Metastasis or recurrence of cancer has been considered as representing a near terminal life stage. As a result, for a long time, cancer patients with metastasis or recurrence have been classified as one group and treated using only systemic therapy. However, recent advances in cancer therapy have dramatically improved both local and systemic therapies. The concept of oligometastases was proposed by Hellman and Wechselbaum in 1995 [1] and revised by Niibe et al. in 2006 as oligo-recurrence [2]. These notions represent the first classification of metastasis or recurrence to identify subgroups for achieving long-term survival or even cure.
Oligometastases are defined as 1–5 distant metastases that can be treated by local therapy to achieve long-term survival or cure. The most important prognostic factor for oligometastases is the status of the primary lesion [3, 4]. Niibe et al. proposed the concept of oligo-recurrence to overcome this problem. Oligo-recurrence is thus defined as 1–5 distant metachronous metastases that can be treated by local therapy, under conditions of a controlled primary lesion. More favorable subgroups of oligometastases have subsequently been classified. Niibe et al. proposed the classification and naming of sync-oligometastases and oligo-recurrences [3]. Sync-oligometastasis indicates a state of oligometastases with active but controllable primary lesions. This classification appears reasonable.
Based on a review of the literature, we propose a more detailed classification of metastases and recurrence. Table 1 shows the Niibe-Onishi-Chang classification, which includes not only oligometastases, but also polymetastases. Oligometastases and oligo-recurrences usually offer a better prognosis than polymetastases. However, oligometastases and oligo-recurrence are cancer- and organ-specific. The appearance status of oligometastases or oligo-recurrence is thus sometimes equivalent to polymetastases such as in pancreatic cancer, sarcoma, or malignant melanoma, although the last one is related to the abscopal effect, a key cure-related phenomenon for oligometastases and oligo-recurrences [5–7]. Among oligometastases and oligo-recurrences, patients with 1-2 metastases and recurrences reportedly show better prognosis than those with 3–5 metastases and recurrences [8]. In oligo-recurrence of NSCLC in only the brain or adrenal gland, patients achieve favorable survival [4, 9]. Lung or liver metastases of colon or rectal cancer are also be associated with favorable survival [10, 11]. Patients with oligo-recurrence of renal cell carcinoma also achieve long-term survival [12]. In sync-oligometastases of NSCLC affecting only the brain or adrenal gland, patients reportedly achieve relatively favorable survival [9, 13]. In sync-oligometastases of colon and rectal cancer, renal cell cancer also reportedly shows relatively favorable survival [10–12]. In oligo-recurrence of breast cancer, patients are reported to achieve relatively favorable survival [14, 15]. Niibe et al. reported that all seven of breast cancer patients with bone-only oligo-recurrence were still alive at the last followup (median followup, 40 months). In sync-oligometastases of SCLC, several cases have been reported to survive more than 5 years [16, 17]. Patients with metastatic pancreatic cancer, sarcoma, or melanoma reportedly display unfavorable outcomes [18–20].
Niibe-Onishi-Chang classification.
Favorable
Intermediate
Unfavorable
Relatively favorable
Relatively unfavorable
OligorecurrenceSite no. 1-2NSCLC (brain and adrenal gland)Colon and rectum cancer (lung and liver)Renal cell cancer
oligo-recurrencesite no. 1-2breast cancer (bone, lung, and liver)SCLC (brain)site no. 3–5NSCLC (brain and adrenal gland)colon and rectum cancer (lung and liver)renal cell cancer
oligo-recurrencesite no. 3–5breast cancer (bone, lung, and liver)SCLC (brain)
Oligometastases and oligo-recurrencepancreatic cancer (any site)melanoma (any site)sarcoma (any site)
sync-oligometastasessite no. 1-2NSCLC (brain and adrenal gland)colon and rectum cancer (lung and liver)renal cell cancer
sync-oligometastasessite no. 3–5NSCLC (brain and adrenal gland)colon and rectum cancer (lung and liver)breast cancer (bone, lung, and liver)
polymetastases
This new classification, the Niibe-Onishi-Chang classification, should be revised in the future due to the rapid improvements being achieved in local and systemic therapies for cancer. This classification is tentative, but is very important given the fact that even a decade ago, many oncologists considered patients with metastasis and recurrence in only a single group.
Yuzuru NiibeJoe Y. ChangHiroshi OnishiJoseph SalamaTakao HirakiHideomi Yamashita
HellmanS.WechselbaumR. R.Oligometastases1995131810NiibeY.KazumotoT.ToitaT.Frequency and characteristics of isolated para-aortic lymph node recurrence in patients with uterine cervical carcinoma in Japan: a multi-institutional study2006103243543810.1016/j.ygyno.2006.03.034NiibeY.NishimuraT.InoueT.KarasawaK.ShioyamaY.OgawaY.TakemotoM.ShiratoH.Oligometastases of brain only in patients with non-small cell lung cancer (NSCLC) treated with stereotactic irradiation (STI): a multi-institutional study in Japan783S497Lopez GuerraJ. L.GomezD.ZhuangY.HongD. S.HeymachJ. V.SwisherS. G.LinS. H.KomakiR.CoxJ. D.LiaoZ.Prognostic impact of radiation therapy to the primary tumor in patients with non-small cell lung cancer and oligometastasis at diagnosis2012841e61e6710.1016/j.ijrobp.2012.02.054PostowM. A.CallahanM. K.BarkerC. A.YamadaY.YuanJ.KitanoS.MuZ.RasalanT.AdamowM.RitterE.SedrakC.JungbluthA. A.ChuaR.YangA. S.RomanR. A.RosnerS.BensonB.AllisonJ. P.LesokhinA. M.GnjaticS.WolchokJ. D.Immunologic correlates of the abscopal effect in a patient with melanoma20123661092593110.1056/NEJMoa1112824TakayaM.NiibeY.TsunodaS.JoboT.ImaiM.KotaniS.UnnoN.HayakawaK.Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma: a case report2007271B4995032-s2.0-33847712185OkumaK.YamashitaH.NiibeY.HayakawaK.NakagawaK.Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: a case report20115, article 1112-s2.0-7995270411410.1186/1752-1947-5-111SalamaJ. K.ChmuraS. J.MehtaN.YeniceK. M.StadlerW. M.VokesE. E.HarafD.HellmanS.WeichselbaumR. R.An initial report of a radiation dose-escalation trial in patients with one to five sites of metastatic disease20081416525552592-s2.0-5264908824610.1158/1078-0432.CCR-08-0358HolyR.PirothM.PinkawaM.EbleM. J.Stereotactic Body Radiation Therapy (SBRT) for treatment of adrenal gland metastases from non-small cell lung cancer201118742452512-s2.0-7995570915510.1007/s00066-011-2192-zRicardiU.FilippiA. R.GuarneriA.RagonaR.MantovaniC.GiglioliF.BotticellaA.CiammellaP.IftodeC.BuffoniL. L.RuffiniE.ScagliottiG. V.Stereotactic boby radiation therapy for lung metastases2012751778110.1016/j.lungcan.2011.04.021RusthovenK. E.KavanaghB. D.CardenesH.StieberV. W.BurriS. H.FeigenbergS. J.ChidelM. A.PughT. J.FranklinW.KaneM.GasparL. E.SchefterT. E.Multi-institutional phase I/II trial of stereotactic body radiation therapy for liver metastases200927101572157810.1200/JCO.2008.19.6329RanckM. C.GoldenD. W.CorbinK. S.HasselleM. D.LiauwS. L.StadlerW. M.HahnO. M.WeichselbaumR. R.SalamaJ. K.Stereotactic body radiotherapy for the treatment of oligometastatic renal cell carcinomaAmerican Journal of Clinical Oncology. In pressHuC.ChangE. L.HassenbuschS. J.IIIAllenP. K.WooS. Y.MahajanA.KomakiR.LiaoZ.Nonsmall cell lung cancer presenting with synchronous solitary brain metastasis20061069199820042-s2.0-3364636458010.1002/cncr.21818NiibeY.KuranamiM.MatsunagaK.TakayaM.KakitaS.HaraT.SekiguchiK.WatanabeM.HayakawaK.Value of high-dose radiation therapy for isolated osseous metastasis in breast cancer in terms of oligo-recurrence2008286B392939312-s2.0-58149173509KagaraN.NakanoY.WatanabeA.InatomeJ.NakamuraH.KimC.DannoK.TaniguchiH.KanohT.KimuraY.OhnishiT.TonoT.MondenT.ImaokaS.KagawaK.Curative-intent stereotactic body radiation therapy for residual breast cancer liver metastasis after systemic chemotherapyBreast Cancer. In press2-s2.0-7995973917910.1007/s12282-011-0290-5NiibeY.KarasawaK.HayakawaK.Ten-year disease-free survival of a small cell lung cancer patient with brain metastasis treated with chemoradiotherapy2004243B209721002-s2.0-3242738552ImaiR.HayakawaK.SakuraiH.NakayamaY.MitsuhashiN.NiibeH.Small cell lung cancer with a brain metastasis controlled for 5 years: a case report200131311611810.1093/jjco/hye0242-s2.0-0035027861FrigeriM.De DossoS.Castillo-FernandezO.FeuerleinK.NeuenschwanderH.SalettiP.Chemotherapy in patients with advanced pancreatic cancer: too close ro death?201321115716310.1007/s00520-012-1505-9van der GraafW. T.BlavJ. Y.ChawlaS. P.Pazopanib for metastatic soft-tissue sarcoma (PALETTE): a randomized, double-blind, placebo-controlled phase 3 trial2012379982918791886MateusC.RobertC.Major therapeutic advances in the treatment of metastatic melanoma2012996619625