Evaluation of Relevance between Advanced Glycation End Products and Diabetic Retinopathy Stages Using Skin Autofluorescence
Abstract
:1. Introduction
2. Materials and Methods
2.1. Subjects
2.2. Measurement of AGEs in the Fingertip Skin
2.3. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Parameters | Control | DM | p-Value a | □ | NDR | DR | p-Value b |
---|---|---|---|---|---|---|---|
N | 165 | 229 | 101 | 128 | |||
Age (years) | |||||||
Mean ± SD | 70.9 ± 14.1 | 66.6 ± 13.0 | 0.0017 ** | 68.0 ± 14.6 | 65.5 ± 11.6 | 0.0028 ** | |
range | 23–95 | 16–95 | 16–95 | 32–92 | |||
p-value, vs. Control c | 0.0845 | 0.0007 ## | |||||
p-value, vs. NDR c | − | 0.1638 | |||||
Sex | |||||||
Men, n (%) | 47 (28.5) | 125 (54.6) | <0.0001 ** | 49 (48.5) | 76 (59.4) | <0.0001 ** | |
Women, n (%) | 118 (71.5) | 104 (45.4) | 52 (51.5) | 52 (40.6) | |||
p-value, vs. Control c | 0.0057 ## | <0.0001 ## | |||||
p-value, vs. NDR c | − | 0.1102 | |||||
Hypertension | |||||||
No, n (%) | 94 (57.0) | 105 (45.9) | 0.0323 * | 49 (48.5) | 56 (43.8) | 0.0723 | |
Yes, n (%) | 71 (43.0) | 124 (54.1) | 52 (51.5) | 72 (56.2) | |||
HbA1c (%) | |||||||
Mean ± SD | − | 7.8 ± 0.1 | − | 8.1 ± 2.7 | 7.6 ± 1.8 | - | |
range | − | 4.4–17.3 | 4.4–17.3 | 5.6–16.0 | |||
Insulin usage | |||||||
No, n (%) | − | 144 (63.7) | − | 71 (72.4) | 73 (57.0) | - | |
Yes, n (%) | − | 82 (36.3) | 27 (27.6) | 55 (43.0) | |||
Current smoking habit | |||||||
No, n (%) | 153 (92.7) | 189 (82.9) | 0.0039 ** | 82 (81.2) | 107 (84.2) | 0.0132 * | |
Yes, n (%) | 12 (7.3) | 39 (17.1) | 19 (18.8) | 20 (15.8) | |||
p-value, vs. Control c | 0.0057 ## | 0.0242 # | |||||
p-value, vs. NDR c | - | 0.5971 | |||||
Lens status | |||||||
Phakic, n (%) | 132 (80.0) | 143 (62.5) | 0.0002 ** | 79 (78.2) | 64 (50.0) | <0.0001 ** | |
Pseudophakic, n (%) | 33 (20.0) | 87 (37.5) | 22 (21.8) | 64 (50.0) | |||
p-value, vs. Controlc | 0.7564 | <0.0001 ## | |||||
p-value, vs. NDRc | − | <0.0001 ## | |||||
BCVA (LogMAR) | |||||||
Mean ± SD | 0.12 ± 0.22 | 0.34 ± 0.65 | <0.0001 ** | 0.10 ± 0.27 | 0.53 ± 0.78 | <0.0001 ** | |
range | −0.08–1.40 | −0.08–2.89 | −0.08–1.30 | −0.08–2.89 | |||
p-value, vs. Control c | 0.7673 | <0.0001 ## | |||||
p-value, vs. NDR c | − | <0.0001 ## | |||||
Highest IOP (mmHg) | |||||||
Mean ± SD | 14.3 ± 2.8 | 19.2 ± 9.5 | <0.0001 ** | 16.5 ± 4.3 | 21.4 ± 11.7 | <0.0001 ** | |
range | 6.9–20.0 | 8.0–80.0 | 9.7–35.0 | 8.0–80.0 | |||
p-value, vs. Control c | 0.0173 # | <0.0001 ## | |||||
p-value, vs. NDR c | − | <0.0001 ## | |||||
AGEs score (A.U.) | |||||||
Mean ± SD | 0.52 ± 0.12 | 0.59 ± 0.17 | <0.0001 ** | 0.58 ± 0.16 | 0.60 ± 0.18 | <0.0001 ** | |
range | 0.26–1.21 | 0.25–1.55 | 0.25–1.48 | 0.26–1.55 | |||
p-value, vs. Control c | 0.0012 ## | <0.0001 ## | |||||
p-value, vs. NDR c | − | 0.3349 |
Parameters | Q1 | Q2 | Q3 | Q4 | p-Value a |
---|---|---|---|---|---|
Range | Low–≤0.467 | >0.467–≤0.539 | >0.539–≤0.635 | >0.635–High | |
N | |||||
Age (years) | |||||
Mean ± SD | 71.4 ± 12.3 | 68.1 ± 12.9 | 68.5 ± 13.8 | 65.5 ± 15.0 | 0.0259 * |
Range | 16–95 | 23–92 | 23–95 | 28–94 | |
p-value, vs. Q1 b | − | 0.0903 | 0.1271 | 0.0024 # | |
p-value, vs. Q2 b | − | − | 0.8571 | 0.1851 | |
p-value, vs. Q3 b | − | − | − | 0.1296 | |
Sex | |||||
Men, n (%) | 34 (33.7) | 40 (41.4) | 41 (41.4) | 57 (58.2) | 0.0011 ** |
Women, n (%) | 67 (66.3) | 56 (58.3) | 58 (58.6) | 41 (41.8) | |
p-value, vs. Q1 b | − | 0.3030 | 0.3069 | 0.0006 ## | |
p-value, vs. Q2 b | − | − | 1.0000 | 0.0310 | |
p-value, vs. Q3 b | − | − | − | 0.0227 | |
Hypertension | |||||
No, n (%) | 52 (51.5) | 55 (57.3) | 50 (50.5) | 42 (42.9) | 0.1647 |
Yes, n (%) | 49 (48.5) | 41 (42.7) | 49 (49.5) | 56 (57.1) | |
Diabetic retinopathy | |||||
Control, n (%) | 55 (54.5) | 45 (46.9) | 47 (47.5) | 18 (18.4) | <0.0001 ** |
NDR, n (%) | 24 (23.8) | 23 (24.0) | 24 (24.2) | 30 (30.6) | |
SDR, n (%) | 7 (6.9) | 7 (7.3) | 11 (11.1) | 11 (11.2) | |
PPDR, n (%) | 7 (6.9) | 9 (9.4) | 3 (3.0) | 6 (6.1) | |
PDR, n (%) | 8 (7.9) | 12 (12.5) | 14 (14.1) | 33 (33.7) | |
HbA1c (%) | |||||
Mean ± SD | 7.5 ± 1.2 | 8.0 ± 2.2 | 7.8 ± 2.3 | 7.9 ± 2.3 | 0.6009 |
Range | 5.6–10.8 | 5.6–14.6 | 5.8–17.3 | 4.4–16 | |
Insulin use | |||||
No, n (%) | 30 (66.7) | 38 (74.5) | 33 (66.0) | 43 (53.8) | 0.0530 |
Yes, n (%) | 15 (33.3) | 13 (25.5) | 17 (34.0) | 37 (46.3) | |
Current smoking habit | |||||
No, n (%) | 86 (85.1) | 82 (86.3) | 90 (90.9) | 84 (85.7) | 0.6899 |
Yes, n (%) | 15 (14.9) | 13 (13.7) | 9 (9.1) | 14 (14.3) | |
Lens status | |||||
Phakic, n (%) | 76 (75.3) | 70 (72.9) | 72 (72.7) | 58 (59.2) | 0.0213 * |
Pseudophakic, n (%) | 25 (24.8) | 26 (27.1) | 27 (27.3) | 40 (40.9) | |
p-value, vs. Q1 b | − | 0.7466 | 0.7480 | 0.0230 | |
p-value, vs. Q2 b | − | − | 1.0000 | 0.0496 | |
p-value, vs. Q3 b | − | − | − | 0.0513 | |
BCVA (logMAR) | |||||
Mean ± SD | 0.19 ± 0.39 | 0.23 ± 0.47 | 0.23 ± 0.54 | 0.33 ± 0.66 | 0.3040 |
Range | −0.08–2.89 | −0.08–2.89 | −0.08–2.89 | −0.08–2.89 | |
Highest IOP (mmHg) | |||||
Mean ± SD | 15.4 ± 5.1 | 16.0 ± 6.0 | 17.8 ± 8.3 | 19.6–0.78 | 0.0006 ** |
Range | 6.9–44 | 10–63 | 8–68 | 9–80 | |
p-value, vs. Q1 b | − | 0.5748 | 0.0286 | 0.0001 ## | |
p-value, vs. Q2 b | − | − | 0.1082 | 0.0013 ## | |
p-value, vs. Q3 b | − | − | − | 0.1003 |
Parameters | Q1 | Q2 | Q3 | Q4 |
---|---|---|---|---|
Entire model | ||||
p-value | — | 0.0001 ** | 0.0005 ** | <0.0001 ** |
Age (/year) | ||||
p-value | — | 0.0981 | 0.1670 | 0.0540 |
OR (95% CI) | 1 | 0.98 (0.95–1.00) | 0.98 (0.96–1.01) | 1.03 (0.99–1.05) |
Women (/men) | ||||
p-value | — | 0.2552 | 0.1668 | 0.0059 ** |
OR (95% CI) women/men | 1 | 0.68 (0.35–1.32) | 0.62 (0.33–1.21) | 0.38 (0.20–0.76) ** |
Hypertension, yes (/no) | ||||
p-value | — | 0.6611 | 0.5677 | 0.1388 |
OR (95% CI) | 1 | 0.87 (0.48–1.59) | 1.19 (0.64–2.24) | 1.64 (0.85–3.18) |
DR, yes (/no) | ||||
p-value | 0.9521 | 0.9547 | 0.0009 ** | |
OR (95% CI) non-PDR/control | 1.11 (0.58–2.11) | 0.95 (0.45–2.00) | 3.09 (1.48–6.44) ** | |
OR (95% CI) PDR/control | 1.08 (0.31–3.72) | 1.10 (0.31–3.83) | 6.73 (1.96–23.16) ** | |
OR (95% CI) PDR/non-PDR | 0.98 (0.30–3.16) | 1.17 (0.35–3.92) | 2.18 (0.68–6.96) | |
Current smoking habit, yes(/no) | ||||
p-value | — | 0.3262 | 0.0198 * | 0.1309 |
OR (95% CI) | 1 | 0.64 (0.26–1.58) | 0.29 (0.10–0.82) * | 0.48 (0.18–1.25) |
Phakic (/pseudophakic) | ||||
p value | — | 0.4358 | 0.5659 | 0.3425 |
OR (95% CI) | 1 | 0.75 (0.36–1.56) | 1.26 (0.57–2.77) | 0.67 (0.29–1.53) |
BCVA (/logMAR) | ||||
p-value | — | 0.5757 | 0.4068 | 0.7487 |
OR (95% CI) | 1 | 1.24 (0.56–2.85) | 0.70 (0.31–1.62) | 0.67 (0.29–1.53) |
Highest IOP (/mmHg) | ||||
p-value | — | 0.9206 | 0.0097 ** | 0.6988 |
OR (95% CI) | 1 | 1.00 (0.93–1.06) | 1.09 (1.01–1.16) ** | 0.99 (0.93–1.05) |
Parameters | Non-PDR | PDR | p-Value a | □ | PDR, non-NVG | PDR, NVG | p-Value b |
---|---|---|---|---|---|---|---|
N | 162 | 67 | 45 | 22 | |||
Age (years) | |||||||
Mean ± SD | 68.4 ± 13.2 | 62.2 ± 11.6 | 0.0009 ** | 62.0 ± 11.8 | 62.5 ± 11.5 | 0.0039 ** | |
Range | 16–95 | 32–83 | 32–82 | 38–83 | |||
p-value, v.s. no PDRc | 0.0033 # | 0.0411 | |||||
p-value, v.s. PDRc | — | 0.8967 | |||||
Sex | |||||||
Men, n (%) | 84 (51.9) | 41 (61.2) | 0.2433 | 29 (64.4) | 12 (54.6) | 0.3242 | |
Women, n (%) | 78 (48.1) | 26 (38.8) | 16 (35.6) | 10 (45.5) | |||
Hypertension | |||||||
No, n (%) | 76 (46.9) | 29 (43.3) | 0.6633 | 21 (46.7) | 8 (36.4) | 0.6430 | |
Yes, n (%) | 86 (53.1) | 38 (56.7) | 24 (53.3) | 14 (63.6) | |||
HbA1c (%) | |||||||
Mean ± SD | 8.0 ± 2.2 | 7.4 ± 1.8 | 0.0313 * | 7.6 ± 0.3 | 7.2 ± 1.5 | 0.1369 | |
range | 4.4–17.3 | 5.6–16 | 5.9–16.0 | 5.6–11.6 | |||
Insulin usage | |||||||
No, n (%) | 107 (67.3) | 37 (55.2) | 0.0966 | 28 (62.2) | 9 (40.9) | 0.0530 | |
Yes, n (%) | 52 (32.7) | 30 (44.8) | 17 (37.8) | 13 (50.1) | |||
Current smoking habit | |||||||
No, n (%) | 132 (82.0) | 57 (85.1) | 0.7002 | 39 (86.7) | 18 (81.8) | 0.7547 | |
Yes, n (%) | 29 (18.0) | 10 (16.7) | 6 (13.3) | 4 (18.2) | |||
Lens status | |||||||
Phakic, n (%) | 121 (74.7) | 23 (34.3) | <0.0001 ** | 19 (42.2) | 4 (18.2) | <0.0001 ** | |
Pseudophakic, n (%) | 41 (25.3) | 44 (65.7) | 26 (57.8) | 18 (81.8) | |||
p-value, v.s. no PDR c | 0.0001 ## | <0.0001 ## | |||||
p-value, v.s. PDR c | − | 0.0606 | |||||
BCVA (LogMAR) | |||||||
Mean ± SD | 0.14 ± 28 | 0.83 ± 0.95 | <0.0001 ** | 0.74 ± 0.86 | 1.01 ± 1.11 | <0.0001 ** | |
range | −0.07–2.88 | −0.08–2.89 | −0.08–2.89 | −0.08–2.89 | |||
p-value, v.s. no PDR c | 0.0002 ## | <0.0001 ## | |||||
p-value, v.s. PDR c | − | 0.1614 | |||||
Highest IOP (mmHg) | |||||||
Mean ± SD | 16.6 ± 4.1 | 25.7 ± 1.3 | <0.0001 ** | 19.9 ± 8.6 | 37.5 ± 17.3 | <0.0001 ** | |
range | 9–35 | 8–80 | 8–51 | 17–80 | |||
p-value, v.s. no PDR c | <0.0001 ## | <0.0001 ## | |||||
p-value, v.s. PDR c | − | 0.0748 | |||||
AGEs score (A.U.) | |||||||
Mean ± SD | 0.56 ± 0.15 | 0.64 ± 0.02 | 0.0015 * | 0.64 ± 0.19 | 0.64 ± 0.23 | 0.0064 ** | |
range | 0.25–1.48 | 0.39–1.55 | 0.40–1.53 | 0.39–1.55 | |||
p-value, v.s. no PDR c | 0.0059 # | 0.0426 | |||||
p-value, v.s. PDR c | − | 0.9852 |
Parameters | OR | 95% CI | p-Value a |
---|---|---|---|
Entire model | — | — | <0.0001 ** |
Age (/years) | 0.92 ** | 0.89–0.95 | <0.0001 ** |
Women(/men) | 0.35 * | 0.15–0.81 | 0.0130 * |
Hypertension, yes (/no) | 1.20 | 0.54–2.66 | 0.6629 |
Current smoking habit, yes (/no) | 0.48 | 0.13–1.79 | 0.2613 |
Phakic (/pseudophakic) | 0.08 ** | 0.03–0.22 | <0.0001 ** |
BCVA (/logMAR) | 23.67 ** | 7.40–75.75 | <0.0001 ** |
Highest IOP (/mmHg) | 1.08 * | 1.01–1.16 | 0.0197 * |
AGE score (/A.U.) | 27.85 * | 2.69–288.30 | 0.0100 * |
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Takayanagi, Y.; Yamanaka, M.; Fujihara, J.; Matsuoka, Y.; Gohto, Y.; Obana, A.; Tanito, M. Evaluation of Relevance between Advanced Glycation End Products and Diabetic Retinopathy Stages Using Skin Autofluorescence. Antioxidants 2020, 9, 1100. https://doi.org/10.3390/antiox9111100
Takayanagi Y, Yamanaka M, Fujihara J, Matsuoka Y, Gohto Y, Obana A, Tanito M. Evaluation of Relevance between Advanced Glycation End Products and Diabetic Retinopathy Stages Using Skin Autofluorescence. Antioxidants. 2020; 9(11):1100. https://doi.org/10.3390/antiox9111100
Chicago/Turabian StyleTakayanagi, Yuji, Mikihiro Yamanaka, Jo Fujihara, Yotaro Matsuoka, Yuko Gohto, Akira Obana, and Masaki Tanito. 2020. "Evaluation of Relevance between Advanced Glycation End Products and Diabetic Retinopathy Stages Using Skin Autofluorescence" Antioxidants 9, no. 11: 1100. https://doi.org/10.3390/antiox9111100
APA StyleTakayanagi, Y., Yamanaka, M., Fujihara, J., Matsuoka, Y., Gohto, Y., Obana, A., & Tanito, M. (2020). Evaluation of Relevance between Advanced Glycation End Products and Diabetic Retinopathy Stages Using Skin Autofluorescence. Antioxidants, 9(11), 1100. https://doi.org/10.3390/antiox9111100