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A Patient-Level Data Meta-analysis of the Abscopal Effect

Open AccessPublished:March 03, 2022DOI:https://doi.org/10.1016/j.adro.2022.100909

      Abstract

      Purpose

      The abscopal effect is defined when a form of local therapy causes tumor regression of both the target lesion and any untreated tumors. Herein cases of the abscopal effect were systematically reviewed and a patient-level data analysis was performed for clinical predictors of both duration of response and survival.

      Methods and Materials

      The Population, Intervention, Control, Outcome, Study (PICOS) design approach, Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) literature selection process, and Meta-analysis of Observational Studies in Epidemiology (MOOSE) were used to find articles published before September 2019 in MEDLINE/PubMed and Google Scholar. Inclusion criteria were (1) population: patients with reported abscopal response; (2) intervention: documented treatment(s); (3) control: none; (4) outcomes: overall and progression-free survival; and (5) setting: retrospective case reports. Time from treatment until abscopal response and time from abscopal response until progression/death were calculated. Univariate and multivariate analyses were conducted for survival outcomes.

      Results

      Fifty studies (n = 55 patients) were included. Median age was 65 years (interquartile range [IQR], 58-70) and 62% were male. Fifty-four (98%) patients received radiation therapy, 34 (62%) received radiation therapy alone, 5 (9.1%) underwent surgery, 4 (7.3%) received chemotherapy, and 11 (20%) received immunotherapy. Median total dose was 32 Gy (IQR, 25.5-48 Gy) and median dose per fraction was 3 Gy (IQR, 2-7.2). Median time until abscopal response was 4 months (IQR, 1-5; min 0.5, max 24). At 5 years, overall survival was 63% and distant progression-free survival was 45%. No variables had statistical significance in predicting duration of response or survival.

      Conclusions

      Almost all reported cases of the abscopal response are after radiation therapy; however, there are no known predictors of duration of response or survival in this population.

      Introduction

      The abscopal effect is defined when a form of local therapy (eg, radiation therapy [RT]) causes tumor regression of both the target lesion and any untreated tumors. Precise biological mechanisms are unknown, but the immune system may be integral in abscopal responses (Fig. 1).
      • Liu Y
      • Dong Y
      • Kong L
      • Shi F
      • Zhu H
      • Yu J.
      Abscopal effect of radiotherapy combined with immune checkpoint inhibitors.
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      • Venkat P
      • Kim S.
      Systematic review of case reports on the abscopal effect.
      • Siva S
      • MacManus MP
      • Martin RF
      • Martin OA.
      Abscopal effects of radiation therapy: A clinical review for the radiobiologist.
      Owing to promising preclinical data, interest exists in combining immunotherapy with hypofractionated RT to stimulate abscopal responses
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      Immunomodulatory effects of stereotactic body radiation therapy: Preclinical insights and clinical opportunities.
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      DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity.
      • Deng L
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      • Burnette B
      • et al.
      Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice.
      • Lan J
      • Li R
      • Yin LM
      • et al.
      Targeting myeloid-derived suppressor cells and programmed death ligand 1 confers therapeutic advantage of ablative hypofractionated radiation therapy compared with conventional fractionated radiation therapy.
      and improve patient outcomes.
      • Liu Y
      • Dong Y
      • Kong L
      • Shi F
      • Zhu H
      • Yu J.
      Abscopal effect of radiotherapy combined with immune checkpoint inhibitors.
      ,
      • Wani SQ
      • Dar IA
      • Khan T
      • Lone MM
      • Afroz F.
      Radiation therapy and its effects beyond the primary target: an abscopal effect.
      • Dagoglu N
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      • Oral EN.
      Abscopal effect of radiotherapy in the immunotherapy era: Systematic review of reported cases.
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      • De Ruysscher D.
      The abscopal effect of local radiotherapy: Using immunotherapy to make a rare event clinically relevant.
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      • Rezaeyan A
      • Najafi M
      Abscopal effect in radioimmunotherapy.
      • Xing D
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      • Hanna GG.
      The abscopal effect of stereotactic radiotherapy and immunotherapy: Fool's gold or El Dorado?.
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      Immunological mechanisms responsible for radiation-induced abscopal effect.
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      • Koller KM
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      • et al.
      Improved survival and complete response rates in patients with advanced melanoma treated with concurrent ipilimumab and radiotherapy versus ipilimumab alone.
      • Parker CC
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      • Brawley CD
      • et al.
      Radiotherapy to the primary tumour for newly diagnosed, metastatic prostate cancer (STAMPEDE): A randomised controlled phase 3 trial.
      • Ngwa W
      • Irabor OC
      • Schoenfeld JD
      • Hesser J
      • Demaria S
      • Formenti SC.
      Using immunotherapy to boost the abscopal effect.
      Various mechanisms have been proposed to explain how radiation interacts with the immune system.
      • Reynders K
      • Illidge T
      • Siva S
      • Chang JY
      • De Ruysscher D.
      The abscopal effect of local radiotherapy: Using immunotherapy to make a rare event clinically relevant.
      • Ashrafizadeh M
      • Farhood B
      • Eleojo Musa A
      • Taeb S
      • Rezaeyan A
      • Najafi M
      Abscopal effect in radioimmunotherapy.
      • Xing D
      • Siva S
      • Hanna GG.
      The abscopal effect of stereotactic radiotherapy and immunotherapy: Fool's gold or El Dorado?.
      ,
      • Brooks ED
      • Chang JY.
      Time to abandon single-site irradiation for inducing abscopal effects.
      Synergistic RT and immunotherapy have been shown to promote local immune responses
      • Marciscano AE
      • Haimovitz-Friedman A
      • Lee P
      • et al.
      Immunomodulatory effects of stereotactic body radiation therapy: Preclinical insights and clinical opportunities.
      • Vanpouille-Box C
      • Alard A
      • Aryankalayil MJ
      • et al.
      DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity.
      • Deng L
      • Liang H
      • Burnette B
      • et al.
      Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice.
      • Lan J
      • Li R
      • Yin LM
      • et al.
      Targeting myeloid-derived suppressor cells and programmed death ligand 1 confers therapeutic advantage of ablative hypofractionated radiation therapy compared with conventional fractionated radiation therapy.
      ,
      • Rodríguez-Ruiz ME
      • Vanpouille-Box C
      • Melero I
      • Formenti SC
      • Demaria S.
      Immunological mechanisms responsible for radiation-induced abscopal effect.
      and have been hypothesized to improve the probability of tumor control.
      • Ashrafizadeh M
      • Farhood B
      • Eleojo Musa A
      • Taeb S
      • Rezaeyan A
      • Najafi M
      Abscopal effect in radioimmunotherapy.
      As a brief review, high dose per fraction RT has been shown to stimulate tumor associated antigen presentation and causes an increased ratio of immunologic cell death to tolerogenic responses, which stimulates CD8+ T lymphocytes, dendritic cells, and natural killer cells.
      • Ashrafizadeh M
      • Farhood B
      • Eleojo Musa A
      • Taeb S
      • Rezaeyan A
      • Najafi M
      Abscopal effect in radioimmunotherapy.
      Immune checkpoint inhibitors prevent immune tolerance of tumor cells by blocking tumor cell escape from immune surveillance via cellular targets (ie, Programmed Cell Death-1 and Cytotoxic T-Lymphocyte Antigen-4), which are expressed by tumor suppressor cells (CD4+ T lymphocytes, CD8+ T lymphocytes, dendritic cells, and natural killer cells).
      • Marciscano AE
      • Haimovitz-Friedman A
      • Lee P
      • et al.
      Immunomodulatory effects of stereotactic body radiation therapy: Preclinical insights and clinical opportunities.
      • Vanpouille-Box C
      • Alard A
      • Aryankalayil MJ
      • et al.
      DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity.
      • Deng L
      • Liang H
      • Burnette B
      • et al.
      Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice.
      • Lan J
      • Li R
      • Yin LM
      • et al.
      Targeting myeloid-derived suppressor cells and programmed death ligand 1 confers therapeutic advantage of ablative hypofractionated radiation therapy compared with conventional fractionated radiation therapy.
      ,
      • Ashrafizadeh M
      • Farhood B
      • Eleojo Musa A
      • Taeb S
      • Rezaeyan A
      • Najafi M
      Abscopal effect in radioimmunotherapy.
      ,
      • Rodríguez-Ruiz ME
      • Vanpouille-Box C
      • Melero I
      • Formenti SC
      • Demaria S.
      Immunological mechanisms responsible for radiation-induced abscopal effect.
      These synergistic effects were thought to prime the immune system and induce an abscopal response.
      Previous systematic reviews have examined the abscopal effect
      • Abuodeh Y
      • Venkat P
      • Kim S.
      Systematic review of case reports on the abscopal effect.
      ,
      • Dagoglu N
      • Karaman S
      • Caglar HB
      • Oral EN.
      Abscopal effect of radiotherapy in the immunotherapy era: Systematic review of reported cases.
      ; however, data on progression-free survival, distant metastasis, and overall survival were not reported; use of systemic therapies (including immune checkpoint inhibitors) were not routinely mentioned; and analyses for predictors of response were not performed. The hypothesis was that certain clinical covariates might predict for survival of patients with an abscopal response. Thus, we performed the first patient-level data meta-analysis for predictors of response.

      Methods and Materials

      Literature selection

      The Population, Intervention, Control, Outcome, Study (PICOS) design approach was used to define the inclusion criteria (Table 1). A systematic search was performed using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) literature selection process (Fig. 2) of studies in MEDLINE (PubMed) and Google Scholar. Inclusion criteria were (1) population: patients with reported abscopal response, which was defined by any form of local therapy causing regression of both the target lesion and any untreated tumors; (2) intervention: documented treatment(s); (3) control: none; (4) outcomes: overall and progression-free survival; and (5) setting: retrospective case reports.
      Table 1PICOS inclusion criteria
      PopulationCase reports of the abscopal effect published before September 26, 2019.
      InterventionClearly defined cancer therapy at time of abscopal response and prior courses of treatment (eg, radiation therapy, immunotherapy, chemotherapy, target therapy).
      ControlNone.
      OutcomesOverall and progression-free survival.

      Time from treatment until abscopal response and time from abscopal response until progression or death were calculated. For overall and progression-free survival, the start time was calculated from the time of abscopal effect.
      Study designCase reports and case series published in the English literature.
      Abbreviation: PICOS = Population, Intervention, Control, Outcome, Study.
      Fig 2
      Figure 2Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram.
      This method of a patient-level data meta-analysis has been described previously in the literature.
      • Lehrer EJ
      • Peterson J
      • Brown PD
      • et al.
      Treatment of brain metastases with stereotactic radiosurgery and immune checkpoint inhibitors: An international meta-analysis of individual patient data.
      ,
      • Cummings M
      • Lehrer EJ
      • Drabick JJ
      • Gusani NJ
      • Trifiletti DM
      • Zaorsky NG.
      Exceptional responders in oncology: A systematic review and meta-analysis of patient level data.
      Relevant case reports were systematically identified through a search of PubMed/MEDLINE and Google Scholar with the broad term “abscopal effect.” The initial search yielded 701 articles. Reports that were cited or linked from any review articles and the individual case reports were included. After identifying 98 articles, 4 were rejected because they were not case reports. The remaining articles were screened by the first author (S.J.H.) and were included based upon the aforementioned criteria. Patients could receive any combination of treatment: surgery, RT, immunotherapy, chemotherapy, or targeted therapy for any malignancy. Finally, 50 studies including 55 patients were included.

      Data abstraction and analysis

      The definition for the start time of an abscopal effect was marked by any regression at an untreated tumor site as noted by imaging, per the report of primary authors from each case report. Individual case reports were reviewed by authors and information was manually extracted and coded into a database. The following data were coded from each case report: characteristics about patients (ie, age, sex), cancer (ie, type [per National Comprehensive Cancer Network guidelines], histology, mutation, stage), treatments received at any point before an abscopal response (ie, surgery, radiation, chemotherapy, immunotherapy), radiation dose (ie, Gy, dose/Gy, biologically effective dose with an α/β of 10), treatment received during the abscopal response (eg, radiation, chemotherapy, immunotherapy, target therapy), time from radiation to an abscopal effect, interval of follow- up/recurrence, and outcomes (ie, overall survival and distant progression-free survival at last known contact date). Unknown/missing variables were coded as missing in the database.

      Results

      The data of both patient and cancer characteristics are in Table 2. Fifty studies (n = 55 patients) published from 1954 to 2019 met inclusion criteria and were used.
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      • Matsushita Y
      • Nakamura K
      • Furuse H
      • Ichinohe K
      • Miyake H.
      Marked response to nivolumab combined with external radiation therapy for metastatic renal cell carcinoma: Report of two cases.
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      • MacManus MP
      • Hofman MS
      • Hicks RJ
      • et al.
      Abscopal regressions of lymphoma after involved-site radiation therapy confirmed by positron emission tomography.
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      • Leung HWC
      • Wang SY
      • Jin-Jhih H
      • Chan ALF
      Abscopal effect of radiation on bone metastases of breast cancer: A case report.
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      • Tubin S
      • Raunik W.
      Hunting for abscopal and bystander effects: Clinical exploitation of non-targeted effects induced by partial high-single-dose irradiation of the hypoxic tumour segment in oligometastatic patients.
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      • Sham RL.
      The abscopal effect and chronic lymphocytic leukemia.
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      • Rees GJG
      • Ross CMD.
      Abscopal regression following radiotherapy for adenocarcinoma.
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      • Nakanishi M
      • Chuma M
      • Hige S
      • Asaka M.
      Abscopal effect on hepatocellular carcinoma.
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      • Bruton Joe M
      • Truong PT.
      Abscopal effect after palliative radiation therapy for metastatic adenocarcinoma of the esophagus.
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      • Ebner DK
      • Kamada T
      • Yamada S.
      Abscopal effect in recurrent colorectal cancer treated with carbon-ion radiation therapy: 2 case reports.
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      • Antoniades J
      • Brady LW
      • Lightfoot DA.
      Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas.
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      • Masue N
      • Hasegawa Y
      • Moriyama Y
      • Ikeda Y
      • Gotoh T
      • Deguchi T.
      Spontaneous disappearance of multiple lung metastases after nephroureterectomy from sarcomatoid carcinoma of the renal pelvis: A case report.
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      The median patient age was 65 years (interquartile range [IQR], 57-70), and there were 34 (62%) men and 21 (38%) women. Although all patients had metastatic disease at the time of the abscopal effect, only 17 (31%) patients initially presented with a metastatic tumor, and all others had recurrences after initially localized disease. Sixty-seven percent of patients had 5 cancer types: non-small cell lung cancer (NSCLC) (10, 18%),
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      ,
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      ,
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      ,
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      ,
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      ,
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      ,
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      kidney (9, 16%),
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      ,
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      ,
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.
      ,
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      ,
      • Masue N
      • Hasegawa Y
      • Moriyama Y
      • Ikeda Y
      • Gotoh T
      • Deguchi T.
      Spontaneous disappearance of multiple lung metastases after nephroureterectomy from sarcomatoid carcinoma of the renal pelvis: A case report.
      melanoma (7, 13%),
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      ,
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      ,
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      ,
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      ,
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      ,
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      lymphoma (6, 11%),
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      ,
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      ,
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      ,
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      ,
      • Antoniades J
      • Brady LW
      • Lightfoot DA.
      Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas.
      and hepatobiliary (5, 9.1%).
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      ,
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      ,
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      • Nakanishi M
      • Chuma M
      • Hige S
      • Asaka M.
      Abscopal effect on hepatocellular carcinoma.
      Table 2Included articles demonstrating abscopal effect
      StudyYearTrue defined
      Refers to whether or not the article demonstrates a true abscopal response (as defined by the result of any local therapy affecting a distant, untreated tumor).
      SexAgeCancer typeRT to primaryRT to metastasisRT at multiple sitesRT total dose (Gy)RT fxAverage RT dose/fx (Gy)BEDRT onlyRT + surgeryRT + chemotherapyRT + ITFollow- up time (mo)OutcomeNew met
      Cotter et al
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      2011YM7039NYN122619.2YNNN25AliveY
      Ebner et al
      • Ebner DK
      • Kamada T
      • Yamada S.
      Abscopal effect in recurrent colorectal cancer treated with carbon-ion radiation therapy: 2 case reports.
      2017YM7513NYN73.6164.6107YNNN46DeadY
      YM8513NYN50.4124.271.5YNNN92AliveN
      Fairlamb
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      1981YF7323NYN40152.750.6YNNN56AliveY
      Golden et al
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      2013YM6441NYN305648NNNY10AliveY
      Antoniades et al
      • Antoniades J
      • Brady LW
      • Lightfoot DA.
      Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas.
      1977YM4455YNN30201.534.5YNNN-AliveN
      YM4055YNN30201.534.5YNNN-AliveN
      Cong et al
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      2017YF6441YNN37.557.565.6NNNY-AliveN
      Desar et al
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      2016YM1947NYN3010339YNNN6DeadY
      Joe et al
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      2017YF5714YYY54301.863.7NNYN48AliveN
      Lakshmanagowda et al
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      2009YF6555YNN2412228.8YNNN6AliveN
      MacManus et al
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      1994YM5823YNN2010224YNNN9DeadN
      Nam et al
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      2005YM6521NYN30---YNNN15AliveN
      Ohba et al
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      1998YM7621NYN36---YNNN25AliveN
      Okuma et al
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      2011YM6321NYN60.8272.274.4YNNN54AliveN
      Postow et al
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      2012YF3325NYN28.539.555.5NNNY10AliveN
      Rees and Ross
      • Rees GJG
      • Ross CMD.
      Abscopal regression following radiotherapy for adenocarcinoma.
      1983YM4916YNN4020248YNNN20Dead-
      Robins et al
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      1981YF5955NYN2010224YNNN4DeadY
      Stamell et al
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      2012YM6725YNN243843.2YNNN84AliveY
      Takaya et al
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      2007YF6910YNY22102.226.8YNNN12AliveN
      Wersäll et al
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      2009YF8323YNN324857.6YNNN-AliveN
      YF6423NYN----NNYN54AliveN
      YM6923NYN3021575YNNN24AliveY
      YF5523YNN324857.6YNNN-AliveN
      Sullivan et al
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      2013YM6825NYN----NNNN13AliveN
      Hiniker et al
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      2012Y--25NYN----NNNY-AliveN
      Isobe et al
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      2009NF6555NNN40---NNNN60AliveN
      Joe et al
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      2018YM7416YYY3010339YNNN14AliveN
      Kodama et al
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      2013YM7441NYY4824257.6NNNY61DeadY
      Nakanishi et al
      • Nakanishi M
      • Chuma M
      • Hige S
      • Asaka M.
      Abscopal effect on hepatocellular carcinoma.
      2008YM7921YNN48148278YNNN-AliveN
      Okwan-Duodu et al
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      2015YF5025NYN----NYNY20AliveY
      Hamilton et al
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      2018YM4741NYN255537.5NYNN7AliveN
      Gutkin et al
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      2018YM5725NYN54318151NNNY78AliveY
      Chino et al
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      2018YM5841NYN6087.5105YNNN18AliveN
      Leung et al
      • Leung HWC
      • Wang SY
      • Jin-Jhih H
      • Chan ALF
      Abscopal effect of radiation on bone metastases of breast cancer: A case report.
      2018YF657YYY2251515562YNNN60AliveN
      Sperduto et al
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      2017YF3625NYY255537.5NYYN120AliveN
      Van de Walle et al
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      2016YF6623NYN3913350.7YNNN17AliveY
      Zhao et al
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      2018YM6516NYN426771.4YNNN15AliveN
      Katayama et al
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      2017YM6341NYY4515358.5YNNN9AliveN
      Britschgi et al
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      2018YM4741NYN183628.8NNNY24AliveN
      Kim and Kim
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      2019YM7021YNN48412105NYNN21AliveN
      Bitran
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      2019YF6241YNN279335.1NNNY54AliveN
      Shinde et al
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      2019YM7520YNY14.827.425.7NNNY10AliveN
      Lin et al
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      2019YM7141NYN488676.8YNNN19AliveY
      Brenneman et al
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      2019YF6747YNN5025260YNNN18AliveN
      Sato et al
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      2016YM5418YNN4824257.6NNNY5DeadY
      Shi et al
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      2017YF6743YNN4515358.5NYNN1DeadN
      Hidaka et al
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      2017YM8855YNY328444.8YNNN6DeadN
      Barsky et al
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      2019YM6724YNN3010339NNYN7DeadN
      Siva et al
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      2013YF7841YNY6030272YNNN2AliveY
      Ishiyama et al
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.
      2012YM6123NYY1811850.4YNNN34AliveY
      Poon and Wong
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      2017YM7945NYY244638.4YNNN6AliveN
      Azami et al
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      2018YF647YYY6030272YNNN21AliveN
      Masue et al
      • Masue N
      • Hasegawa Y
      • Moriyama Y
      • Ikeda Y
      • Gotoh T
      • Deguchi T.
      Spontaneous disappearance of multiple lung metastases after nephroureterectomy from sarcomatoid carcinoma of the renal pelvis: A case report.
      2007NM5823NNN----NNNN46AliveN
      Agyeman et al
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      2019YM5647YNN4020248YNNN17AliveN
      Abbreviations: BED = biologically effective dose, assuming an α:β ratio of 10; fx = fraction; IT = immunotherapy; met = metastasis; RT = radiation therapy.
      low asterisk Refers to whether or not the article demonstrates a true abscopal response (as defined by the result of any local therapy affecting a distant, untreated tumor).
      Data pertinent to treatment characteristics are in Table 2. Treatment analysis was broken up into 3 phases: (1) prior treatment course, (2) treatment course leading up to an abscopal response, and (3) treatment during or after an abscopal response. All but 1 patient
      • Masue N
      • Hasegawa Y
      • Moriyama Y
      • Ikeda Y
      • Gotoh T
      • Deguchi T.
      Spontaneous disappearance of multiple lung metastases after nephroureterectomy from sarcomatoid carcinoma of the renal pelvis: A case report.
      received RT either at the time of an abscopal response or in prior courses of therapy. (1) Prior treatment courses were as follows (treatments in this phase were not mutually exclusive): 9 (16%) had RT,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      ,
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      ,
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      ,
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      26 (47%) had surgery,
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      ,
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      ,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      ,
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      ,
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      ,
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      ,
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      • Ebner DK
      • Kamada T
      • Yamada S.
      Abscopal effect in recurrent colorectal cancer treated with carbon-ion radiation therapy: 2 case reports.
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      ,
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      • Masue N
      • Hasegawa Y
      • Moriyama Y
      • Ikeda Y
      • Gotoh T
      • Deguchi T.
      Spontaneous disappearance of multiple lung metastases after nephroureterectomy from sarcomatoid carcinoma of the renal pelvis: A case report.
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      23 (42%) had chemotherapy,
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      ,
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      ,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      ,
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      ,
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      ,
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      ,
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      ,
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      ,
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      ,
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      ,
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      ,
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      ,
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      ,
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      ,
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      and 14 (25%) had immunotherapy.
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      ,
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      ,
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      ,
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      ,
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      ,
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      ,
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      ,
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      ,
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      (2) During the course of treatment leading up to an abscopal response, 34 (62%) patients received RT alone,
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      ,
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      • Leung HWC
      • Wang SY
      • Jin-Jhih H
      • Chan ALF
      Abscopal effect of radiation on bone metastases of breast cancer: A case report.
      ,
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      ,
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      ,
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      ,
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      ,
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      ,
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      • Rees GJG
      • Ross CMD.
      Abscopal regression following radiotherapy for adenocarcinoma.
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      ,
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      ,
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      ,
      • Nakanishi M
      • Chuma M
      • Hige S
      • Asaka M.
      Abscopal effect on hepatocellular carcinoma.
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      ,
      • Bruton Joe M
      • Truong PT.
      Abscopal effect after palliative radiation therapy for metastatic adenocarcinoma of the esophagus.
      ,
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.
      ,
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      • Ebner DK
      • Kamada T
      • Yamada S.
      Abscopal effect in recurrent colorectal cancer treated with carbon-ion radiation therapy: 2 case reports.
      ,
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      ,
      • Antoniades J
      • Brady LW
      • Lightfoot DA.
      Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas.
      ,
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      ,
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      5 (9.1%) underwent surgery with RT,
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      ,
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      ,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      ,
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      4 (7.3%) received chemotherapy with RT,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      ,
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      and 11 (20%) received immunotherapy with RT.
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      ,
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      ,
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      ,
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      ,
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      ,
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      ,
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      ,
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      (3) Treatments during or after the abscopal response were as follows: 22 (40%) patients received RT only to their primary tumor
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      ,
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      ,
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      ,
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      ,
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      ,
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      ,
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      ,
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      ,
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      ,
      • Rees GJG
      • Ross CMD.
      Abscopal regression following radiotherapy for adenocarcinoma.
      ,
      • Nakanishi M
      • Chuma M
      • Hige S
      • Asaka M.
      Abscopal effect on hepatocellular carcinoma.
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      ,
      • Stamell EF
      • Wolchok JD
      • Gnjatic S
      • Lee NY
      • Brownell I.
      The abscopal effect associated with a systemic anti-melanoma immune response.
      ,
      • Antoniades J
      • Brady LW
      • Lightfoot DA.
      Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas.
      ,
      • Agyeman MB
      • Vanderpuye VD
      • Yarney J.
      Abscopal effect of radiotherapy in imatinib-resistant dermatofibrosarcoma protuberans.
      and 29 (53%) received RT only to a metastasis.
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      ,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      ,
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      ,
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      ,
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      ,
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      ,
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      ,
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      ,
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      ,
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      ,
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.
      • Hiniker SM
      • Chen DS
      • Knox SJ.
      Abscopal effect in a patient with melanoma.
      • Fairlamb DJ.
      Spontaneous regression of metastases of renal cancer: A report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature.
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      ,
      • Ebner DK
      • Kamada T
      • Yamada S.
      Abscopal effect in recurrent colorectal cancer treated with carbon-ion radiation therapy: 2 case reports.
      ,
      • Postow MA
      • Callahan MK
      • Barker CA
      • et al.
      Immunologic correlates of the abscopal effect in a patient with melanoma.
      ,
      • Golden EB
      • Demaria S
      • Schiff PB
      • Chachoua A
      • Formenti SC.
      An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer.
      ,
      • Cotter SE
      • Dunn GP
      • Collins KM
      • et al.
      Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: Potential role of induced antitumor immunity.
      Three (5.5%) patients received RT to both the primary tumor and a metastasis,
      • Leung HWC
      • Wang SY
      • Jin-Jhih H
      • Chan ALF
      Abscopal effect of radiation on bone metastases of breast cancer: A case report.
      ,
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      ,
      • Bruton Joe M
      • Truong PT.
      Abscopal effect after palliative radiation therapy for metastatic adenocarcinoma of the esophagus.
      but still experienced the abscopal response at a distant site from radiation (Table 2). Only 1 (1.8%) patient did not receive RT during the course of treatment leading to an abscopal response, but had a history of prior RT (Table 2).
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      Targeted therapy was documented in 8 (15%) cases.
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      ,
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      ,
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      ,
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      ,
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      ,
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      ,
      • Desar IME
      • Braam PM
      • Kaal SEJ
      • Gerritsen WR
      • Oyen WJG
      • van der Graaf WTA.
      Abscopal effect of radiotherapy in a patient with metastatic diffuse-type giant cell tumor.
      ,
      • Cong Y
      • Shen G
      • Wu S
      • Hao R.
      Abscopal regression following SABR for non-small-cell-lung cancer: A case report.
      The median reported radiation dose and dose per fraction were 32 Gy (IQR, 25.5-48 Gy; min 12 Gy, max 73.6 Gy) and 3 Gy per fraction (IQR, 2-7.2 Gy per fraction; min 1.5 Gy per fraction, max 48 Gy per fraction).
      Ninety-six percent of the articles selected in this work demonstrated a clear abscopal effect as defined by the result of any local therapy affecting a distant, untreated tumor (Table 2). The median time until an abscopal effect was 3 months (IQR, 1-5; min 0.5, max 24). Median follow-up time after the abscopal effect was 18.5 months.
      • Zhao X
      • Kang J
      • Zhao R.
      Abscopal effect of radiation on lymph node metastasis in esophageal carcinoma: A case report and literature review.
      • Van de Walle M
      • Demol J
      • Staelens L
      • Rottey S.
      Abscopal effect in metastatic renal cell carcinoma.
      • Hamilton AJ
      • Seid J
      • Verdecchia K
      • Chuba P.
      Abscopal effect after radiosurgery for solitary brain metastasis from non-small cell lung cancer.
      • Matsushita Y
      • Nakamura K
      • Furuse H
      • Ichinohe K
      • Miyake H.
      Marked response to nivolumab combined with external radiation therapy for metastatic renal cell carcinoma: Report of two cases.
      • Shi F
      • Wang X
      • Teng F
      • Kong L
      • Yu J.
      Abscopal effect of metastatic pancreatic cancer after local radiotherapy and granulocyte-macrophage colony-stimulating factor therapy.
      ,
      • Sperduto W
      • King DM
      • Watanabe Y
      • Lou E
      • Sperduto PW.
      Case report of extended survival and quality of life in a melanoma patient with multiple brain metastases and review of literature.
      • Shinde A
      • Novak J
      • Freeman ML
      • Glaser S
      • Amini A.
      Induction of the abscopal effect with immunotherapy and palliative radiation in metastatic head and neck squamous cell carcinoma: A case report and review of the literature.
      • MacManus MP
      • Hofman MS
      • Hicks RJ
      • et al.
      Abscopal regressions of lymphoma after involved-site radiation therapy confirmed by positron emission tomography.
      • Sato H
      • Suzuki Y
      • Yoshimoto Y
      • et al.
      An abscopal effect in a case of concomitant treatment of locally and peritoneally recurrent gastric cancer using adoptive T-cell immunotherapy and radiotherapy.
      • Lin X
      • Lu T
      • Xie Z
      • et al.
      Extracranial abscopal effect induced by combining immunotherapy with brain radiotherapy in a patient with lung adenocarcinoma: A case report and literature review.
      • Katayama K
      • Tamiya A
      • Koba T
      • Fukuda S
      • Atagi S.
      An abscopal response to radiation therapy in a patient with metastatic non-small cell lung cancer: A case report.
      • Leung HWC
      • Wang SY
      • Jin-Jhih H
      • Chan ALF
      Abscopal effect of radiation on bone metastases of breast cancer: A case report.
      • Kim JO
      • Kim CA.
      Abscopal resolution of a hepatic metastasis in a patient with metastatic cholangiocarcinoma following radical stereotactic body radiotherapy to a synchronous early stage non-small cell lung cancer.
      • Brenneman RJ
      • Sharifai N
      • Fischer-Valuck B
      • et al.
      Abscopal effect following proton beam radiotherapy in a patient with inoperable metastatic retroperitoneal sarcoma.
      • Hidaka Y
      • Takeichi T
      • Ishikawa Y
      • Kawamura M
      • Akiyama M.
      Abscopal effect of local irradiation treatment for diffuse large B-cell lymphoma.
      • Gutkin PM
      • Hiniker SM
      • Swetter SM
      • Reddy SA
      • Knox SJ.
      Complete response of metastatic melanoma to local radiation and immunotherapy: 6.5 year follow-up.
      • Barsky AR
      • Cengel KA
      • Katz SI
      • Sterman DH
      • Simone CB.
      First-ever abscopal effect after palliative radiotherapy and immuno-gene therapy for malignant pleural mesothelioma.
      • Chino F
      • Pollis KE
      • Choi S
      • Salama JK
      • Palta M.
      stereotactic body radiation therapy–induced abscopal effect on hepatocellular carcinoma after treatment for lung cancer: A case report.
      • Britschgi C
      • Riesterer O
      • Burger IA
      • Guckenberger M
      • Curioni-Fontecedro A.
      Report of an abscopal effect induced by stereotactic body radiotherapy and nivolumab in a patient with metastatic non-small cell lung cancer.
      • Bitran J.
      The abscopal effect exists in non-small cell lung cancer: A case report and review of the literature.
      • Azami A
      • Suzuki N
      • Azami Y
      • et al.
      Abscopal effect following radiation monotherapy in breast cancer: A case report.
      • Nam SW
      • Han JY
      • Kim JI
      • et al.
      Spontaneous regression of a large hepatocellular carcinoma with skull metastasis.
      • Wersäll PJ
      • Blomgren H
      • Pisa P
      • Lax I
      • Kälkner K-M
      • Svedman C.
      Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma.
      • Takaya M
      • Niibe Y
      • Tsunoda S
      • et al.
      Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - A case report.
      • Tubin S
      • Raunik W.
      Hunting for abscopal and bystander effects: Clinical exploitation of non-targeted effects induced by partial high-single-dose irradiation of the hypoxic tumour segment in oligometastatic patients.
      • Sullivan RJ
      • Lawrence DP
      • Wargo JA
      • Oh KS
      • Gonzalez RG
      • Piris A.
      Case 21-2013.
      • Siva S
      • Callahan J
      • Macmanus MP
      • Martin O
      • Hicks RJ
      • Ball DL.
      Asbcopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer.
      • Sham RL.
      The abscopal effect and chronic lymphocytic leukemia.
      • Robins HI
      • Buchon JA
      • Varanasi VR
      • Weinstein AB.
      The abscopal effect: Demonstration in lymphomatous involvement of kidneys.
      • Rees GJG
      • Ross CMD.
      Abscopal regression following radiotherapy for adenocarcinoma.
      • Poon DMC
      • Wong KCW.
      Lymph node response in a patient with metastatic castration-resistant prostate cancer treated with radium-223.
      • Okwan-Duodu D
      • Pollack BP
      • Lawson D
      • Khan MK.
      Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma.
      • Okuma K
      • Yamashita H
      • Niibe Y
      • Hayakawa K
      • Nakagawa K.
      Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: A case report.
      • Ohba K
      • Omagari K
      • Nakamura T
      • et al.
      Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis.
      ,
      • MacManus MP
      • Harte RJ
      • Stranex S.
      Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour.
      • Lakshmanagowda PB
      • Viswanath L
      • Thimmaiah N
      • Dasappa L
      • Supe SS
      • Kallur P.
      Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: A case report.
      • Kodama K
      • Higashiyama M
      • Okami J
      • et al.
      A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors.
      • Joe MB
      • Lum JJ
      • Watson PH
      • Tonseth RP
      • McGhie JP
      • Truong PT.
      Radiation generates an abscopal response and complete resolution of metastatic squamous cell carcinoma of the anal canal: A case report.
      • Bruton Joe M
      • Truong PT.
      Abscopal effect after palliative radiation therapy for metastatic adenocarcinoma of the esophagus.
      • Isobe Y
      • Aritaka N
      • Sasaki M
      • Oshimi K
      • Sugimoto K.
      Spontaneous regression of natural killer cell lymphoma.
      • Ishiyama H
      • Teh BS
      • Ren H
      • et al.
      Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: Abscopal effect prevented by the blood-brain barrier?.