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Front. Med.    2018, Vol. 12 Issue (6) : 678-687    https://doi.org/10.1007/s11684-018-0671-7
RESEARCH ARTICLE
Type 2 diabetes is causally associated with depression: a Mendelian randomization analysis
Liping Xuan1,2,3, Zhiyun Zhao1,2,3, Xu Jia1,2,3, Yanan Hou1,2,3, Tiange Wang1,2,3, Mian Li1,2,3, Jieli Lu1,2,3, Yu Xu1,2,3, Yuhong Chen1,2,3, Lu Qi4, Weiqing Wang1,2,3, Yufang Bi1,2,3, Min Xu1,2,3()
1. State Key Laboratory of Medical Genomics, Key Laboratory for Endocrine and Metabolic Diseases of Ministry of Health, National Clinical Research Center for Metabolic Diseases, Collaborative Innovation Center of Systems Biomedicine, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
2. Shanghai Institute of Endocrine and Metabolic Diseases, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
3. Department of Endocrine and Metabolic Diseases, Ruijin Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
4. Department of Epidemiology, Tulane University School of Public Health and Tropical Medicine, New Orleans, LA 70112, USA
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Abstract

Type 2 diabetes (T2D) has been associated with a high prevalence of depression. We aimed to determine the causal relation by performing a Mendelian randomization (MR) study using 34 T2D risk genetic variants validated in East Asians as the instrumental variable (IV). An MR analysis was performed involving 11 506 participants from a large longitudinal study. The T2D genetic risk score (GRS) was built using the 34 typical T2D common variants. We used T2D_GRS as the IV estimator and performed inverse-variance weighted (IVW) and Egger MR analysis. The T2D_GRS was found to be associated with depression with an OR of 1.21 (95% CI: 1.07–1.37) after adjustments for age, sex, body mass index, current smoking and drinking, physical activity, education, and marital status. Using T2D_GRS as the IV, we similarly found a causal relationship between genetically determined T2D and depression (OR: 1.84, 95% CI: 1.25–2.70). Though we found no association between the combined effect of the genetic IVs for T2D and depression with Egger MR (OR: 0.95, 95% CI: 0.42–2.14), we found an association for T2D and depression with IVW (OR: 1.75, 95% CI: 1.31–2.46) after excluding pleiotropic SNPs. Overall, the MR analyses provide evidence inferring a potential causal relationship between T2D and depression.
Keywords causal modeling      depression      Mendelian randomization      type 2 diabetes     
Corresponding Author(s): Min Xu   
Just Accepted Date: 25 October 2018   Online First Date: 16 November 2018    Issue Date: 03 December 2018
 Cite this article:   
Liping Xuan,Zhiyun Zhao,Xu Jia, et al. Type 2 diabetes is causally associated with depression: a Mendelian randomization analysis[J]. Front. Med., 2018, 12(6): 678-687.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-018-0671-7
https://academic.hep.com.cn/fmd/EN/Y2018/V12/I6/678
T2D_GRS P for trend
Quartile 1 Quartile 2 Quartile 3 Quartile 4
n 2878 2874 2876 2878 /
Age, year 63.2±0.3 63.4±0.3 63.3±0.3 63.2±0.3 0.92
Male, n (%) 987 (34.3) 978 (34.0) 1052 (36.6) 1073 (37.3) 0.0039
Current smoker, n (%) 396 (14.6) 389 (14.4) 412 (15.1) 438 (16.0) 0.11
Current drinker, n (%) 240 (8.8) 245 (9.1) 265 (9.8) 279 (10.2) 0.05
BMI, kg/m2 25.4±0.07 25.4±0.07 25.2±0.07 25.1±0.07 0.0004
FPG, mmol/L 5.78±0.03 5.97±0.03 6.08±0.03 6.20±0.03 <0.0001
2h PG, mmol/L 8.30±0.07 8.82±0.07 9.05±0.07 9.40±0.07 <0.0001
log10HOMA-IR 0.47±0.01 0.49±0.01 0.50±0.01 0.50±0.01 0.03
log10HOMA-β, % 4.14±0.01 4.06±0.01 4.03±0.01 3.97±0.01 <0.0001
log10TG, mmol/L 0.29±0.009 0.28±0.009 0.28±0.009 0.29±0.009 0.82
TC, mmol/L 4.92±0.02 4.94±0.02 4.95±0.02 4.96±0.02 0.31
SBP, mmHg 136.3±0.4 137.0±0.4 137.1±0.4 137.2±0.4 0.02
DBP, mmHg 77.4±0.2 77.2±0.2 77.4±0.2 76.9±0.2 0.27
Hypertension, n (%) 1680 (58.4) 1646 (57.3) 1650 (57.4) 1647 (57.3) 0.42
Diabetes, n (%) 523 (18.2) 692 (24.1) 749 (26.0) 896 (31.1) <0.0001
PHQ-9 score 0.475±0.028 0.506±0.028 0.501±0.028 0.586±0.028 0.009
Depression, n (%) 60 (2.08) 71 (2.47) 75 (2.61) 84 (2.92) 0.04
Sub-threshold depression, n (%) 53 (1.85) 55 (1.92) 64 (2.23) 70 (2.44) 0.08
Probable depression, n (%) 7 (0.24) 16 (0.56) 11 (0.38) 14 (0.49) 0.30
Tab.1  Characteristics of the participants according to quartiles of weighted T2D_GRS
Gene Chr. SNP Effect/other allele EAF Pleiotropic effect Diabetes Present depression
OR 95% CI P value OR 95% CI P value
PROX1 1 rs340874 G/A 0.38 No 1.04 1.03–1.04 0.18 1.16 0.99–1.38 0.07
BCL11 2 rs243021 A/G 0.67 Yes 1.08 1.01–1.15 0.02 1.13 0.94–1.35 0.20
GCKR 2 rs780094 G/A 0.47 Yes 1.01 0.95–1.08 0.67 1.02 0.86–1.20 0.86
IRS1 2 rs2943641 C/T 0.94 No 1.32 1.15–1.51 <0.0001 1.16 0.81–1.66 0.43
IGF2BP2 3 rs4402960 T/G 0.24 Yes 1.17 1.08–1.25 <0.0001 0.94 0.77–1.14 0.50
PPARG 3 rs1801282 C/G 0.94 No 1.11 0.98–1.27 0.10 0.83 0.61–1.14 0.26
PSMD6 3 rs831571 C/T 0.64 No 1.01 0.95–1.08 0.67 1.12 0.94–1.33 0.20
UBE2E2 3 rs7612463 C/A 0.79 Yes 1.15 1.07–1.25 0.0003 0.89 0.73–1.08 0.23
MAEA 4 rs6815464 C/G 0.57 No 1.07 1.01–1.14 0.02 1.13 0.96–1.34 0.14
CDKAL1 6 rs9356744 T/C 0.40 Yes 1.24 1.17–1.32 <0.0001 1.07 0.91–1.27 0.40
ZFAND3 6 rs9470794 C/T 0.29 No 1.04 0.97–1.11 0.31 1.08 0.91–1.29 0.38
DGKB 7 rs2191349 T/G 0.65 Yes 1.07 0.998–1.14 0.06 1.14 0.95–1.36 0.16
GCC1/PAX4 7 rs6467136 A/G 0.12 No 0.93 0.86–1.01 0.10 1.14 0.90–1.45 0.28
JAZF1 7 rs864745 T/C 0.77 Yes 1.05 0.97–1.12 0.23 1.12 0.92–1.36 0.28
SLC30A8 8 rs13266634 C/T 0.56 Yes 1.13 1.06–1.20 <0.0001 1.17 0.997–1.38 0.06
TP53INP1 8 rs896854 A/G 0.33 No 1.09 1.02–1.17 0.007 1.12 0.94–1.33 0.20
CDKN2A/B 9 rs10811661 T/C 0.53 No 1.19 1.12–1.26 <0.0001 1.00 0.84–1.17 0.95
GLIS3 9 rs7041847 A/G 0.45 No 1.01 0.95–1.07 0.86 0.94 0.80–1.11 0.48
PTPRD 9 rs17584499 T/C 0.09 Yes 0.95 0.86–1.06 0.40 1.04 0.78–1.39 0.77
CDC123/CAMK1D 10 rs10906115 A/G 0.63 Yes 1.12 1.05–1.19 0.0005 1.02 0.86–1.21 0.79
CDC123/CAMK1D 10 rs12779790 G/A 0.17 No 1.06 0.98–1.15 0.16 1.13 0.92–1.40 0.25
HHEX/IDE 10 rs1111875 G/A 0.27 Yes 1.07 0.998–1.14 0.06 0.96 0.80–1.15 0.65
TCF7L2 10 rs7903146 T/C 0.03 Yes 1.27 1.08–1.49 0.005 1.25 0.83–1.88 0.30
CENTD2 11 rs1552224 A/C 0.92 Yes 1.08 0.97–1.20 0.19 1.13 0.83–1.53 0.45
KCNQ1 11 rs231362 C/T 0.89 Yes 1.10 0.997–1.22 0.06 1.08 0.82–1.41 0.59
KCNQ1 11 rs2237892 C/T 0.67 Yes 1.24 1.16–1.32 <0.0001 0.91 0.77–1.08 0.29
KCNJ11 11 rs5215 C/T 0.39 Yes 1.08 1.01–1.15 0.02 0.94 0.79–1.11 0.46
SPRY2 13 rs1359790 G/A 0.72 No 1.13 1.05–1.21 0.0009 1.09 0.90–1.31 0.38
C2CD4A/C2CD4B 15 rs7172432 A/G 0.61 No 1.07 1.01–1.14 0.03 1.06 0.90–1.26 0.49
FTO 16 rs17817449 G/T 0.12 Yes 1.10 1.00–1.21 0.049 1.10 0.86–1.42 0.43
TCF2(HNF1B) 17 rs4430796 G/A 0.29 Yes 1.19 1.11–1.27 <0.0001 1.01 0.85–1.22 0.88
SRR 17 rs391300 G/A 0.70 No 1.02 0.95–1.09 0.65 1.08 0.90–1.29 0.43
PEPD 19 rs3786897 A/G 0.52 Yes 1.09 1.03–1.16 0.006 0.93 0.79–1.10 0.41
FITM2/R3HDML/HNF4A 20 rs6017317 G/T 0.57 Yes 1.05 0.98–1.11 0.17 1.08 0.91–1.27 0.38
Tab.2  Information of each individual SNP and its association with diabetes and depression
Gene SNP BMI SBP DBP TC log10TG
β (SE) P value β (SE) P value β (SE) P value β (SE) P value β (SE) P value
PPARG rs1801282 −0.11 (0.10) 0.27 −0.08 (0.51) 0.88 −0.15 (0.26) 0.56 0.03 (0.03) 0.33 0.001 (0.006) 0.85
KCNJ11 rs5215 −0.13 (0.05) 0.006 0.27 (0.26) 0.29 0.23 (0.13) 0.08 −0.003 (0.02) 0.87 −0.002 (0.003) 0.50
TCF7L2 rs7903146 −0.18 (0.13) 0.16 0.63 (0.69) 0.36 0.20 (0.35) 0.57 0.05 (0.04) 0.25 0.009 (0.008) 0.27
TCF2(HNF1B) rs4430796 −0.04 (0.05) 0.40 0.48 (0.28) 0.08 0.04 (0.14) 0.75 0.03 (0.02) 0.06 0.003 (0.003) 0.38
IGF2BP2 rs4402960 −0.11 (0.06) 0.046 0.29 (0.29) 0.32 −0.04 (0.15) 0.78 0.004 (0.02) 0.84 0.005 (0.003) 0.16
CDKN2A/B rs10811661 −0.01 (0.05) 0.76 0.40 (0.25) 0.15 −0.09 (0.13) 0.47 −0.004 (0.02) 0.81 0.004 (0.003) 0.18
HHEX/IDE rs1111875 −0.15 (0.05) 0.005 −0.11 (0.28) 0.68 −0.02 (0.14) 0.92 −0.03 (0.02) 0.08 0.005 (0.003) 0.13
SLC30A8 rs13266634 −0.01 (0.05) 0.76 0.49 (0.24) 0.04 0.12 (0.13) 0.34 0.04 (0.01) 0.01 −0.0004 (0.003) 0.89
JAZF1 rs864745 −0.03 (0.06) 0.65 0.07 (0.29) 0.81 −0.14 (0.15) 0.37 0.02 (0.02) 0.24 0.005 (0.003) 0.16
CDC123/CAMK1D rs12779790 −0.03 (0.06) 0.65 0.22 (0.33) 0.51 0.002 (0.17) 0.99 0.02 (0.02) 0.28 0.0003 (0.004) 0.95
IRS1 rs2943641 0.15 (0.10) 0.12 0.41 (0.52) 0.43 0.24 (0.27) 0.37 −0.02 (0.03) 0.59 0.009 (0.006) 0.15
PROX1 rs340874 −0.05 (0.05) 0.31 −0.26 (0.26) 0.31 −0.10 (0.13) 0.44 −0.00002 (0.02) 0.999 0.0007 (0.003) 0.81
GCKR rs780094 0.02 (0.05) 0.61 −0.59 (0.25) 0.02 −0.21 (0.13) 0.11 −0.05 (0.02) 0.0007 −0.02 (0.003) <0.0001
DGKB rs2191349 −0.02 (0.05) 0.73 0.75 (0.26) 0.004 0.45 (0.13) 0.0008 0.03 (0.02) 0.04 0.005 (0.003) 0.13
BCL11 rs243021 0.11 (0.05) 0.04 −0.003 (0.27) 0.99 0.12 (0.14) 0.38 −0.03 (0.02) 0.03 −0.003 (0.003) 0.30
CENTD2 rs1552224 −0.07 (0.08) 0.40 −1.39 (0.44) 0.002 −0.51 (0.23) 0.03 0.02 (0.03) 0.44 0.003 (0.005) 0.51
KCNQ1 rs231362 −0.15 (0.07) 0.045 −0.14 (0.40) 0.72 0.03 (0.20) 0.88 0.02 (0.02) 0.34 −0.01 (0.005) 0.02
TP53INP1 rs896854 0.01 (0.05) 0.84 0.06 (0.26) 0.82 0.01 (0.14) 0.94 0.0006 (0.02) 0.97 0.0008 (0.003) 0.79
KCNQ1 rs2237892 −0.08 (0.05) 0.09 0.04 (0.27) 0.88 −0.05 (0.14) 0.70 −0.005 (0.02) 0.79 0.0008 (0.003) 0.79
C2CD4A/C2CD4B rs7172432 −0.06 (0.05) 0.20 −0.002 (0.26) 0.99 −0.15 (0.13) 0.26 0.03 (0.02) 0.07 −0.0004 (0.0002) 0.66
SPRY2 rs1359790 −0.04 (0.05) 0.41 −0.18 (0.28) 0.53 −0.07 (0.14) 0.62 −0.0008 (0.02) 0.96 −0.005 (0.003) 0.09
FITM2/R3HDML/HNF4A rs6017317 0.06 (0.05) 0.22 −0.55 (0.25) 0.03 −0.005 (0.13) 0.97 0.01 (0.02) 0.41 0.003 (0.003) 0.32
UBE2E2 rs7612463 −0.05 (0.06) 0.36 0.12 (0.31) 0.70 −0.44 (0.16) 0.005 0.02 (0.02) 0.20 0.003 (0.004) 0.46
PTPRD rs17584499 0.07 (0.08) 0.39 0.94 (0.44) 0.03 0.10 (0.23) 0.67 −0.03 (0.03) 0.28 −0.006 (0.005) 0.26
SRR rs391300 −0.06 (0.05) 0.21 −0.17 (0.27) 0.54 −0.18 (0.14) 0.20 0.003 (0.02) 0.87 −0.002 (0.003) 0.59
CDC123/CAMK1D rs10906115 −0.09 (0.05) 0.07 0.51 (0.26) 0.048 −0.01 (0.13) 0.93 0.01 (0.02) 0.54 0.0003 (0.003) 0.92
PSMD6 rs831571 −0.09 (0.05) 0.06 −0.07 (0.26) 0.78 −0.04 (0.13) 0.77 0.005 (0.02) 0.74 −0.002 (0.003) 0.43
MAEA rs6815464 0.007 (0.05) 0.88 −0.04 (0.25) 0.87 −0.10 (0.13) 0.42 −0.009 (0.02) 0.54 0.005 (0.003) 0.08
ZFAND3 rs9470794 0.09 (0.05) 0.08 −0.47 (0.27) 0.09 −0.19 (0.14) 0.18 0.004 (0.02) 0.81 0.002 (0.003) 0.46
GCC1/PAX4 rs6467136 −0.005 (0.06) 0.94 −0.08 (0.34) 0.82 −0.09 (0.17) 0.60 0.002 (0.02) 0.91 −0.004 (0.004) 0.32
GLIS3 rs7041847 −0.04 (0.05) 0.36 0.32 (0.25) 0.21 0.11 (0.13) 0.37 0.02 (0.02) 0.14 0.0002 (0.003) 0.95
PEPD rs3786897 −0.10 (0.05) 0.03 0.74 (0.25) 0.003 −0.02 (0.13) 0.86 −0.01 (0.02) 0.43 0.005 (0.003) 0.06
CDKAL1 rs9356744 −0.11 (0.05) 0.02 0.50 (0.25) 0.048 0.16 (0.13) 0.22 0.01 (0.02) 0.44 0.002 (0.003) 0.40
FTO rs17817449 0.21 (0.07) 0.004 0.13 (0.39) 0.74 −0.19 (0.20) 0.34 −0.01 (0.02) 0.66 −0.008 (0.004) 0.09
Tab.3  The associations of each SNP with T2D related traits
Depression
Model 1 Model 2 Model 3
OR (95% CI) P value OR (95% CI) P value OR (95% CI) P value
Un-weighted GRS (per SD, points)
T2D_GRS/concluding 34 SNPs (3.62) 1.18 (1.05–1.33) 0.006 1.21 (1.07–1.37) 0.002 1.17 (1.03–1.32) 0.01
T2D_GRS/concluding 14 SNPs (2.33) 1.19 (1.05–1.34) 0.004 1.21 (1.07–1.37) 0.002 1.19 (1.06–1.33) 0.004
Weighted GRS (per SD, points)
T2D_GRS/concluding 34 SNPs (3.90) 1.11 (0.99–1.25) 0.08 1.14 (1.01–1.29) 0.03 1.10 (0.97–1.25) 0.13
T2D_GRS/concluding 14 SNPs (2.51) 1.15 (1.03–1.30) 0.02 1.19 (1.06–1.35) 0.004 1.16 (1.02–1.31) 0.02
Present T2D 1.37 (1.05–1.78) 0.02 1.45 (1.10–1.92) 0.009 / /
Tab.4  Associations of present depression with T2D_GRS and T2D
T2D (N = 2860) Non-T2D (N = 8646)
OR (95% CI) P value OR (95% CI) P value
Depression (n, %) 84 (2.94) / 206 (2.38) /
Un-weighted GRS (per SD, points)
T2D_GRS/concluding 34 SNPs (3.62) 1.31 (1.04–1.65) 0.02 1.12 (0.97–1.30) 0.12
T2D_GRS/concluding 14 SNPs (2.33) 1.44 (1.14–1.82) 0.002 1.09 (0.95–1.26) 0.23
Weighted GRS (per SD, points)
T2D_GRS/concluding 34 SNPs (3.90) 1.32 (1.04–1.67) 0.02 1.03 (0.89–1.19) 0.65
T2D_GRS/concluding 14 SNPs (2.51) 1.46 (1.15–1.85) 0.002 1.06 (0.92–1.23) 0.43
Tab.5  The associations of present depression with T2D_GRS according to present T2D status
T2D_GRS /concluding 34 SNPs T2D_GRS/concluding 14 SNPs
OR 95% CI P value OR 95% CI P value
Weighted GRS 1.57 1.04–2.37 0.02 3.41 1.48–7.86 0.001
Un-weighted GRS 1.83 1.25–2.70 0.0003 3.67 1.63–8.26 0.0002
IVW 1.30 1.03–1.63 0.03 1.79 1.31–2.46 0.003
Egger Estimate 0.75 0.50–1.13 0.18 0.95 0.42–2.14 0.91
Egger Intercept (in b) 0.08 0.03–0.11 0.005 0.08 −0.02–0.19 0.13
Tab.6  Sensitivity analysis of T2D with depression
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