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Journal of Peking University (Health Sciences) ›› 2022, Vol. 54 ›› Issue (3): 412-420. doi: 10.19723/j.issn.1671-167X.2022.03.004

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Interaction between ischemic stroke risk loci identified by genome-wide association studies and sleep habits

Ruo-tong YANG,Meng-ying WANG,Chun-nan LI,Huan YU,Xiao-wen WANG,Jun-hui WU,Si-yue WANG,Jia-ting WANG,Da-fang CHEN,Tao WU,Yong-hua HU*()   

  1. Department of epidemiology and Biostatistics, Peking University School of Public Health, Beijing 100191, China
  • Received:2022-02-27 Online:2022-06-18 Published:2022-06-14
  • Contact: Yong-hua HU E-mail:yhhu@bjmu.edu.cn
  • Supported by:
    the National Natural Science Foundation of China(81230066);the National Natural Science Foundation of China(81473043);the National Natural Science Foundation of China(81703291);the National Natural Science Foundation of China(81872695)

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Abstract:

Objective: To explore the relationship between sleep habits (sleep duration, sleep efficiency, sleep onset timing) and ischemic stroke, and whether there is an interaction between sleep habits and ischemic stroke susceptibility gene loci. Methods: A questionnaire survey, physical examination, blood biochemical testing and genotyping were conducted among rural residents in Beijing, and the gene loci of ischemic stroke suggested by previous genome-wide association studies (GWAS) were screened. Multivariable generalized linear model was used to analyze the correlation between sleep habits, sleep-gene interaction and ischemic stroke. Results: A total of 4 648 subjects with an average age of (58.5±8.7) years were enrolled, including 1 316 patients with ischemic stroke. Compared with non-stroke patients, stroke patients with sleep duration ≥9 hours, sleep efficiency < 80%, and sleep onset timing earlier than 22:00 accounted for a higher proportion (P < 0.05). There was no significant association between sleep duration and risk of ischemic stroke (OR=1.04, 95%CI: 0.99-1.10, P=0.085). Sleep efficiency was inversely associated with the risk of ischemic stroke (OR=0.18, 95%CI: 0.06-0.53, P=0.002). The risk of ischemic stroke in the subjects with sleep efficiency < 80% was 1.47-fold (95%CI: 1.03-2.10, P=0.033) of that in the subjects with sleep efficiency ≥80%. Falling asleep earlier than 22:00 was associated with 1.26 times greater risk of stroke than falling asleep between 22:00 and 22:59 (95%CI: 1.04-1.52, P=0.017). Multifactorial adjustment model showed that rs579459 on ABO gene had an interaction with sleep time (P for interaction =0.040). When there were two T alleles for rs579459 on the ABO gene, those who fell asleep before 22:00 had 1.56 times (95%CI: 1.20-2.04, P=0.001) the risk of stroke compared with those who fell asleep between 22:00 and 22:59, and there was no significant difference when the number of pathogenic alleles was 0 or 1. In the model adjusted only for gender, age and family structure, sleep duration and the number of T allele rs2634074 on PITX2 gene had an interaction with ischemic stroke (P for interaction=0.033). Conclusion: Decreased sleep efficiency is associated with increased risk of ischemic stroke, and falling asleep earlier than 22:00 is associated with higher risk of ischemic stroke. Sleep onset timing interacted with rs579459 in ABO gene and the risk of ischemic stroke. Sleep duration and PITX2 rs2634074 may have a potential interaction with ischemic stroke risk.

Key words: Gene loci, Sleep, Ischemic stroke, Interaction

CLC Number: 

  • R181

Table 1

Basic characteristics of participants"

Items Total
(n= 4 648)		 Participants without IS
(n= 3 332)		 Participants with IS
(n= 1 316)		 P
Age/years, $\bar x \pm s$ 58.5±8.7 57.5±8.7 60.8±8.3 < 0.001
Male, n (%) 2 112 (45.4) 1 384 (41.5) 728 (55.3) < 0.001
Married, n (%) 4 060 (87.4) 2 934 (88.0) 1 126 (85.6) < 0.001
Junior high school education or above, n (%) 2 574 (55.4) 1 962 (58.9) 612 (46.5) < 0.001
Annual household income /10 000 yuan, $\bar x \pm s$ 3.0±4.4 3.2±4.5 2.5±4.2 < 0.001
Smoker, n (%) 1 303 (28.0) 910 (27.3) 393 (29.9) < 0.001
Drinker, n (%) 1 307 (28.1) 971 (29.1) 336 (25.5) < 0.001
Adequate exercise, n (%) 892 (19.2) 673 (20.2) 219 (16.6) 0.006
Vegetables≥300 g/d and fruits≥200 g/d, n (%) 2 988 (64.3) 2 149 (64.5) 839 (63.8) 0.634
BMI/(kg/m2), $\bar x \pm s$ 26.2±3.5 26.1±3.6 26.3±3.4 0.126
Total cholesterol/(mmol/L), $\bar x \pm s$ 3.0±1.1 3.1±1.1 2.9±1.1 0.001
Hypertension, n (%) 3 328 (71.6) 2 182 (65.5) 1 146 (87.1) < 0.001
Diabetes, n (%) 2 449 (52.7) 1 826 (54.8) 623 (47.4) < 0.001
Coronary heart disease, n (%) 1 034 (22.3) 668 (20.1) 366 (27.8) < 0.001
Family medical history, n (%)
  IS 2 887 (62.1) 1 769 (53.1) 1 118 (85.0) < 0.001
  Diabetes 3 696 (79.5) 2 838 (85.2) 858 (65.2) < 0.001
  Coronary heart disease 2 299 (49.5) 1 743 (52.3) 556 (42.3) < 0.001
Sleep duration/h, n (%) < 0.001
   < 7 1 031 (22.2) 758 (22.8) 273 (20.7)
  7.0-8.9 2 393 (51.5) 1 768 (53.1) 625 (47.5)
  ≥9 1 224 (26.3) 806 (24.2) 418 (31.8)
Sleep efficiency/%, n (%) 0.015
  ≥80 4 378 (94.2) 3 156 (94.7) 1 222 (92.9)
   < 80 270 (5.8) 176 (5.3) 94 (7.1)
Sleep onset timing, n (%) < 0.001
   < 22:00 1 111 (23.9) 688 (20.7) 423 (32.1)
  22:00-22:59 1 844 (39.7) 1 354 (40.6) 490 (37.2)
  23:00-23:59 1 058 (22.8) 822 (24.7) 236 (17.9)
  ≥24:00 635 (13.7) 468 (14.1) 167 (12.7)

Table 2

Relationship between sleep behaviors and ischemic stroke"

Sleep behaviors Model 1 Model 2
OR (95%CI) P OR (95%CI) P
Sleep duration/h 1.04 (0.99, 1.08) 0.115 1.04 (0.99, 1.10) 0.085
   < 7 1.04 (0.90, 1.29) 0.407 1.01 (0.83, 1.24) 0.895
  7.0-8.9 1.00 1.00
  ≥9 1.22 (1.04, 1.43) 0.016 1.17 (0.98, 1.40) 0.081
Sleep efficiency/% 0.10 (0.04, 0.26) < 0.001 0.18 (0.06, 0.53) 0.002
  ≥80 1.00 1.00
   < 80 1.71 (1.25, 2.34) 0.001 1.47 (1.03, 2.10) 0.033
Sleep onset timing
   < 22:00 1.44 (1.22, 1.71) < 0.001 1.26 (1.04, 1.52) 0.017
  22:00-22:59 1.00 1.00
  23:00-23:59 0.86 (0.72, 1.04) 0.118 0.93 (0.76, 1.15) 0.517
  ≥24:00 0.86 (0.67, 1.10) 0.223 0.86 (0.66, 1.13) 0.291

Table 3

Basic information of positive SNPs suggested by genome-wide association studies (GWAS) and their association with ischemic stroke"

Chromosome rsID Gene n MAF Risk allele OR (95%CI) P P′
1 rs225132 ERRFI1 4 448 0.34 T 1.09 (0.99, 1.21) 0.083 1.000
1 rs10489177 C1orf156 4 421 0.32 G 1.27 (1.15, 1.41) < 0.001* < 0.001*
2 rs780094 GCKR 3 440 0.47 G 1.03 (0.92, 1.14) 0.629 1.000
2 rs2292832 miR-149 3 394 0.32 T 1.04 (0.93, 1.17) 0.462 1.000
3 rs16851055 SPSB4 4 380 0.20 G 1.16 (1.03, 1.31) 0.015* 0.405
4 rs2200733 PITX2 3 345 0.48 T 1.03 (0.93, 1.15) 0.534 1.000
4 rs2634074 PITX2 4 199 0.40 T 1.23 (1.12, 1.36) < 0.001* < 0.001*
5 rs1428155 GLRA1 3 405 0.32 C 1.03 (0.92, 1.15) 0.597 1.000
5 rs2910164 miR-146a 4 402 0.47 G 0.97 (0.88, 1.07) 0.557 1.000
6 rs556621 HCG27 3 377 0.50 A 1.07 (0.97, 1.19) 0.178 1.000
7 rs662 PON1 3 400 0.37 A 1.12 (1.00, 1.25) 0.042* 1.000
7 rs3735590 PON1 3 444 0.14 C 1.11 (0.96, 1.30) 0.169 1.000
9 rs579459 ABO 4 418 0.34 T 1.29 (1.17, 1.42) < 0.001* < 0.001*
9 rs2383207 CDKN2B-AS1 3 438 0.33 A 1.03 (0.92, 1.15) 0.590 1.000
9 rs505922 ABO 4 419 0.48 C 0.96 (0.88, 1.06) 0.446 1.000
10 rs11196288 HABP2 4 391 0.36 G 1.03 (0.93, 1.14) 0.593 1.000
11 rs660599 MMP-12 3 438 0.12 T 0.95 (0.81, 1.11) 0.518 1.000
12 rs12425791 NINJ2 4 409 0.25 A 0.99 (0.89, 1.11) 0.868 1.000
12 rs11614913 MIR-196A2 4 328 0.50 C 0.98 (0.89, 1.08) 0.702 1.000
12 rs10849373 NINJ2 4 423 0.14 G 1.51 (1.28, 1.79) < 0.001* < 0.001*
12 rs11833579 NINJ2 4 378 0.34 A 1.06 (0.95, 1.17) 0.301 1.000
14 rs1952706 PTCSC3 3 867 0.49 C 0.97 (0.87, 1.07) 0.496 1.000
14 rs2787417 PTCSC3 4 362 0.49 T 0.95 (0.86, 1.04) 0.280 1.000
14 rs934075 PTCSC3 4 415 0.49 G 0.97 (0.88, 1.06) 0.481 1.000
16 rs12445022 JPH3 4 441 0.10 A 1.06 (0.91, 1.23) 0.457 1.000
16 rs879324 ZFHX3 3 433 0.34 T 1.08 (0.97, 1.20) 0.177 1.000
16 rs7193343 ZFHX3 4 428 0.41 T 1.14 (1.03, 1.26) 0.008* 0.216

Table 4

Association between sleep behaviors, rs579459 on ABO gene and IS"

rs579459 number of pathogenic alleles Model 1 Model 2
0(n=784) 1(n=435) 2(n=201) Pint 0(n=784) 1(n=1435) 2(n=2201) Pint
Sleep duration/ h 1.11 (0.97, 1.27) 1.04 (0.96, 1.12) 1.02(0.96, 1.08) 0.889 1.15(0.99, 1.34) 1.03(0.94, 1.13) 1.03 (0.96, 1.11) 0.668
   < 7 0.82 (0.47, 1.37) 1.12 (0.81, 1.55) 1.15(0.89, 1. 48) 0.65 (0.35, 1.18) 1.07(0.74, 1.53) 1.14(0.86, 1.51)
  7.0 ~8.9 1.00 1.00 1.00 1.00 1.00 1.00
  ≥9 1.72 (1.08, 2.72) 1.29 (0.96, 1.72) 1.06(0.84, 1.33) 1.97 (1.15, 3.39) 1.15(0.83, 1.61)) 1.10 (0.85, 1.42)
Sleep efficiency/% 0.57 (0.07, 5.72) 0.04 (0.01, 0.23) 0.06 (0.01, 0.26) 0.576 0.87(0.07, 13.53) 0.06（0.01, 0.38) 0.16 (0.03, 0.86) 0.661
  ≥80 1.00 1.00 1.00 1.00 1.00 1.00
   < 80 0.70(0.26, 1.74) 2.32 (1.35, 4.02) 1.55(0.97, 2.46) 0.62(0.21, 1.74) 1.85 (1.00, 3.43) 1.27 (0.75, 2.15)
Sleep onset timing
   < 22:00 0.78 (0.47, 1.28) 1.21(0.89, 1.66) 1.83 (1.44, 2.32) 0.007 0.65 (0.35, 1.17) 1.02 (0.72, 1.45) 1.56(1.20, 2.04)0.040 0.040
  22:00 -22:59 1.00 1.00 1.00 1.00 1.00 1.00
  23:00 -23:59 0.84 (0.50, 1.40) 0.91 (0.65, 1.27) 0.85 (0.65, 1.10) 0.782 0.70 (0.38, 1.25) 1.00 (0.69, 1.44) 0.97 (0.72, 1.29) 0.310
  ≥24：00 1.63 (0.83, 3.10) 0.72 (0.45, 1.11) 0.84 (0.59, 1.19) 0.719 1.45 (0.67, 3.07) 0.72 (0.44, 1.17) 0.88 (0.59, 1.29) 0.954

Table 5

Association between sleep behaviors, rs2634074 on PITX2 gene and IS"

rs2634074 number of pathogenic alleles Model 1 Model 2
0(n=935) 1(n=1469) 2(n=1795) Pint 0(n=935) 1(n=1469) 2(n=1795) Pint
Sleep duration /h 1.14 (1.02, 1.28) 1.08 (0.99, 1.17) 0.97 (0.90, 1.03) 0.033 1.15 (1.02, 1.31) 1.09 (0.99, 1.20) 0.97 (0.90, 1.05) 0.060
   < 7 0.74 (0.45, 1.20) 1.01 (0.72, 1.42) 1.18 (0.90, 1.55) 0.73 (0.43, 1.24) 0.94 (0.64, 1.37) 1.11 (0.82, 1.50)
  7.0 -8.9 1.00 1.00 1.00 1.00 1.00 1.00
  ≥9 1.66 (1.12, 2.45) 1.19 (0.89, 1.60) 1.01 (0.79, 1.30) 1.71 (1.10, 2.65) 1.18 (0.85, 1.64) 1.00 (0.75, 1.33)
Sleep efficiency /% 0.08 (0.01, 0.73) 0.24 (0.05, 1.27) 0.04 (0.01, 0.24) 0.532 0.14 (0.01, 1.58) 0.61 (0.09, 4.49) 0.03 (0.00, 0.23) 0.230
  ≥80 1.00 1.00 1.00 1.00 1.00 1.00
   < 80 1.62 (0.71, 3.62) 1.58 (0.90, 2.74) 1.76 (1.04, 2.96) 1.35 (0.54, 3.32) 1.22 (0.64, 2.29) 1.84 (1.02, 3.33)
Sleep onsettiming
   < 22:00 1.00 (0.65, 1.54) 1.58 (1.16, 2.17) 1.52 (1.17, 1.98) 0.606 0.80 (0.49, 1.29) 1.22 (0.85, 1.74) 1.45 (1.08, 1.94) 0.223
  22:00 -22:59 1.00 1.00 1.00 1.00 1.00 1.00
  23:00 -23:59 1.13 (0.71, 1.77) 0.86 (0.62, 1.20) 0.78 (0.58, 1.05) 0.398 1.30 (0.78, 2.14) 0.85 (0.58, 1.22) 0.88 (0.64, 1.22) 0.505
  ≥24：00 0.99 (0.52, 1.81) 1.01 (0.66, 1.54) 0.76 (0.50, 1.13) 0.785 0.86 (0.42, 1.70) 0.93 (0.58, 1.49) 0.83 (0.53, 1.29) 0.625
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