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. 2020 Jul 7;10:781. doi: 10.3389/fonc.2020.00781

Table 1.

General characteristics and main outcomes of the studies.

Studies Study type and no. of BM No. of patients Treatments and comparison Primary histology Tumor control (months) Survival (OS) (months) Prognostic factors (OS)
Univariate Multivariate
Primary randomized controlled trials Kondziolka et al. (3) RCT
2–4 BMs
27
13/14
WBRT vs. WBRT+SRS Lung, Melanoma, RCC, Breast, Other LC: 36 vs. 6
(p = 0.0005)
MST: 7.5 vs. 11
(p = 0.22)
breast 11 vs. lung 11 vs. melanoma 5.5 (p = 0.17)
Extent of extracranial disease
Andrews et al. (4) RCT
1–3 BMs
331
167/164
WBRT vs. WBRT+SRS Breast, Lung (Squamous, Adenocarcinoma, Large cell, Small cell), Melanoma, Renal, Other LC: p = 0·0132
(Favors WBRT + SRS)
MST: 5.7 vs. 6.5
(p = 0·1356)
Single BM (6·5 vs. 4·9, p = 0·0393)
Squamous NSCLC (5·9 vs. 3·9, p = 0·0508)
(Favors WBRT + SRS)
Single metastases, RPA class 1, largest metastasis was > 2 cm in diameter RPA 1 and type of tumor (Lung primary)
Aoyama et al. (5) RCT
1–4 BMs
132
67/65
WBRT+SRS vs. SRS Breast,
Lung, Colorectal Renal, Other
12 month BTRR: 46.8% 76.4%
(p < 0.001)
MST: 8.0 (0.5-57.0) vs. 7.5 (0.8–58.7)
(p = 0.42)
Primary tumor status (stable), Extracranial metastases (stable), RPA 1, KPS (90–100) Age (<65 y), Primary tumor status (stable), Extracranial metastases (stable), KPS score (90–100)
El Gantery et al. (6) RCT
1–3 BMs
60
21/18/21
WBRT+SRS vs. SRS vs. WBRT LC: 10 vs. 6 vs. 5
(p = 0.04)
NS
- Largest brain metastases = 3 cm in diameter: 15 vs. 8 vs. 5, p = 0.002
- Controlled primary: 12 vs. 8 vs. 5.5, p = 0.027
(Favors WBRT + SRS)
Single brain metastasis
Brown et al. (7) RCT
1–3 BMs
213
111/102
SRS vs. WBRT+SRS Breast, Colorectal, Lung, Skin/melanoma, Bladder, Kidney, Gynecologic, Other ICF: HR: 3.6; 95% CI, 2.2-5.9; (p < 0.001) OS: HR: 1.02; 95% CI, 0.75–1.38; (p = 0.92)
Chougule et al. (8) RCT
multiple
109
36/37/31
SRS vs. WBRT vs. WBRT+SRS Breast, Lung, colorectal LC: 87 vs. 91 vs. 62% MST: 7 vs. 5 vs. 9
p = NS
- Breast 9.5 vs. Colorectal 7 vs. Lung 6
Retrospective studies Sanghavi et al. (9) Retrospective 1,702
502/1200
WBRT+SRS vs. WBRT Lung, breast, melanoma and others RPA I = 16.1 vs. 7.1
RPA II = 10.3 vs. 4.2
RPA III = 8.7 vs. 2.3
(p < 0.05)
KPS, a controlled primary, absence of extracranial metastases, and RPA class
Sneed et al. (10) Retrospective 569
268/301
SRS vs. WBRT+SRS Breast, Kidney, lung, melanoma and others HR: 1.07 (0.89–1.27),
p = 0.49
KPS, Extracranial metastases, Control of the primary, Number of metastases
Frazier et al. (11) Retrospective 237
192/45
SRS vs. WBRT+SRS Breast, Melanoma, NSCLC, Renal, Other 5.9 (4.6–7.3) vs. 6.7 (4.0–12.1)
(p = 0.22)
14.6 (11.4–19.1) vs. 10.8
(6.2–18.0) (p = 0.31)
KPS >70, histology of breast cancer, smaller tumor volume, and age <65 years
Elaimy et al. (12) Retrospective 275
65/15/48/
19/117/11
SRS/S+SRS/
WBRT+SRS/S
+WBRT+SRS
/WBRT/
S+WBRT
NSCLC,
SCLC,
Breast,
Melanoma, RCC, Other
- SRS vs. WBRT (HR:1.94; 95% CI: 1.37–2.73,
p < 0.001)
SRS vs. WBRT+SRS
(HR:0.99; 95% CI: 0.93–1.05, p = 0.660)
ECOG-PS, Primary histology
- NSCLC vs. Melanoma & RCC (HR:1.17; 95% CI: 1.06-1.3, p < 0.001)
- NSCLC vs. Breast (HR:0.87; 95% CI: 0.78-0.96, p < 0.001)
Lung cancer Sperduto et al. (13) Secondary analysis (RCT) 252
126/126
WBRT+SRS vs. WBRT Lung, gastrointestinal, renal cancers and melanoma HR: 1.0; 95% CI: 0.8–1.4, p = 0.78) MST: 21.0 vs. 10.3, (P = 0.05)
(GPA 3.5–4.0)
Aoyama et al. (14) Secondary analysis (RCT) 88
45/43
SRS vs. WBRT+SRS NSCLC HR: 5.01 (2.44–11.11,
p < 0.001)
HR: 1.33 (0.85–2.08,
p = 0.20)
HR: 1.92; 95% CI, 1.01–3.78, p = 0.04)
DS GPA 2.5–4.0 group
Churilla et al. (15) Secondary analysis (RCT) 127
70/57
SRS vs. SRS+WBRT NSCLC HR: 4.11 (2.11–8.00), p < 0.001 HR: 0.98 (0.66–1.46),
p = 0.92
Li et al. (16) Retrospective Single BMs 70
29/23/18
WBRT/SRS vs. SRS+WBRT Lung (SCLC, NSCLC) - FFLP: 3.97 ± 0.33 vs. 6.85 ± 0.50 vs. 8.56 ± 1.36 (P < 0.0001)
- FFNBM: 4.07 ± 0.32 vs. 6.74 ± 0.52 vs. 8.56 ± 1.36 (P < 0.0001)
- SRS vs. SRS+WBRT (p = 0.0392)
MST: 5.67 ± 0.38, 9.33 ± 0.59, and 10.64 ± 1.54, (P < 0.0001)
SRS vs. SRS+WBRT (p = 0.7079)
Tumor volume, the absence of active extra-cranial disease, treatment methods, and worst pattern of enhancement
Sperduto et al. (17) Prospective
multiple
1,888
815/396/342
WBRT vs. SRS/WBRT
+SRS
NSCLC HR: 0.62;0.51–0.75,
p < 0.0001
HR: 0.53;0.45–0.63,
p < 0.0001
Age, KPS, ECM, No. of BMs
Lin et al. (18) Retrospective multiple 20,396
20241/155
WBRT vs. WBRT+SRS NSCLC HR: 0.49 (0.36–0.66),
p < 0.0001
Minniti et al. (19) Prospective
2–3 BMs
122
66/66
WBRT vs. WBRT+SRS NSCLC - LC 6 month: 90 vs. 100%
- 12 month: 47 vs. 93%
- BC 6 month: 75 vs. 82%
12 month: 18 vs. 42% (p = 0.001)
MST: 7.2 vs. 10.3,
p = 0.005
Stable extracranial disease and KPS
Marko et al. (20) Prospective
multiple
162
26/121/15
SRS vs. WBRT vs. WBRT+SRS NSCLC MST: 12.32 vs. 12.25 vs. 12.74, (p = 0.98, 0.62, 0.91)
Abacioglu et al. (21) Prospective
multiple
100
(22/78)
SRS vs. WBRT+SRS NSCLC (Adenocarcinoma Squamous cell carcinoma Unclassified NSCLC) MST: 8 vs. 9, p = 0.757 Adenocarcinoma histology, KPS score ≥ 80, 1–3 metastases and tumor diameter < 2 cm
Sun et al. (22) Prospective
multiple
82
(33/49)
WBRT+SRS
vs. WBRT
SCLC MST: 13.4 vs. 8.5 months; p = 0.004
OS rate at 6 m: 84.5 vs. 59.8%
12 m: 62.7 vs. 29.9%
24 m: 21.5 vs. 9.6%
(p = 0.004)
Limited number (1 to 3) of BMs, KPS ≥ 70, asymptomatic BMs, controlled extracranial diseases, and maximum diameter of the largest tumor ≤ 2.0 cm
Mansour and Shawky (23) Prospective
multiple
36 SRS+WBRT SCLC MST: 13.5
OS rate at 6m: 84.5%
12m: 62.7%
24m: 21.5%
KPS, single BMs, controlled extracranial diseases, ≤ 2 cm maximum diameter of the largest BMs tumor and asymptomatic BMs ≤ 2 cm maximum diameter of the largest BMs tumor
Wegner et al. (24) Prospective
multiple
44
(6/38)
WBRT+SRS
vs. SRS
(prior WBRT or PCI = 30)
SCLC ALC at 6 m: 90%,
12 m: 86%
MST: 14 vs. 6 (p = 0.04)
Sperduto et al. (17) Prospective
multiple
268
(247/21)
WBRT vs. WBRT+SRS SCLC MST: 3.87 vs. 15.23,
p = 0.003
KPS, age, ECM, No. of BMs
Breast cancer Caballero et al. (25) Retrospective 310 SRS after prior WBRT 90 breast, 113 NSCLC, 31 SCLC, 42 melanoma, and 34 miscellaneous MST: 8.4 (11.4 vs. 8.1 vs. 7.2) Breast; age <50 years, smaller total target volume, and longer interval from WBRT to SRS
NSCLC; controlled primary tumor, and number of BM, melanoma; smaller total target volume
Breast; age <50 years, smaller total target volume, and longer interval from WBRT to SRS
NSCLC; number of BM, KPS, and controlled primary
Melanoma; smaller total target volume
Firlik et al. (26) Retrospective SRS vs. WBRT+SRS Breast cancer 93% P = 0.20 Tumor volume and Solitary metastasis
Muacevic et al. (27) Retrospective SRS vs. WBRT+SRS Breast cancer 9.5 ± 1.4 vs.
11.4 ± 3.5, p = 0.7
KPS and RPA
Kased et al. (28) Retrospective SRS vs. WBRT+SRS Breast cancer MBFFP: 8.6 vs. 10.5, p = 0.75 MST: 17.1 vs. 15.9,
p = 0.20
Age <50 y
KPS > 70 Primary controlled, ER positive Overexpression,
Her2/neu overexpression.
Sperduto et al. (17) Retrospective multiple 642
277/141/
123
WBRT vs. SRS/WBRT
+SRS
Breast cancer HR: 0.75;0.54–1.04,
p = 0.088
HR: 0.72;0.53–0.98, p = 0.035
NA KPS
Jaboin et al. (29) Retrospective 100
26/25/37
SRS vs. SRS+WBRT vs. WBRT+ (salvage)SRS Breast (luminal A, luminal B, HER2/neu, basal, unknown) MST: 12.4 vs. 12.2 vs. 9.5, p = NS Age, stage and number of lesions, CNS failure
Perez et al. (30) Retrospective 231
66/165
SRS vs. SRS+WBRT Breast cancer HR: 1.78;1.06–2.99,
p = 0.03
(multivariate)
Controlled systemic disease, adjuvant chemotherapy, and RPA
Sperduto et al. (31) Retrospective 383 SRS/WBRT/
WBRT+SRS/
S+WBRT/S+
SRS+WBRT/
S+SRS
Basal (TN)
Luminal A (ER/PR(+)/HER2(–)
HER2(+)/ER/PR(–)
Luminal B (TP)
MST: 7.3 (4.9–9.5)
10.0 (7.4–19.5)
17.9 (13.4–22.9)
22.9 (16.1–29.5) p < 0.01
Cho et al. (32) Retrospective 131
79/43+4/5
SRS vs. WBRT+ salvage SRS vs. WBRT+SRS boost vs. S+SRS boost ER(+)/HER2(–); 41(31%), ER(+)/HER2(+); 30 (23%), ER(–)/HER2(+); 23 (18%), and ER(–)/HER2(–); 28 (21%) (TNBC). TNBC vs. ER(+)/HER2(–); HR:3.12 (p < 0.001)
(retreatment or death)
SRS vs. WBRT+SRS: HR = 1.18, p = 0.4
MST: 16 vs. 26 vs. 23, vs. 7 (p < 0.001)
Xu et al. (33) Retrospective 264
HER2known
/unknown
(172/92)
SRS vs. S/WBRT
162/49+214
Breast cancer
HER2+ vs. HER2–172 (82/90)
SRS vs. S/WBRT: 96.6 vs. 106.5, p = 0.73
MST: OS:105.7 vs. 74.3, p < 0.01
Survival after SRS: 31.3 vs. 14.1, p < 0.01
HER2+; HR:0.66, p = 0.021
Age >45 y, Estrogen receptor positive, Progesterone receptor positive
HER2+; HR:0.18, p < 0.001
Xu, et al. (34) Retrospective 103
(SRS = 27, WBRT+SRS = 59 S+SRS = 9, S+WBRT+
SRS = 8)
SRS vs. WBRT+SRS Breast cancer
(Triple negative, Non–triple negative, ER+, PR+, HER2+)
(TN = 24/Non–T
N = 79
- OLC: 90/3%
- ATC rate at 6 m: 96.5%
- at 12 m: 92.2%
- at 24 m:83.3%
SRS vs. WBRT+SRS;
p = 0.797
Non-TN vs. TN; MST: 43 (27.3–58.7) vs. 82 (66.3–97.7), p = 0.042
Non-TN vs. TN; HR:0.461 (0.279–0.763), p = 0.003
HER2+ vs. HER2–; HR:0.629 (0.405–0.975), p = 0.038
Non-TN status and lower recursive partitioning analysis class
Radioresistant histology Lwu et al. (35) Retrospective 103
34/56
SRS alone vs. SRS + prior WBRT 41 RCC, 62 Melanoma ALC at 6m: 89%
12 m: 84%
18: 76% 24 m:61%
- LC at 12 m: 91% (RCC) and 75% (melanoma)
HR: 0.98 (0.30–3.26),
p = 0.98
- Melanoma vs. RCC; HR: 3.48 (1.08–11.23), p = 0.04)
Tumor volume, Primary tumor
Brown et al. (36) Retrospective 41 SRS vs. SRS+WBRT boost 16 RCC, 23 melanoma, 2 sarcoma LF; 12%
DBF; 54% -SRS+WBRT vs. SRS:
- ALC at 6 month; 100 vs. 85%,
p = 0.018
- DBF rate at 6-m; 17 vs. 64%, p = 0.0027
MST: 14.2
- RCC vs. melanoma; 17.8 vs. 9.7, p = 0.12
Systemic disease status, RPA RPA, histological diagnosis of primary tumor
Manon et al. (37) Retrospective 31 SRS Melanoma 14, Sarcoma 3, RCC 14 ICF at 3m; 25.8%
- at 6 m; 48.3%
8.3 months (95% CI, 7.4 to 12.2).
Chang et al. (38) Retrospective 189 SRS 103 melanoma, 77 RCC, 9 sarcoma 1-year AFFP: 64% RCC;
47% melanoma; 0% sarcoma (P < 0.001)
MST: 7.5
1-year SR: 40% RCC; 25% melanoma; 22% sarcoma
(P = 0.0354)
Renal cell carcinoma Wronski, M., et al. (39) Retrospective 119 WBRT RCC MST: 4.4 single brain metastasis, lack of distant metastases at the time of diagnosis, and tumor diameter < or = 2 cm
Takashi et al. (40) Retrospective 69 SRS RCC 82.6% MST: 9.5 Number of lesions, KPS, RPA, and the interval from diagnosis of RCC to brain metastasis
Jasonet al. (41) Retrospective 69 SRS RCC ALC; 94% MST: 6 Age, preoperative KPS score, radiosurgical dose to the tumor margin, maximal radiosurgical dose, treatment iso-dose, time from diagnosis of renal cell cancer to the development of brain metastasis
Goyal et al. (42) Retrospective 29 (13/16) SRS vs. SRS+WBRT RCC -DBF: 33 vs. 25%
- LC: 2/18 vs. 2/29, p = NS
MST: 5.2 vs. 6.8, NS
Mori et al. (43) Retrospective multiple 25
12/13
SRS vs. SRS+WBRT RCC MST: 11
SRS vs. SRS+WBRT; p = 0.35
Age, good KPS at the time of radiosurgery, nephrectomy prior to radiosurgery Age, lack of active systemic disease, use of chemotherapy and/or immunotherapy after SR
Ippen et al. (44) Retrospective multiple 66
36/24/6
SRS vs. S+SRS vs. SRS+WBRT RCC −1-year LC: 84%, 94%, and 88%,
p = 0.445
- DTC: Prior WBRT vs. others
(p = 0.007)
OS: 13.9, 21.9, 5.9
- Prior WBRT was associated with worst OS (uni/multivariate)
Age, prior surgery, RPA, KPS, SIR, BSBM, number of brain metastases, initial tumor volume, and Ds-GPA Age, RPA, KPS, and the initial number of brain metastases, prior surgery
Fokas et al. (45) Retrospective 1–3 (SRS/SRS+
WBRT)
Multiple (WBRT)
88
51/17/20
SRS vs. SRS+WBRT vs. WBRT RCC 1-, 2-, 3-year IC rates; 42%, 29%, 22% MST: 12 vs. 16 vs. 2
-SRS/SRS+WBRT vs. WBRT; p < 0.001
Age, lack of extracranial metastases, RPA, SRS, SRS + WBRT lack of extracerebral metastases, RPA, SRS, SRS + WBRT
Bates et al. (46) Retrospective multiple 25
9/11/5
SRS vs. WBRT vs. SRS+WBRT RCC BPFS; 8.3 vs. 2.5
(p = 0.38) vs. 4.5
(p = 0.65).
OS; 8.3 vs. 2.8 (p = 0.82) vs.8.5 (p = 0.65) Age, sex, KPS, presence of extracranial metastases, history of smoking, alcohol consumption, DS-GPA, use of surgery, multiple intracranial metastases DS-GPA score
Melanoma Hauswald et al. (47) Retrospective 87 WBRT Melanoma MST: 3.5
OSR:
- at 6 m: 29.2%
- at 12 m: 16.5%
DS-GPA, RPA Total treatment dose, surgical resection, GPA
Noël et al. (48) Retrospective 25 SRS Melanoma 3-, 6- and 12-m LC rates; 95 ± 3, 90 ± 5 and 84 ± 7% MST: 8 months
3-, 6- and 12-m OS rates; 75 ± 9, 53 ± 10, and 29 ± 10%
Extracranial controlled disease, SIR -
Seung et al. (49) Retrospective 55
11/28/16
WBRT+SRS, SRS, WBRT+SRS (salvage) Melanoma 6 month and 1-year actuarial freedom from progression rates of 89% and 77% 35 wks Total target volume treated
Mathieu et al. (50) Retrospective 244
115/110/53
SRS (prior WBRT /prior surgery) Melanoma LC: 30.9%
DC: 41.7%
MST: 5.3 Age, Extracranial disease status, RPA, KPS, Number of metastases, Single or multiple metastasis, WBRT at any time Active extracranial disease, KPS, multiple metastases, tumor volume >8 cm3, cerebellar metastases
Yu et al. (51) Retrospective 122 SRS vs. SRS+WBRT 39 (32%) WBRT Melanoma MST: 7.0 total intracranial tumor volume <3 cm3, inactive systemic disease
Selek, U., et al. (52) Retrospectiv3 103
61/12/30
RS, SRS+WBRT, WBRT+ SRS (salvage) Melanoma −1-year LC; 49%
- 1-year DF; 14.7%.
1-year OS: 25.2% Score Index for Radiosurgery (SIR)
Dyer et al. (53) Retrospective 147 SRS/SRS+
WBRT/salvage WBRT
Melanoma DICF: omission of up-front WBRT; HR: 2.24, p = 0.005 MST: 7.3
Omission of up-front WBRT; HR: 2.56, p = 0.08
(multivariate)
Extensive extracranial metastases, KPS, multiple brain metastases Extensive extracranial metastases, KPS
Bagshaw et al. (54) Retrospective 185
154/51/31
SRS/salvage WBRT /SRS+WBRT Melanoma MTTLF: 23.4 MST: 7.8
Radbillet al. (55) Retrospective 51
32/8/8/2
SRS/SRS+
WBRT/SRS+S
/SRS+WBRT
+S
Melanoma ALC
- at 26 wks: 66%
-at 52 wks: 56% ADC
- at 26 wks: 46%
- at 52 wks: 25%
OS rate
- at 12 wks; 71%
- at 26 wks;51%,
- at 52 wks; 30%
RPA I, Treatment of infratentorial lesion, Multiple lesions present (categoric)
Initial WBRT with radiosurgery; HR:1.08 (0.39–2.98), p = 0.88

OS, overall survival; MST, median survival time; LC, local control; DF, distant failure; DC, distant control; ICF, intrcranial failure; MTTLF, median time to local failure; MTTDF, median time to distant failure; ALC, actuarial local control; DICF, distant intracranial failure; BPFS, brain progression free survival; IC, intracranial; DTC, distant tumor control; DBF, distant brain failure; AFFP, actuarial freedom from progression; FFNBM, free from new brain meatsases; RPA, recursive partitioning analysis; DS-GPA, Diagnosis-specific graded prognostic assessment; WBRT, whole brain radiotherapy; SRS, stereotactic radiosurgery; S, surgery; RCT, randomized controlled trial; NSCLC, non-small cell lung cancer, SCLC, small cell lung carcinoma; wks, weeks; m, months; NS, not significant; ER+, estrogen receptor positive; PR+, progesterone receptor positive; HER2+, human epidermal growth factor receptor 2; TN, triple negative; TNBC, triple negative breast cancer.