Predictive value of single nucleotide polymorphisms in XRCC1 for radiation-induced normal tissue toxicity

Figures & data

Table 1 Baseline characteristics of the eligible studies

Author, year	Country	Ethnicity	Disease	SNP	Sample size (N)	Adverse effect	Assessment criteria	RT dose	CT involved	Study design	Genotyping method
Alsbeih et al,^Citation24 2010	Saudi Arabia	Caucasian	NPC	rs25487	60	Late: fibrosis	RTOG/EORTC ≥G2	66–70 Gy	Yes	Case–control	PCR
Andreassen et al,^Citation29 2003	Denmark	Caucasian	Breast	rs25487	41	Late: fibrosis	LENT-SOMA ≥G3	36.6–51.4 Gy	No	Cohort	PCR
Andreassen,^Citation63 2005	Denmark UK	Caucasian	Breast	rs25487	52	Late: breast appearance	Photographic ≥G2	50 Gy/25f, 42.9 Gy/13f, 39 Gy/13f	NA	Case–control	PCR
Andreassen et al,^Citation30 2006	Denmark	Caucasian	Breast	rs25487, rs25489, rs1799782	120	Late: fibrosis	LENT-SOMA ≥G3	41 Gy	Yes	Cohort	PCR
Azria et al,^Citation57 2008	France	Caucasian	Breast, HNC	rs25489	34	Late: fibrosis	RTOG/EORTC CTC v3.0 ≥G3	NA	Yes	Case–control	PCR
Brem et al,^Citation31 2006	France	Caucasian	Breast	rs3213245	247	Acute and Late	EORTC	50 Gy, tumor bed boost 10 Gy	NA	Case–control	PCR-RFLP
Burri et al,^Citation14 2008	America	Mixed	Prostate	rs25487, rs25489, rs1799782	135	Late: rectal bleeding, urinary morbidity, erectile dysfunction	RTOG/EORTC ≥G2	125I: 160 Gy 103 Pd: 124 Gy 103 Pd: 100 Gy+EBRT: 45 Gy	NA	Cohort	PCR
Changclaude et al,^Citation33 2005	Germany	Caucasian	Breast	rs25487, rs25489, rs1799782	446	Acute: skin reaction	CTCAE v2.0 ≥G2c	Mean 54.0±4.8 Gy (35.5–64.5 Gy)	No	Cohort	PCR-RFLP
Changclaude et al,^Citation32 2009	Germany	Caucasian	Breast	rs25487, rs25489, rs1799782, rs3213245	409	Late: telangiectasia	RTOG/EORTC LENT-SOMA ≥G2	Mean 61.8±4.10 Gy (51–71 Gy)	No	Cohort	PCR-RFLP
Cheuk et al,^Citation20 2014	Hong Kong	Asian	NPC	rs25487, rs1799782	120	Late: fibrosis	RTOG ≥G1	66–76 Gy	Yes	Cohort	PCR-RFLP
Damaraju et al,^Citation45 2006	Canada	Mixed	Prostate	rs25489, rs1799782	83	Late: bladder or rectal toxicity	RTOG ≥G2	Mean 77.1 Gy (68.3–82.1 Gy)	No	Cohort	PCR
De Ruyck et al,^Citation49 2005	Belgium	Caucasian	Cervical, endometria	rs25487, rs25489, rs1799782	62	Late	CTCAE v3.0 ≥G2	EBRT: 45–66 Gy 192I: 15–35 Gy	Yes	Cohort	PCR-RFLP
De Ruyck et al,^Citation25 2013	Belgium	Caucasian	HNC	rs3213245	189	Acute: dysphagia	CTCAE v3.0 ≥G3	66–70 Gy	Yes	Cohort	PCR-RFLP
Duldulao et al,^Citation52 2013	USA	Caucasian	Rectal	rs25487	132	Acute: gastrointestinal toxicity	CTCAE v3.0 ≥G3	NA	Yes	Cohort	PCR, direct sanger sequencing
Falvo et al,^Citation42 2011	Italy	Caucasian	Breast	rs1799782	57	Acute: erythema	CTCAE v3.0 ≥G1	21 Gy/f	Yes	Cohort	PCR
Falvo et al,^Citation34 2012	Italy	Caucasian	Breast	rs25487	57	Late: fibrosis, fat necrosis	CTCAE v3.0 ≥G2	21 Gy/f	Yes	Cohort	PCR
Giotopoulos et al,^Citation35 2007	UK	Mixed	Breast	rs25487	167	Late: telangiectasia	RTOG LENT-SOMA ≥G2	40–50 Gy, tumor bed boost of 15 Gy/5f	Yes	Cohort	PCR-RFLP
Ishikawa et al,^Citation50 2011	Japan	Asian	Cervical	rs25487	208	Acute: diarrhea	CTCAE v2.0 ≥G2	EBRT 50.6 Gy Brachytherapy 24.0 Gy	Yes	Cohort	PCR
Langsenlehner et al,^Citation46 2011	Austria	Caucasian	Prostate	rs25487, rs25489, rs1799782	579	Late: bladder or rectal toxicity	RTOG/EORTC ≥G2	66–70.4 Gy	No	Cohort	PCR
Li et al,^Citation21 2013	China	Asian	NPC	rs25487, rs1799782	114	Acute: mucositis, dermatitis	CTCAE v3.0 ≥G3	50–70 Gy	Yes	Cohort	PCR-RFLP
Mangoni et al,^Citation43 2011	Italy	Caucasian	Breast	rs25487, rs1799782	87	Acute: skin reaction	CTCAE v2.0 ≥G2c	50 Gy/25f, 44 Gy/16f	Yes	Cohort	PCR
Moullan et al,^Citation36 2003	France	Caucasian	Breast	rs25487, rs25489, rs1799782	254	Acute and Late	EORTC	50 Gy, tumor bed boost 10 Gy	NA	Cohort	PCR
Mumbrekar et al,^Citation37 2017	India	Asian	Breast	rs25487	126	Acute: skin reaction	RTOG ≥G2	50 Gy, tumor bed boost 10 Gy for 26 patients	Yes	Cohort	PCR
Popanda et al,^Citation47 2009	Germany	Caucasian	Prostate	rs25487, rs25489, rs1799782	405	Acute: proctitis cystitis	CTCAE v2.0 ≥G3	61–72 Gy	No	Cohort	Sequence-specific hybridization probes
Pratesi et al,^Citation26 2011	Italy	Caucasian	HNC	rs25487	101	Acute: mucositis, skin erythema	CTCAE v3.0 ≥G2	Mean 62 Gy (54–70 Gy)	Yes	Case–control	PCR-RFLP
Raabe et al,^Citation44 2012	Germany	Caucasian	Breast	rs25487	83	Acute: erythema	RTOG ≥G2	50–50.4 Gy	NA	Cohort	PCR-RFLP, MALDI-TOF
Sakano et al,^Citation51 2010	Japan	Asian	Bladder	rs25487	95	Acute: gastrointestinal toxicity	CTCAE v3.0 ≥G2	Median 48.6 Gy (30.0–60.4 Gy)	Yes	Cohort	PCR-RFLP
Smith et al,^Citation53 2017	America	Mixed	Rectal	rs25487	165	Acute: gastrointestinal and genitourinary toxicity (diarrhea, proctitis, cystitis)	CTCAE v3.0 ≥G3	Median 50.4 Gy	Yes	Cohort	PCR, MALDI-TOF
Suga et al,^Citation38 2007	Japan	Asian	Breast	rs25487	399	Acute: skin reaction	CTCAE v2.0 ≥G2	46–60 Gy	Yes	Cohort	PCR
Terrazzino et al,^Citation39 2012	Italy	Caucasian	Breast	rs25487, rs1799782, rs3213245	286	Acute: skin reaction	RTOG ≥G2	50–50.4 Gy, tumor bed boost 9–16 Gy	Yes	Cohort	PCR-RFLP
Terrazzino et al,^Citation40 2012	Italy	Caucasian	Breast	rs25487, rs1799782	237	Late: fibrosis	LENT-SOMA ≥G2	50–50.4 Gy, tumor bed boost 9–16 Gy	Yes	Cohort	PCR-RFLP
Tucker et al,^Citation54 2013	USA	Caucasian	NSCLC	rs25487	141	Late: radiation pneumonitis	CTCAE v3.0 ≥G3	Median 63 Gy (50.4–72 Gy)	Yes	Cohort	PCR-RFLP
Usmani et al,^Citation48 2014	Canada	Caucasian	Prostate	rs25487	217	Late: urinary toxicity	RTOG ≥G2	125I ≥145 Gy	No	Cohort	PCR
Venkatesh et al,^Citation27 2014	India	Caucasian	HNC	rs25487, rs25489, rs1799782, rs3213245	183	Acute: mucositis, skin reaction	RTOG ≥G3	60–70 Gy	Yes	Cohort	PCR-RFLP
Yin et al,^Citation55 2011	USA	Mixed	NSCLC	rs25487	165	Late: radiation pneumonitis	CTCAE v3.0 ≥G2	Median 63 Gy (50.4–84.0 Gy)	Yes	Cohort	PCR-RFLP
Yoon et al,^Citation56 2011	USA	Mixed	Esophageal adenocarcinoma	rs25487	60	Acute: dysphagia	CTCAE v2.0 ≥G3	45 Gy	Yes	Cohort	PCR, MALDI-TOF
Xian et al,^Citation22 2015	China	Asian	Esophageal squamous cell carcinoma	rs25487	118	Acute: esophagitis	CTCAE ≥G3	Median 60 Gy (45–66 Gy)	Yes	Cohort	PCR
Zhai et al,^Citation23 2016	China	Asian	NPC	rs25487	60	Acute and Late: skin, mucosa, salivary gland	RTOG ≥G2	66–76 Gy	Yes	Cohort	PCR-LDR
Zhou et al,^Citation15 2010	China	Asian	Breast	rs25487, rs25489, rs1799782, rs3213245	119	Acute: skin reaction	CTCAE v3.0 ≥G2	46–54 Gy	No	Cohort	PCR-RFLP
Zschenker et al,^Citation41 2010	Germany	Caucasian	Breast	rs25487	69	Late: fibrosis	LENT-SOMA ≥G2	54–55 Gy	Yes	Cohort	PCR-RFLP, MALDI-TOF

Abbreviations: CT, chemotherapy; CTC, Common Toxicity Criteria; CTCAE, Common Terminology Criteria for Adverse Events; EBRT, external beam radiation therapy; EORTC, European Organization for Research and Treatment of Cancer; HNC, head and neck cancer; LDR, ligase detection reaction; MALDI-TOF, matrix-assisted laser desorption/ionization time of flight; LENT-SOMA, Late Effects of Normal Tissue-Subjective Objective Management Analytical; NA, not available; NPC, nasopharyngeal carcinoma; NSCLC, non-small-cell lung cancer; PCR, polymerase chain reaction; RFLP, restriction fragment length polymorphism; RT, radiotherapy; RTOG, Radiation Therapy Oncology Group; SNP, single nucleotide polymorphism.

Figure 1 Flow diagram of study search and screening for the meta-analysis.

Abbreviations: RT, radiotherapy; SNP, single nucleotide polymorphism.

Figure 2 Forest plot for the association between rs25487 and radiation-induced adverse effects.

Notes: A fixed-effects model was used. The square with the corresponding horizontal line represents the OR and 95% CI of each study. The area of the square reflects the weight of the study. The diamond represents the pooled OR and 95% CI. The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a2, mucositis; a3, gastrointestinal and genitourinary toxicity; a3-1, gastrointestinal reactions (nausea and vomiting); a3-2, gastrointestinal reactions (diarrhea, rectal pain, obstipation, bleeding and proctitis); a4, dysphagia; a5, salivary gland; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis, skin telangiectasia and breast appearance); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction; b3, radiation pneumonitis; b4, mucous membrane; b5, salivary gland.
Abbreviations: M–H, Mantel–Haenszel; OR, odds ratio.

Figure 3 Forest plot for the association between rs25487 and radiation-induced acute adverse effects by specific side effect.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a2, mucositis; a3, gastrointestinal and genitourinary toxicity; a3-1, gastrointestinal reactions (nausea and vomiting); a3-2, gastrointestinal reactions (diarrhea, rectal pain, obstipation, bleeding and proctitis); a4, dysphagia; a5, salivary gland.
Abbreviation: M–H, Mantel–Haenszel.

Figure 4 Forest plot for the association between rs25487 and radiation-induced late adverse effects by specific side effect.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis, skin telangiectasia and breast appearance); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction; b3, radiation pneumonitis; b4, mucous membrane; b5, salivary gland.
Abbreviation: M–H, Mantel–Haenszel.

Figure 5 Forest plot for the association between rs25487 and radiation-induced adverse effects by irradiation area.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a2, mucositis; a3, gastrointestinal and genitourinary toxicity; a3-1, gastrointestinal reactions (nausea and vomiting); a3-2, gastrointestinal reactions (diarrhea, rectal pain, obstipation, bleeding and proctitis); a4, dysphagia; a5, salivary gland; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis, skin telangiectasia and breast appearance); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction; b3, radiation pneumonitis; b4, mucous membrane; b5, salivary gland.
Abbreviation: M–H, Mantel–Haenszel.

Figure 6 Forest plot for the association between rs25489 and radiation-induced adverse effects.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a3, gastrointestinal and genitourinary toxicity; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis and skin telangiectasia); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction.
Abbreviation: M–H, Mantel–Haenszel.

Figure 7 Forest plot for the association between rs25489 and radiation-induced adverse effects by irradiation area.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a3, gastrointestinal and genitourinary toxicity; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis and skin telangiectasia); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction.
Abbreviation: M–H, Mantel–Haenszel.

Figure 8 Forest plot for the association between rs1799782 and radiation-induced adverse effects.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a2, mucositis; a3, gastrointestinal and genitourinary toxicity; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis and skin telangiectasia); b1-1, subcutaneous fibrosis; b2, gastrointestinal and genitourinary toxicity; b2-1, gastrointestinal toxicity; b2-2, genitourinary toxicity; b2-3, erectile dysfunction.
Abbreviation: M–H, Mantel–Haenszel.

Figure 9 Forest plot for the association between rs3213245 and radiation-induced adverse effects.

Notes: The “case” represents patients with severe radiation-induced side effects and “control” represents patients without or with light radiation-induced side effects. a, acute side effects; a1, skin reactions (dermatitis and erythema); a2, mucositis; a4, dysphagia; b, late side effects; b1, skin and subcutaneous reactions (subcutaneous fibrosis and skin telangiectasia).
Abbreviation: M–H, Mantel–Haenszel.

Figure 10 Begg’s funnel plot for the effect of rs25487 on radiation-induced skin toxicity.

Note: Circles represent the actually included studies.
Abbreviations: OR, odds ratio; SE, standard error.

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