 10.1016/j.ejso.2011.10.013.CrossRefPubMed Spelt L, Andersson B, Nilsson J, Andersson R: Prognostic models for outcome following liver resection for colorectal cancer metastases: A systematic review. Eur J Surg Oncol. 2012, 38: 16-24. 10.1016/j.ejso.2011.10.013.CrossRefPubMed
87.
Zurück zum Zitat Kanzaki R, Higashiyama M, Fujiwara A, Tokunaga T, Maeda J, Okami J, Nishimura K, Kodama K: Long-term results of surgical resection for pulmonary metastasis from renal cell carcinoma: a 25-year single-institution experience. Eur J Cardiothorac Surg. 2011, 39: 167-172. 10.1016/j.ejcts.2010.05.021.CrossRefPubMed Kanzaki R, Higashiyama M, Fujiwara A, Tokunaga T, Maeda J, Okami J, Nishimura K, Kodama K: Long-term results of surgical resection for pulmonary metastasis from renal cell carcinoma: a 25-year single-institution experience. Eur J Cardiothorac Surg. 2011, 39: 167-172. 10.1016/j.ejcts.2010.05.021.CrossRefPubMed
88.
Zurück zum Zitat Rees M, Tekkis PP, Welsh FK, O’Rourke T, John TG: Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg. 2008, 247: 125-135. 10.1097/SLA.0b013e31815aa2c2.CrossRefPubMed Rees M, Tekkis PP, Welsh FK, O’Rourke T, John TG: Evaluation of long-term survival after hepatic resection for metastatic colorectal cancer: a multifactorial model of 929 patients. Ann Surg. 2008, 247: 125-135. 10.1097/SLA.0b013e31815aa2c2.CrossRefPubMed
89.
Zurück zum Zitat Konopke R, Kersting S, Distler M, Dietrich J, Gastmeier J, Heller A, Kulisch E, Saeger HD: Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases. Liver Int. 2009, 29: 89-102. 10.1111/j.1478-3231.2008.01845.x.CrossRefPubMed Konopke R, Kersting S, Distler M, Dietrich J, Gastmeier J, Heller A, Kulisch E, Saeger HD: Prognostic factors and evaluation of a clinical score for predicting survival after resection of colorectal liver metastases. Liver Int. 2009, 29: 89-102. 10.1111/j.1478-3231.2008.01845.x.CrossRefPubMed
90.
Zurück zum Zitat Malik HZ, Prasad KR, Halazun KJ, Aldoori A, Al-Mukhtar A, Gomez D, Lodge JP, Toogood GJ: Preoperative prognostic score for predicting survival after hepatic resection for colorectal liver metastases. Ann Surg. 2007, 246: 806-814. 10.1097/SLA.0b013e318142d964.CrossRefPubMed Malik HZ, Prasad KR, Halazun KJ, Aldoori A, Al-Mukhtar A, Gomez D, Lodge JP, Toogood GJ: Preoperative prognostic score for predicting survival after hepatic resection for colorectal liver metastases. Ann Surg. 2007, 246: 806-814. 10.1097/SLA.0b013e318142d964.CrossRefPubMed
91.
Zurück zum Zitat Minagawa M, Yamamoto J, Kosuge T, Matsuyama Y, Miyagawa S, Makuuchi M: Simplified staging system for predicting the prognosis of patients with resectable liver metastasis: development and validation. Arch Surg. 2007, 142: 269-276. 10.1001/archsurg.142.3.269. discussion 277CrossRefPubMed Minagawa M, Yamamoto J, Kosuge T, Matsuyama Y, Miyagawa S, Makuuchi M: Simplified staging system for predicting the prognosis of patients with resectable liver metastasis: development and validation. Arch Surg. 2007, 142: 269-276. 10.1001/archsurg.142.3.269. discussion 277CrossRefPubMed
92.
Zurück zum Zitat Lussier YA, Khodarev NN, Regan K, Corbin K, Li H, Ganai S, Khan SA, Gnerlich JL, Darga TE, Fan H, Karpenko O, Paty PB, Posner MC, Chmura SJ, Hellman S, Ferguson MK, Weichselbaum RR: Oligo- and polymetastatic progression in lung metastasis(es) patients is associated with specific microRNAs. PLoS One. 2012, 7: e50141-10.1371/journal.pone.0050141.PubMedCentralCrossRefPubMed Lussier YA, Khodarev NN, Regan K, Corbin K, Li H, Ganai S, Khan SA, Gnerlich JL, Darga TE, Fan H, Karpenko O, Paty PB, Posner MC, Chmura SJ, Hellman S, Ferguson MK, Weichselbaum RR: Oligo- and polymetastatic progression in lung metastasis(es) patients is associated with specific microRNAs. PLoS One. 2012, 7: e50141-10.1371/journal.pone.0050141.PubMedCentralCrossRefPubMed
Metadaten
Titel
Oligometastasis and oligo-recurrence: more than a mirage
verfasst von
Fang Huang
Gang Wu
Kunyu Yang
Publikationsdatum
01.12.2014
Verlag
BioMed Central
Erschienen in
Radiation Oncology / Ausgabe 1/2014
Elektronische ISSN: 1748-717X
DOI
https://doi.org/10.1186/s13014-014-0230-6

Weitere Artikel der Ausgabe 1/2014

Radiation Oncology 1/2014 Zur Ausgabe

Update Onkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.