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Acute Renal Failure
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Urinary Biomarkers in the Early Detection of Acute Kidney Injury after Cardiac Surgery

Won K. Han, Gebhard Wagener, Yanqing Zhu, Shuang Wang and H. Thomas Lee
CJASN May 2009, 4 (5) 873-882; DOI: https://doi.org/10.2215/CJN.04810908
Won K. Han
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Gebhard Wagener
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Yanqing Zhu
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Shuang Wang
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H. Thomas Lee
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    Figure 1.

    Pattern of urinary biomarker expression. Graphs show mean normalized urinary kidney injury molecule-1 (KIM-1), N-acetyl-β-D-glucosaminidase (NAG), and neutrophil gelatinase associated lipocalin (NGAL) concentrations at multiple time points after cardiac surgeries. Error bars are SEM. AKI, acute kidney injury; early AKI, development of acute kidney injury within first 24 h after operation; late AKI, development of acute kidney injury between 24 and 72 h after operation; Ucr, urine creatinine concentration.

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    Table 1.

    Formula for fitted multiple logistic regression model for combining biomarkersa

    For AKI (n = 36) versus all non-AKI (n = 54) combined
        pre-OP[−0.9596 + 0.01386 × NAG + 0.3102 × KIM1 + 0.0006661 × NGAL]
        immediately post-OP[−2.0269 + 0.001718 × NAG + 0.7716 × KIM1 + 0.0001331 × NGAL]
        3 h post-OP[−2.0673 + 0.01182 × NAG + 1.0965 × KIM1 + 0.00009982 × NGAL]
        18 h post OP[−1.6097 + 0.03977 × NAG + 0.2894 × KIM1 + 0.0005103 × NGAL]
        24 h post-OP[−0.5933 + 0.007838 × NAG + 0.06978 × KIM1 + 0.0008006 × NGAL]
    For early AKI (n = 16) versus all non-AKI (n = 54) combined
        pre-OP[−2.0360 − 0.0005436 × NAG + 0.5281 × KIM1 + 0.0008857 × NGAL]
        immediately post-OP[−3.3182 + 0.00212 × NAG + 1.088 × KIM1 + 0.00009552 × NGAL]
        3 h post-OP[−3.4557 + 0.01294 × NAG + 1.4386 × KIM1 + 0.0001215 × NGAL]
        18 h post-OP[−3.8619 + 0.06381 × NAG + 0.5328 × KIM1 + 0.0008294 × NGAL]
        24 h post-OP[−2.2619 − 0.01722 × NAG + 0.2097 × KIM1 + 0.0007784 × NGAL]
    For late AKI (n = 20) versus all non-AKI (n = 54) combined
        pre-OP[−1.3241 + 0.01832 × NAG + 0.1329 × KIM1 + 0.0003802 × NGAL]
        immediately post-OP[−2.4918 + 0.002208 × NAG + 0.6224 × KIM1 + 0.0001534 × NGAL]
        3 h post-OP[−2.4066 + 0.01427 × NAG + 0.977 × KIM1 + 0.00006504 × NGAL]
        18 h post-OP[−1.3878 + 0.03679 × NAG + 0.08044 × KIM1 + 0.00009971 × NGAL]
        24 h post-OP[−0.5948 − 0.0148 × NAG - 0.2848 × KIM1 + 0.0008516 × NGAL]
    • ↵a AKI, acute kidney injury; OP, open-heart operation; KIM-1, kidney injury molecule-1; NAG, N-acetyl-β-D-glucosaminidase; NGAL, neutrophil gelatinase associated lipocalin.

    • View popup
    Table 2A.

    Stability of urinary biomarkersa

    Collection and ProcessingMean Percentage Difference (95% confidence interval of mean % difference) when Compared to Immediate Storage at −80°C
    KIM-1, n = 6NAG, n = 6NGAL, n = 6
    Remain at RMb for 2 h, then storage at −80°C−0.26 (−5.52 to 5.01)0.05 (−3.09 to 3.20)−2.45 (−6.54 to 1.64)
    Remain at RM for 4 h, then storage at −80°C1.43 (−5.39 to 8.25)0.48 (−3.19 to 4.15)−5.3 (−14.89 to 4.30)
    Remain at RM for 6 h, then storage at −80°C−3.97 (−10.80 to 2.86)0.48 (−2.42 to 3.38)2.54 (−7.86 to 12.93)
    Remain at RM for 24 h, then storage at −80°C−6.52 (−11.73 to −1.30)−0.43 (−1.46 to 0.60)−9.78 (−22.55 to 3.00)
    Remain at 4°C for 2 h, then storage at −80°C1.25 (−4.98 to 7.48)0.04 (−4.10 to 4.17)−3.97 (−9.91 to 3.77)
    Remain at 4°C for 4 h, then storage at −80°C0.43 (−5.37 to 6.23)2.38 (−1.75 to 6.51)6.65 (0.46 to 12.84)
    Remain at 4°C for 6 h, then storage at −80°C0.16 (−5.61 to 5.92)2.07 (−0.69 to 4.83)−5.19 (−13.47 to 3.09)
    Remain at 4°C for 24 h, then storage at −80°C−2.33 (−7.94 to 3.27)2.26 (−1.90 to 6.42)−1.01 (−14.52 to 12.5)
    Protease inhibitor versus no protease inhibitor1.23 (−3.76 to 6.23)−0.21 (−4.53 to 4.11)−1.51 (−7.23 to 4.20)
    Prolonged storage at −80°C
        1 yr with 3 repeat freeze and thaw cycles−0.53 (−8.57 to 7.50)4.96 (1.51 to 8.41)−2.43 (−13.53 to 8.66)
        2 yr with 3 repeat freeze and thaw cyclesNA2.13 (−4.47 to 8.72)NA
    • ↵a Immediate storage at −80°C and place urine samples at −80°C within first 20 min after initial collection.

    • ↵b RM, room temperature; NA, not applicable.

    • View popup
    Table 2B.

    Stability of urinary biomarkers at prolonged storage at −20°C

    Collection and ProcessingMean Percentage Difference (95% confidence interval of mean % difference)
    KIM-1, n = 32NAG, n = 32NGAL, n = 32
    Prolonged storage at −20 and −80°C
        2 yr with 3 repeat freeze and thaw cycles (−20 versus −80°C)−15.08 (−21.26 to −8.91)−8.88 (−16.03 to −1.74)−40.24 (−52.67 to −27.82)
        compared with initial biomarker levels 2 yr before at −20°C−6.75 (−16.99 to 3.49)−6.11 (−14.44 to 2.22)NA
    • View popup
    Table 3.

    Patient's characteristic and clinical outcomea

    CharacteristicAKI (n = 36)Early AKIb (n = 16)Late AKI (n = 20)Non-AKI (n = 54)
    Age (yr)68.31 ± 2.3065.41 ± 4.1670.64 ± 2.4560.39 ± 1.98
    Gender (male/female)23/139/714/638/16
    Scr (mg/dl)
        baseline (pre-OP)1.06 ± 0.061.10 ± 0.111.02 ± 0.051.02 ± 0.04
        post-OP (immediately)0.99 ± 0.05d1.09 ± 0.10d0.93 ± 0.050.84 ± 0.04
        post-OP day 11.28 ± 0.08c1.59 ± 0.13ce1.04 ± 0.050.91 ± 0.04
        post-OP day 21.51 ± 0.10c1.66 ± 0.19c1.40 ± 0.08c0.92 ± 0.04
        post-OP day 31.52 ± 0.11c1.55 ± 0.21c1.50 ± 0.10c0.91 ± 0.05
        post-OP day 41.54 ± 0.14c1.50 ± 0.21c1.57 ± 0.21c0.93 ± 0.05
        post-OP day 51.57 ± 0.19c1.39 ± 0.21d1.76 ± 0.32c0.92 ± 0.06
    Delta Scr change (%)
        post-OP (immediately)−7.94 ± 2.60d−5.71 ± 4.41d−9.50 ± 3.20d−17.41 ± 2.07
        post-OP day 122.78 ± 4.95c49.38 ± 4.70ce1.50 ± 3.72d−10.37 ± 2.27
        post-OP day 245.83 ± 5.54c56.25 ± 10.04c37.50 ± 5.47c−11.30 ± 2.48
        post-OP day 344.24 ± 6.51c44.67 ± 10.59c43.89 ± 8.33c−11.60 ± 3.11
        post-OP day 446.56 ± 11.06c40.00 ± 10.69c52.35 ± 18.80c−15.20 ± 4.09
        post-OP day 548.89 ± 15.69c31.43 ± 10.73c67.69 ± 30.28c−14.58 ± 4.26
    Mean duration of AKI (days)3.31 ± 0.404.13 ± 0.642.65 ± 0.46NA
    Type of heart operation
        CABG-CPB63311
        OPCABG4317
        single valve104618
        multiple valve1011
        CABG + valve11384
        aneurysm (or aneurysm + valve)1107
        other3216
    Intraoperative
        number of patients with CPB31 (86%)12 (75%)19 (95%)47 (87%)
        CPB (min)147.1 ± 11.6d151.7 ± 21.1d144.3 ± 13.9d113.9 ± 6.7
        aortic cross clamp time (min)92.2 ± 6.3100.4 ± 12.686.8 ± 6.479.6 ± 5.0
    Postoperative
        ICU-free days within 30 d23.7 ± 1.4c21.3 ± 2.7c25.6 ± 1.2d27.8 ± 0.3
        hospital-free days within 30 d15.5 ± 1.6c14.2 ± 2.5c16.6 ± 2.0d21.5 ± 0.9
        renal replacement therapy1100
        mortality5320
    • ↵a Values are means (±SEM).

    • ↵b Early AKI, development of AKI within first 24 h after operation; Late AKI, development of AKI between 24 and 72 h after operation; CPB, cardiopulmonary bypass; CABG-CPB, coronary artery bypass grafting with CPG; OPCABG, off-pump coronary artery bypass grafting; ICU, intensive care unit; Scr, serum creatinine concentration; Delta Scr change, % change in Scr from baseline.

    • ↵c P < 0.005 versus non-AKI.

    • ↵d P < 0.05 versus non-AKI.

    • ↵e P < 0.005 versus late AKI.

    • View popup
    Table 4.

    Comparison of various normalized urinary marker levels in patients with AKI and non-AKIa

    Pre-OPImmediately Post-OP3 h Post-OP18 h Post-OP24 h Post-OP
    Normalized KIM-1 (ng/mg Ucr)b
        AKI1.1 (0.7 to 1.4) (n = 36)1.4 (0.1 to 2.4)c (n = 35)0.7 (0.0 to 2.1)d (n = 28)2.6 (1.2 to 4.0) (n = 34)2.1 (1.4 to 3.9) (n = 34)
        early AKI1.3 (0.8 to 1.7)d (n = 16)2.5 (0.2 to 4.5)cf (n = 15)1.5 (0.0 to 3.6)d (n = 12)4.3 (1.1 to 8.2)d (n = 15)4.2 (1.5 to 10.2)de (n = 15)
        late AKI0.8 (0.5 to 1.4) (n = 20)0.5 (0.0 to 2.0) (n = 20)0.4 (0.0 to 1.5) (n = 16)2.5 (1.1 to 3.3) (n = 19)1.6 (1.1 to 2.2) (n = 19)
        non-AKI0.8 (0.6 to 1.0) (n = 54)0.0 (0.0 to 0.6) (n = 54)0.0 (0.0 to 0.3) (n = 51)1.7 (1.3 to 2.7) (n = 48)1.7 (1.0 to 2.7) (n = 42)
    Normalized NAG (U/gram Ucr)
        AKI4.7 (2.7 to 9.6) (n = 36)47.9 (28.5 to 93.9) (n = 35)19.8 (6.1 to 27.9) (n = 28)6.4 (5.3 to 9.2)d (n = 34)7.6 (4.4 to 13.9) (n = 34)
        early AKI7.6 (1.0 to 16.3) (n = 16)37.8 (18.0 to 132.3) (n = 15)20.9 (3.7 to 43.6) (n = 12)7.7 (5.1 to 12.5) (n = 15)7.3 (3.6 to 22.5) (n = 15)
        late AKI4.3 (2.4 to 9.6) (n = 20)51.9 (26.2 to 168.8) (n = 20)17.7 (5.3 to 97.8) (n = 16)5.6 (5.2 to 10.7) (n = 19)8.0 (3.5 to 13.9) (n = 19)
        non-AKI4.2 (2.1 to 5.6) (n = 54)24.9 (14.5 to 55.6) (n = 54)9.2 (5.5 to 16.5) (n = 51)4.0 (3.2 to 7.2) (n = 48)7.5 (4.7 to 10.2) (n = 42)
    Normalized NGAL (ng/mg Ucr)
        AKI6.1 (2.8 to 12.0) (n = 36)4579.0 (1544.8 to 8074.2) (n = 35)2071.4 (455.4 to 6211.0)d (n = 28)71.2 (31.7 to 255.6)c (n = 34)69.6 (9.9 to 323.1) (n = 34)
        early AKI9.5 (1.4 to 85.1) (n = 16)2044.1 (36.0 to 7247.3) (n = 15)1153.3 (1.1 to 8000.0) (n = 12)70.8 (6.4 to 1418.2)d (n = 15)73.3 (8.0 to 4752.1) (n = 13)
        late AKI5.4 (2.4 to 13.1) (n = 20)7151.1 (1704.2 to 9810.8)d (n = 20)3041.7 (324.5 to 7457.0)d (n = 16)75.6 (26.5 to 251.9)d (n = 19)70.1 (9.1 to 621.6) (n = 19)
        non-AKI3.8 (2.9 to 6.7) (n = 54)2308.5 (344.1 to 5044.8) (n = 54)130.6 (35.9 to 601.9) (n = 51)15.8 (9.0 to 22.0) (n = 48)20.9 (13.8 to 31.6) (n = 42)
    Delta Scr (%)
        AKI−10.00 (−10.00 to 0.00)d (n = 34)−20.00 (10.00 to 31.45)c (n = 36)
        early AKI0.00 (−20.00 to 7.60)d (n = 14)40.00 (30.00 to 70.00)c (n = 16)
        late AKI−10.00 (−20.00 to 0.00) (n = 20)5.00 (−10.00 to 15.50)d (n = 20)
        non-AKI−20.00 (−20.00 to −10.00) (n = 54)−10.00 (−20.00 to 0.00) (n = 54)
    • ↵a Values are medians (95% confidence interval for median).

    • ↵b Ucr, urine creatinine concentration.

    • ↵c P < 0.005 versus non-AKI.

    • ↵d P < 0.05 versus non-AKI.

    • ↵e P < 0.005 versus late AKI.

    • ↵f P < 0.05 versus late AKI.

    • View popup
    Table 5.

    Areas under the curve (AUCs) for normalized urinary biomarkers at various time pointsa

    Time after CPB
    Pre-OPImmediately After3 h18 h24 h
    AKI (n = 36)
        KIM-10.61 (0.51 to 0.72)0.68 (0.58 to 0.78)0.65 (0.54 to 0.75)0.60 (0.49 to 0.71)0.59 (0.47 to 0.70)
        NAG0.56 (0.46 to 0.67)0.61 (0.50 to 0.71)0.63 (0.51 to 0.73)0.64 (0.52 to 0.74)0.56 (0.44 to 0.67)
        NGAL0.55 (0.45 to 0.66)0.59 (0.48 to 0.69)0.65 (0.54 to 0.76)0.70 (0.59 to 0.80)0.59 (0.47 to 0.70)
        Combined0.63 (0.52 to 0.73)0.75 (0.65 to 0.84)b0.78 (0.68 to 0.87)c0.70 (0.58 to 0.79)0.68 (0.56 to 0.78)
        Delta Scr (%)0.67 (0.56 to 0.77)0.83 (0.74 to 0.90)
    Early AKI (n = 16)
        KIM-10.72 (0.60 to 0.82)0.79 (0.67 to 0.88)d0.73 (0.60 to 0.83)0.69 (0.56 to 0.80)0.71 (0.57 to 0.83)
        NAG0.58 (0.45 to 0.69)0.60 (0.47 to 0.71)0.59 (0.46 to 0.71)0.65 (0.52 to 0.77)0.54 (0.40 to 0.68)
        NGAL0.55 (0.42 to 0.67)0.51 (0.38 to 0.63)0.58 (0.45 to 0.70)0.68 (0.56 to 0.79)0.64 (0.50 to 0.77)
        Combined0.75 (0.63 to 0.85)0.80 (0.69 to 0.89)b0.84 (0.72 to 0.92)e0.83 (0.72 to 0.92)c0.78 (0.65 to 0.88)f
        Delta Scr (%)0.72 (0.60 to 0.82)1.00 (0.95 to 1.00)
    Late AKI (n = 20)
        KIM-10.54 (0.42 to 0.65)0.61 (0.49 to 0.72)0.60 (0.47 to 0.71)0.54 (0.41 to 0.66)0.54 (0.40 to 0.67)
        NAG0.55 (0.43 to 0.67)0.62 (0.51 to 0.74)0.65 (0.52 to 0.76)0.62 (0.50 to 0.74)0.54 (0.41 to 0.67)
        NGAL0.56 (0.44 to 0.67)0.66 (0.54 to 0.76)0.71 (0.59 to 0.82)0.72 (0.60 to 0.82)0.62 (0.48 to 0.74)
        Combined0.54 (0.42 to 0.66)0.72 (0.60 to 0.82)0.74 (0.62 to 0.84)0.59 (0.46 to 0.71)0.65 (0.52 to 0.77)
        Delta Scr (%)0.64 (0.52 to 0.75)0.70 (0.58 to 0.80)
    • ↵a Values are AUC (95% confidence interval for AUC).

    • ↵b P < 0.05 versus NGAL, NAG.

    • ↵c P < 0.05 versus KIM-1, NAG.

    • ↵d P < 0.05 versus NGAL.

    • ↵e P < 0.05 versus KIM-1, NAG, NGAL.

    • ↵f P < 0.05 versus NAG.

    • View popup
    Table 6.

    Performance of urinary KIM-1, NAG, and NGAL for diagnosis of AKI at various time points

    AKI (n = 36)SensitivitySpecificityPositive Likelihood RatioNegative Likelihood Ratio
    Urinary KIM-1 at Post Immediately
        >1.2 ng/mg Ucr51.4377.782.310.62
        >1.8 ng/mg Ucr42.8688.893.860.64
    Urinary KIM-1 at 3 h Post-OP
        >1.2 ng/mg Ucr35.7190.203.640.71
        >1.8 ng/mg Ucr32.1496.085.460.72
    Urinary NAG at Post Immediately
        >18.5 U/gram Ucr82.8644.441.490.39
        >25.0 U/gram Ucr74.2950.001.490.51
    Urinary NAG at 3 h Post-OP
        >18.5 U/gram Ucr53.5770.591.820.66
        >25.0 U/gram Ucr28.5780.391.460.89
    Urinary NGAL at Post Immediately
        >456.0 ng/mg Ucr71.4338.891.170.73
        >1900.0 ng/mg Ucr65.7150.001.310.69
    Urinary NGAL at 3 h Post-OP
        >456.0 ng/mg Ucr71.4362.751.920.46
        >1900.0 ng/mg Ucr50.0070.591.700.71
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Urinary Biomarkers in the Early Detection of Acute Kidney Injury after Cardiac Surgery
Won K. Han, Gebhard Wagener, Yanqing Zhu, Shuang Wang, H. Thomas Lee
CJASN May 2009, 4 (5) 873-882; DOI: 10.2215/CJN.04810908

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Urinary Biomarkers in the Early Detection of Acute Kidney Injury after Cardiac Surgery
Won K. Han, Gebhard Wagener, Yanqing Zhu, Shuang Wang, H. Thomas Lee
CJASN May 2009, 4 (5) 873-882; DOI: 10.2215/CJN.04810908
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