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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

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Front. Med.    2015, Vol. 9 Issue (4) : 478-486    https://doi.org/10.1007/s11684-015-0420-0
RESEARCH ARTICLE
U-shaped association between telomere length and esophageal squamous cell carcinoma risk: a case-control study in Chinese population
Jiangbo Du1,2, Wenjie Xue1, Yong Ji3, Xun Zhu1, Yayun Gu1,2, Meng Zhu1,2, Cheng Wang1,2, Yong Gao4, Juncheng Dai1,2, Hongxia Ma1, Yue Jiang1, Jiaping Chen1,2, Zhibin Hu1,2, Guangfu Jin1,2, Hongbing Shen1,2()
1. Department of Epidemiology and Biostatistics, School of Public Health, Nanjing Medical University, Nanjing 211166, China
2. Jiangsu Key Lab of Cancer Biomarkers, Prevention and Treatment, Collaborative Innovation Center for Cancer Personalized Medicine, Nanjing Medical University, Nanjing 211166, China
3. Department of Cardiothoracic Surgery, the Affiliated Wuxi People’s Hospital of Nanjing Medical University, Wuxi 214043, China
4. Department of Medical Oncology, the Affiliated Huai’an First People’s Hospital of Nanjing Medical University, Huai’an 223300, China
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Abstract

Telomeres play a critical role in biological ageing by maintaining chromosomal integrity and preventing chromosome ends fusion. Epidemiological studies have suggested that inter-individual differences of telomere length could affect predisposition to multiple cancers, but evidence regarding esophageal squamous cell carcinoma (ESCC) was still uncertain. Several telomere length-related single nucleotide polymorphisms (TL-SNPs) in Caucasians have been reported in genome-wide association studies. However, the effects of telomere length and TL-SNPs on ESCC development are unclear. Therefore, we conducted a case-control study (1045 ESCC cases and 1433 controls) to evaluate the associations between telomere length, TL-SNPs, and ESCC risk in Chinese population. As a result, ESCC cases showed overall shorter relative telomere length (RTL) (median: 1.34) than controls (median: 1.50, P<0.001). More interestingly, an evident nonlinear U-shaped association was observed between RTL and ESCC risk (P<0.001), with odds ratios (95% confidence interval) equal to 2.40 (1.84–3.14), 1.36 (1.03–1.79), 1.01 (0.76–1.35), and 1.37 (1.03–1.82) for individuals in the 1st (the shortest), 2nd, 3rd, and 5th (the longest) quintile, respectively, compared with those in the 4th quintile as reference group. No significant associations were observed between the eight reported TL-SNPs and ESCC susceptibility. These findings suggest that either short or extremely long telomeres may be risk factors for ESCC in the Chinese population.
Keywords esophageal squamous cell carcinoma      telomere length      genetic variants      susceptibility      genome-wide association study     
Corresponding Author(s): Hongbing Shen   
Just Accepted Date: 10 October 2015   Online First Date: 17 November 2015    Issue Date: 26 November 2015
 Cite this article:   
Jiangbo Du,Wenjie Xue,Yong Ji, et al. U-shaped association between telomere length and esophageal squamous cell carcinoma risk: a case-control study in Chinese population[J]. Front. Med., 2015, 9(4): 478-486.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-015-0420-0
https://academic.hep.com.cn/fmd/EN/Y2015/V9/I4/478
Fig.1  Association between relative telomere length (RTL) and esophageal squamous cell carcinoma risk based on restricted cubic spline function in the logistic regression model.
Characteristics Control ESCC P a
N RTL median (IQR) N RTL median (IQR)
Overall 1433 1.50 (1.22−1.81) 1045 1.34 (1.04−1.72) 7.39 × 10−13
Age (year)
<60 711 1.60 (1.32−1.94) 495 1.40 (1.05−1.81) 5.45 × 10−11
≥60 722 1.40 (1.11−1.68) 550 1.29 (1.01−1.64) 8.41 × 10−4
P b 9.63 × 10−20 1.63 × 10−3
Sex
Male 1016 1.47 (1.18−1.76) 770 1.32 (1.02−1.72) 4.09 × 10−8
Female 417 1.40 (1.28−1.94) 275 1.42 (1.08−1.76) 5.87 × 10−6
P b 1.04 × 10−5 0.081
Smoking
Never 739 1.51 (1.22−1.84) 456 1.33 (1.01−1.72) 3.91 × 10−8
Ever 694 1.50 (1.22−1.80) 589 1.35 (1.05−1.72) 3.01 × 10−6
P b 0.657 0.415
Drinking
Never 907 1.52 (1.23−1.82) 499 1.34 (1.02−1.72) 5.38 × 10−9
Ever 526 1.47 (1.18−1.80) 546 1.35 (1.05−1.73) 6.58 × 10−5
P b 0.217 0.721
Tab.1  Comparative analysis of relative telomere length (RTL) between case-control group and characteristics subgroup
Quintile of RTL by controls category Control N (%) ESCC N (%) OR (95%CI) a P a
≥1.89 286 (19.96) 186 (17.80) 1.37 (1.03−1.82) 0.030
1.60−1.89 287 (20.03) 146 (13.97) 1.00 (referent) −
1.38−1.60 287 (20.03) 155 (14.83) 1.01 (0.76−1.35) 0.950
1.14−1.38 287 (20.03) 214 (20.48) 1.36 (1.03−1.79) 0.027
<1.14 286 (19.96) 344 (32.92) 2.40 (1.84−3.14) 1.46 × 10−10
Tab.2  Association between relative telomere length (RTL) and esophageal squamous cell carcinoma risk
Gene SNPs Control N (%) Cases N (%) OR (95% CI) a P a
TERC rs10936599
TT 402 (28.45) 295 (29.29) 1.00
TC 715 (50.60) 522 (51.84) 0.97 (0.80−1.18) 0.766
CC 296 (20.95) 190 (18.87) 0.92 (0.81−1.04) 0.170
C allele 0.92 (0.82−1.04) 0.181
ACYP2 rs11125529
CC 894 (63.00) 606 (61.15) 1.00
CA 457 (32.21) 349 (35.22) 1.11 (0.93−1.33) 0.240
AA 68 (4.79) 36 (3.63) 0.87 (0.70−1.07) 0.183
A allele 1.01 (0.87−1.16) 0.944
TERT rs2736100
TT 484 (34.20) 333 (32.17) 1.00
TG 679 (47.99) 513 (49.57) 1.08 (0.90−1.30) 0.410
GG 252 (17.81) 189 (18.26) 1.04 (0.92−1.17) 0.535
G allele 1.04 (0.93−1.17) 0.483
TERT rs2736108
GG 720 (50.70) 499 (48.64) 1.00
GA 559 (39.37) 456 (44.44) 1.16 (0.98−1.38) 0.092
AA 141 (9.93) 71 (6.92) 0.86 (0.74−1.01) 0.069
A allele 0.98 (0.86−1.12) 0.776
OBFC1 rs4387287
CC 976 (69.96) 751 (72.84) 1.00
CA 386 (27.67) 281 (24.73) 0.85 (0.70−1.03) 0.095
AA 33 (2.37) 25 (2.42) 1.00 (0.76−1.31) 0.983
A allele 0.90 (0.76−1.05) 0.181
RTEL1 rs755017
AA 447 (32.51) 329 (31.97) 1.00
AG 660 (48.00) 520 (50.53) 1.08 (0.89−1.30) 0.427
GG 268 (19.49) 180 (17.49) 0.94 (0.84−1.06) 0.340
G allele 0.96 (0.86−1.08) 0.527
NAF1 rs7675998
GG 932 (65.77) 700 (67.90) 1.00
GA 431 (30.42) 296 (28.71) 0.94 (0.78−1.12) 0.491
AA 54 (3.81) 35 (3.39) 0.92 (0.73−1.14) 0.437
A allele 0.93 (0.80−1.08) 0.349
ZNF208 rs8105767
AA 703 (49.58) 487 (48.70) 1.00
AG 593 (41.82) 435 (43.50) 1.06 (0.89−1.26) 0.484
GG 122 (8.60) 78 (7.80) 0.96 (0.82−1.12) 0.607
G allele 1.00 (0.88−1.14) 0.960
Tab.3  Association results of reported telomere length related SNPs with ESCC risk
Grouping of WGS by controls quintile category Controls N (%) Cases N (%) OR(95%CI) a P a
≥0.534 265 (19.9) 177 (20.1) referent −
0.458−0.534 269 (20.2) 182 (20.6) 1.05 (0.80−1.37) 0.745
0.394−0.458 263 (19.8) 158 (17.9) 0.94 (0.71−1.24) 0.657
0.310−0.394 267 (20.1) 198 (22.4) 1.17 (0.89−1.53) 0.259
<0.310 266 (20.0) 168 (19.0) 0.99 (0.75−1.30) 0.940
Tab.4  Association between weighted genetic score (WGS) of relative telomere length and ESCC risk
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