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Clinical Research
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Calcification Propensity and Survival among Renal Transplant Recipients

Charlotte A. Keyzer, Martin H. de Borst, Else van den Berg, Willi Jahnen-Dechent, Spyridon Arampatzis, Stefan Farese, Ivo P. Bergmann, Jürgen Floege, Gerjan Navis, Stephan J.L. Bakker, Harry van Goor, Ute Eisenberger and Andreas Pasch
JASN January 2016, 27 (1) 239-248; DOI: https://doi.org/10.1681/ASN.2014070670
Charlotte A. Keyzer
*Department of Internal Medicine, Division of Nephrology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
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Martin H. de Borst
*Department of Internal Medicine, Division of Nephrology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
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Else van den Berg
*Department of Internal Medicine, Division of Nephrology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
†Top Institute Food and Nutrition, Wageningen, The Netherlands;
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Willi Jahnen-Dechent
‡Helmholtz Institute for Biomedical Engineering, Biointerface Laboratory, Rheinisch-Westfälische Technische Hochschule, Aachen, Germany;
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Spyridon Arampatzis
§Department of Nephrology, Hypertension and Clinical Pharmacology, University Hospital Bern (Inselspital), Bern, Switzerland;
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Stefan Farese
‖Department of Nephrology, Bürgerspital Solothurn, Solothurn, Switzerland;
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Ivo P. Bergmann
¶Department of Internal Medicine, Emmental Hospital, Burgdorf, Switzerland;
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Jürgen Floege
**Department of Nephrology, Rheinisch-Westfälische Technische Hochschule University of Aachen, Aachen, Germany;
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Gerjan Navis
*Department of Internal Medicine, Division of Nephrology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
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Stephan J.L. Bakker
*Department of Internal Medicine, Division of Nephrology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
†Top Institute Food and Nutrition, Wageningen, The Netherlands;
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Harry van Goor
††Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands;
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Ute Eisenberger
‡‡Department of Nephrology, University Hospital Essen, University Duisburg-Essen, Essen, Germany; and
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Andreas Pasch
§§Department of Clinical Chemistry, University Hospital Bern (Inselspital), Bern, Switzerland
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    Figure 1.

    Kaplan–Meier curve for mortality and graft failure. (A) All-cause mortality, (B) cardiovascular mortality, and (C) death-censored graft failure among renal transplant recipients according to tertiles of baseline T50.

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    Figure 2.

    Forest plot of sub-analyses of serum T50 demonstrating that hazard ratios for all-cause mortality were consistent in different subgroups.

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    Figure 3.

    Comparative analysis of serum T50 with serum corrected calcium (Ca), phosphate (Pi), magnesium (Mg), parathyroid hormone (PTH) and calcium-phosphate (Ca×Pi) product, displayed per tertile as independent risk factors for all-cause mortality. Bars represent hazard ratio with 95% CI. (A) Crude analyses. (B) Adjustment for age, gender, eGFR, albuminuria, Framingham risk factors (systolic BP, body mass index, smoking, diabetes mellitus and LDL cholesterol), high-sensitivity C-reactive protein (hsCRP), calcineurin inhibitor use, dialysis vintage and type of donor (living versus deceased). Tertile with the lowest risk on mortality served as reference group (R).

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    Table 1.

    Baseline patient characteristics of the study population presented as tertiles of serum T50 in stable renal transplants

    CharacteristicsRenal transplant recipients Tertiles of T50
    Overall n=699Tertile 1 n=231Tertile 2 n=233Tertile 3 n=235P Value
    T50 (minutes)286±62<262262–311      >311<0.001a
    Demographics
     Age, years53.0±12.853.6±12.753.6±13.051.9±12.60.26
     Male gender, n (%)398 (57)135 (58)128 (55)135 (57)0.73
     Current smoker, n (%)84 (13)31 (15)25 (11)28 (13)0.62
     Current diabetes, n (%)170 (24)62 (27)63 (27)45 (19)0.08
     BMI, kg/m226.7±4.826.9±5.126.8±4.626.2±4.60.27
     Systolic BP, mmHg135.9±17.4136.6±17.9136.0±16.6135.1±17.60.66
     Diastolic BP, mmHg82.5±10.982.7±10.982.5±10.282.4±11.70.95
     Heart rate, bpm68.6±11.969.2±13.068.8±11.667.9±11.10.49
    Renal Transplantation
     Transplant vintage, years5.4 [1.9–12.1]6.1 [1.7–12.8]5.3 [2.0–12.3]5.2 [1.8–10.1]0.54
     Living donor, n (%)236 (34)61 (27)77 (34)98 (42)0.002a
     Pre-emptive transplant, n (%)105 (15)28 (12)35 (15)42 (18)0.22
     Dialysis vintage, months27 [9–52]29 [10–55]25 [10–48]25 [8–51]0.22
     HLA mismatches, n2 [1–3]2 [1–3]2 [1–3]2 [1–3]0.50
     Age donor, years42.8±15.641.2±16.243.2±15.343.8±15.20.19
     Acute rejection, n (%)186 (27)69 (30)67 (29)50 (21)0.07
    Laboratory measurements
     Hemoglobin, mmol/L8.2±1.18.0±1.18.3±1.18.4±1.0<0.001a
     HbA1c, %6.00±0.836.02±0.886.08±0.895.85±0.690.01a
     eGFR, CKD-EPI (mL/min per 1.73 m2)52.4±20.246.6±20.353.3±19.356.7±19.5<0.001a
     Corrected calcium, mmol/L2.41±0.152.37±0.142.40±0.142.45±0.15<0.001a
     Phosphate, mmol/L0.96±0.211.07±0.240.95±0.170.87±0.18<0.001a
     Magnesium, mmol/L0.95±0.120.93±0.130.95±0.110.98±0.11<0.001a
     PTH, pmol/L9.0 [5.9–14.7]8.7 [5.2–15.9]9.1 [6.2–14.4]9.1 [6.3–14.1]0.48
     Venous pH7.37±0.047.36±0.057.37±0.047.37±0.04<0.001a
     Venous HCO3–, mmol/L24.6±3.123.6±3.624.5±2.625.8±2.6<0.001a
     hsCRP, mg/L1.6 [0.7–4.6]1.9 [0.8–6.2]1.5 [0.8–4.4]1.4 [0.6–3.5]0.01a
     Albumin, g/L43.0±3.042.1±3.142.8±2.744.0±2.8<0.001a
     Alkaline phosphatase, U/L67 [54–83]67 [53–84]69 [55–83]66 [51–83]0.21
     Total cholesterol, mmol/L5.0 [4.4–5.8]4.9 [4.2–5.9]4.9 [4.3–5.6]5.2 [4.5–5.8]0.03a
     HDL cholesterol, mmol/L1.3 [1.1–1.6]1.3 [1.1–1.6]1.3 [1.0–1.6]1.3 [1.1–1.7]0.09
     LDL cholesterol mmol/L2.9 [2.3–3.5]2.8 [2.2–3.6]2.9 [2.3–3.4]2.9 [2.5–3.6]0.08
     Triglycerides, mmol/L1.68 [1.25–2.30]1.71 [1.24–2.47]1.67 [1.25–2.23]1.66 [1.24–2.24]0.65
     Albuminuria, mg/24 h40 [11–182]82 [16–300]36 [9–133]25 [9–112]<0.001a
    Medication
     Antihypertensives, n (%)616 (88)211 (91)202 (87)203 (86)0.18
     Statins, n (%)371 (53)135 (58)125 (54)111 (47)0.05a
     Calcium supplements, n (%)150 (21)72 (31)47 (20)31 (13)<0.001a
     Vitamin D supplements, n (%)171 (24)73 (32)45 (19)53 (23)0.006a
     Vitamin K antagonists, n (%)78 (11)37 (16)20 (9)21 (9)0.02a
     Prednisone, mg/d10 [7.5–10]10 [7.5–10]10 [7.5–10]10 [7.5–10]0.17
     Calcineurin inhibitors, n (%)400 (57)153 (66)133 (57)114 (49)0.001a
     Proliferation inhibitors, n (%)584 (84)182 (79)202 (87)200 (85)0.05
     Sirolimus, n (%)13 (2)3 (1)4 (2)6 (3)0.69
    • ↵a Differences were tested by ANOVA or Kruskal–Wallis test for continuous variables and with chi-squared test for categorical variables.

    • Data are represented as mean±SD or median [IQR]. BMI, body mass index; HbA1c, glycated hemoglobin; HCO3–, bicarbonate; hsCRP, high-sensitivity C-reactive protein.

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    Table 2.

    Associations of calcification propensity, serum T50, with all-cause mortality and cardiovascular mortality in stable renal transplant recipients

    HighIntermediateLowSerum T50 continuous
    HR (95% CI)HR (95% CI)P (trend) ValueHR (95% CI) per SDP Value
    All-cause mortality (nevents/ntotal=81/699)
    Model 1a1.0 (Ref)1.91 (0.99–3.70)4.09 (2.23 to 7.49)<0.0011.69 (1.37 to 2.09)<0.001
    Model 2b1.0 (Ref)1.77 (0.91–3.42)3.77 (2.06 to 6.91)<0.0011.69 (1.36 to 2.09)<0.001
    Model 3c1.0 (Ref)1.77 (0.90–3.49)3.54 (1.88 to 6.65)<0.0011.57 (1.26 to 1.97)<0.001
    Model 4d1.0 (Ref)2.03 (0.98–4.19)3.50 (1.74 to 7.01)<0.0011.56 (1.23 to 2.00)<0.001
    Model 5e1.0 (Ref)1.58 (0.76–3.32)2.86 (1.41 to 5.80)0.0021.43 (1.11 to 1.85)0.006
    Cardiovascular mortality (nevents/ntotal=38/699)
    Model 1a1.0 (Ref)3.25 (0.88–12.02)7.18 (2.09 to 24.72)0.0011.70 (1.19 to 2.43)0.003
    Model 2b1.0 (Ref)3.12 (0.84–11.55)6.82 (1.98 to 23.50)0.0011.71 (1.18 to 2.46)0.004
    Model 3c1.0 (Ref)3.02 (0.82–11.19)6.12 (1.75 to 21.44)0.0021.61 (1.10 to 2.36)0.01
    Model 4d1.0 (Ref)2.75 (0.74–10.30)6.07 (1.72 to 21.44)0.0021.59 (1.08 to 2.35)0.02
    Model 5e1.0 (Ref)2.63 (0.70–9.92)5.58 (1.58 to 19.72)0.0031.55 (1.04 to 2.29)0.03
    • Data are presented as hazard ratio (HR) plus 95% CI according to tertiles of serum T50 and per SD serum T50 decrease. Mean±SD, T50: 286±62 minutes.

    • ↵a Model 1: crude.

    • ↵b Model 2: adjusted for age and gender.

    • ↵c Model 3: adjusted for model 2 plus eGFR (CKD-EPI) and albuminuria.

    • ↵d Model 4: adjusted for model 3 plus current smoking, body mass index, diabetes mellitus, systolic BP and LDL cholesterol.

    • ↵e Model 5: adjusted for model 4 plus high-sensitivity C-reactive protein, calcineurin inhibitor use, dialysis vintage and type of kidney transplant (living versus deceased donor).

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    Table 3.

    Net reclassification improvement based on serum T50

    Without serum T50aWith serum T50
    <5%5%–10%>10%Total (n)
    Patients with all-cause mortalityb,c
     <5%44d8
     5%–10%94d13
     >10%3e5760
     Total4166181
    Patients without all-cause mortalityb,c
     <5%17617e193
     5%–10%43d9022e155
     >10%3d40d225268
     Total222147247616
    • ↵a Multivariable model including recipient age and gender and eGFR (CKD-EPI).

    • b Net reclassification improvement was 14%, P=0.002.

    • c 697 RTR were included in this analysis.

    • ↵d Numbers of patients who were correctly reclassified by the model with serum T50.

    • ↵e Numbers of patients who were incorrectly reclassified by the model with serum T50.

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Calcification Propensity and Survival among Renal Transplant Recipients
Charlotte A. Keyzer, Martin H. de Borst, Else van den Berg, Willi Jahnen-Dechent, Spyridon Arampatzis, Stefan Farese, Ivo P. Bergmann, Jürgen Floege, Gerjan Navis, Stephan J.L. Bakker, Harry van Goor, Ute Eisenberger, Andreas Pasch
JASN Jan 2016, 27 (1) 239-248; DOI: 10.1681/ASN.2014070670

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Calcification Propensity and Survival among Renal Transplant Recipients
Charlotte A. Keyzer, Martin H. de Borst, Else van den Berg, Willi Jahnen-Dechent, Spyridon Arampatzis, Stefan Farese, Ivo P. Bergmann, Jürgen Floege, Gerjan Navis, Stephan J.L. Bakker, Harry van Goor, Ute Eisenberger, Andreas Pasch
JASN Jan 2016, 27 (1) 239-248; DOI: 10.1681/ASN.2014070670
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Keywords

  • renal transplantation
  • mortality risk
  • graft failure
  • calcification propensity
  • serum T50
  • calciprotein particles

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