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Original ArticleMineral Metabolism
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Serum Phosphate and Microvascular Function in a Population-Based Cohort

Charles Ginsberg, Alfons J.H.M. Houben, Rakesh Malhotra, Tos T.J.M. Berendschot, Pieter C. Dagnelie, Jeroen P. Kooman, Caroll A. Webers, Coen D.A. Stehouwer and Joachim H. Ix
CJASN September 2019, CJN.02610319; DOI: https://doi.org/10.2215/CJN.02610319
Charles Ginsberg
1Nephrology Section, Veterans Affairs San Diego Healthcare System, San Diego, California;
2Division of Nephrology-Hypertension, University of California San Diego, San Diego, California;
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  • ORCID record for Charles Ginsberg
Alfons J.H.M. Houben
3Department of Internal Medicine and
4CARIM School for Cardiovascular Diseases and
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Rakesh Malhotra
1Nephrology Section, Veterans Affairs San Diego Healthcare System, San Diego, California;
5Imperial Valley Family Care Medical Group, El Centro, California
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Tos T.J.M. Berendschot
6University Eye Clinic Maastricht, Maastricht University Medical Center+, Maastricht, The Netherlands;
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Pieter C. Dagnelie
3Department of Internal Medicine and
4CARIM School for Cardiovascular Diseases and
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Jeroen P. Kooman
3Department of Internal Medicine and
7NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, The Netherlands; and
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Caroll A. Webers
6University Eye Clinic Maastricht, Maastricht University Medical Center+, Maastricht, The Netherlands;
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Coen D.A. Stehouwer
3Department of Internal Medicine and
4CARIM School for Cardiovascular Diseases and
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Joachim H. Ix
1Nephrology Section, Veterans Affairs San Diego Healthcare System, San Diego, California;
2Division of Nephrology-Hypertension, University of California San Diego, San Diego, California;
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    Figure 1.

    Maastricht population for each microvascular end point. BMI, body mass index; LDF, laser-Doppler flowmetry.

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    Figure 2.

    Percentage capillary recruitment during postocclusive reactive hyperemia is lower at higher phosphate quartiles. Phosphate quartile ranges were (Q1) 1.6–2.8 mg/dl, (Q2) 2.9–3.2 mg/dl, (Q3) 3.2–3.6 mg/dl, and (Q4) 3.6–5.2 mg/dl. Values presented are adjusted for age, sex, smoking status, 24-hour ambulatory systolic BP, use of antihypertensives, use of lipid modifying agents, diabetes status, eGFR, and serum calcium.

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    Table 1.

    Baseline characteristics of participants by serum phosphate quartiles

    CharacteristicsPhosphate Quartiles (Range)
    Q1 (1.6–2.8 mg/dl)Q2 (2.9–3.2 mg/dl)Q3 (3.2–3.6 mg/dl)Q4 (3.6–5.2 mg/dl)
    n=809n=855n=781n=744
    Age (yr [±SD])60 (9)60 (8)60 (8)59 (8)
    Male (n [%])644 (80)549 (64)307(39)159 (21)
    BMI (kg/m2 [±SD])28 (4.2)27 (4.3)27 (4.5)26 (5.1)
    Smoking (n [%])
     Never283 (35)297 (36)260 (34)226 (31)
     Former433 (54)429 (51)394 (51)375 (52)
     Current82 (10)110 (13)118 (15)123 (17)
    Diabetes status (n [%])a
     Normal424 (52)462 (54)453 (58)438 (59)
     Prediabetes152 (19)119 (14)104 (13)92 (12)
     Type 2 diabetes233 (29)274 (32)224 (29)214 (29)
    HbA1C (% [±SD])5.9 (0.9)5.9 (0.9)5.9 (0.9)6.0 (1.0)
    Retinopathy (n [%])10 (1)12 (2)12 (2)16 (2)
    Cardiovascular disease (n [%])117 (15)145 (17)131 (17)118 (17)
    BP (mm Hg [±SD])
     Office systolic BP139 (17)136 (18)134 (18)130 (18)
     Office diastolic BP 79 (10)76 (10)75 (10)74 (10)
     24-h systolic BP 122 (11)120 (12)118 (12)116 (11)
     24-h diastolic BP 76 (7)74 (7)73 (7)72 (7)
    BP medication (n [%])331 (41)380 (45)304 (39)270 (36)
    Hyperlipidemia medication (n [%])303 (37)337 (40)273 (35)257 (35)
    eGFR (ml/min per 1.73 m2 [±SD])81 (18)82 (17)81 (16)80 (17)
    CKD stage (n [%])
     None (eGFR >60 ml/min per 1.73 m2)760 (94)782 (91)722 (92)695 (93)
     CKD stage 3a45 (6)63 (7)54 (7)39 (5)
     CKD stage 3b4 (0.5)10 (1)5 (1)8 (1)
     CKD stage 40 (0)0 (0)0 (0)2 (0.3)
    Urine albumin/creatinine ratio (mg/g [±IQR])4 (2–8)5 (3–9)5 (3–10)5 (2–8)
    Calcium (mg/dl [±SD])9.3 (0.4)9.3 (0.3)9.4 (0.3)9.4 (0.3)
    • The upper range of Q2 was 3.19, the lower range of Q3 was 3.22, the upper range of Q3 was 3.56, and the lower range of Q4 was 3.60.

    • BMI, body mass index; HbA1C, hemoglobin A1c; IQR, interquartile range.

    • ↵a Glucose metabolism status was assessed by an oral glucose tolerance test and defined according to the World Health Organization 2006 criteria as normal glucose metabolism, impaired fasting glucose, impaired glucose tolerance (combined as prediabetes), and type 2 diabetes mellitus.

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    Table 2.

    Association of phosphate with microvascular measurements

    Measurement Used (% [95% CI])Measurement Results per Phosphate Range QuartilePer 1 mg/dl Higher Serum PhosphatePa
    Q1 (1.6–2.8 mg/dl)Q2 (2.9–3.2 mg/dl)Q3 (3.2–3.6 mg/dl)Q4 (3.6–5.2 mg/dl)
    Capillary recruitment during postocclusive reactive hyperemia (n=659)
     Model 1Reference−7.1 (−13.3 to −0.8)−7.1 (−13.6 to −0.6)−8.7 (−15.9 to −1.6)−5.2 (−10.1 to −0.4)0.04
     Model 2Reference−6.6 (−12.8 to −0.3)−6.3 (−12.8 to 0.3)−8.4 (−15.6 to −1.1)−5.0(−10.0 to −0.1)0.04
    Capillary recruitment during venous congestion (n=659)
     Model 1Reference−5.6 (−12.3 to 1.0)−6.0 (−12.9 to 0.90)−8.1 (−15.7 to −0.5)−4.7 (−9.8 to 0.5)0.08
     Model 2Reference−5.2 (−11.7 to 1.6)−5.0 (−11.9 to 2.0)−7.9 (−15.6 to −0.1)−4.5 (−9.8 to 0.7)0.09
    Heat-induced skin hyperemic response (n=1306)
     Model 1Reference−132 (−242 to −22)−112 (−230 to 6)−120 (−249 to 8)−53 (−140 to 35)0.24
     Model 2Reference−117 (−226 to −7)−92 (−211 to 27)−81 (−211 to 415)−25 (−113 to 63)0.57
    Retinal arteriolar dilation (n=1834)
     Model 1Reference−0.18 (−0.53 to 0.18)−0.12 (−0.50 to 0.25)−0.21 (−0.61 to 0.20)−0.19 (−0.47 to 0.07)0.15
     Model 2Reference−0.11 (−0.46 to 0.24)−0.05 (−0.43 to 0.33)−0.09 (−0.50 to 0.32)−0.12 (−0.30 to 0.15)0.39
    Retinal venular dilation (n=1834)
     Model 1Reference−0.02 (−0.29 to 0.26)−0.25 (−0.54 to 0.05)−0.41 (−0.73 to −0.10)−0.26 (−0.47 to −0.05)0.01
     Model 2Reference0.03 (−0.24 to 0.31)−0.20 (−0.49 to 0.10)−0.35 (−0.66 to −0.03)−0.23 (−0.44 to −0.02)0.03
    • The upper range of Q2 was 3.19, the lower range of Q3 was 3.22, the upper range of Q3 was 3.56, and the lower range of Q4 was 3.60.

    • Model 1 adjusted for age and sex; model 2 additionally adjusted for body mass index, smoking status, 24-h ambulatory systolic BP, use of antihypertensives, use of lipid-modifying agents, glucose metabolism status, eGFR, and serum calcium.

    • ↵a P values reported for the continuous analysis.

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    Table 3.

    Association of serum phosphate with heat-induced skin hyperemic response, stratified by sex

    SexChange per 1 mg/dl Higher Phosphate (% [95% CI])aP ValueP Interaction
    Men−149 (−260 to −38)0.010.01
    Women88 (−55 to 230)0.23
    • ↵a Adjusted for age, sex, body mass index, smoking status, 24-h ambulatory systolic BP, use of antihypertensives, use of lipid-modifying agents, diabetes status, eGFR, and serum calcium.

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Serum Phosphate and Microvascular Function in a Population-Based Cohort
Charles Ginsberg, Alfons J.H.M. Houben, Rakesh Malhotra, Tos T.J.M. Berendschot, Pieter C. Dagnelie, Jeroen P. Kooman, Caroll A. Webers, Coen D.A. Stehouwer, Joachim H. Ix
CJASN Sep 2019, CJN.02610319; DOI: 10.2215/CJN.02610319

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Serum Phosphate and Microvascular Function in a Population-Based Cohort
Charles Ginsberg, Alfons J.H.M. Houben, Rakesh Malhotra, Tos T.J.M. Berendschot, Pieter C. Dagnelie, Jeroen P. Kooman, Caroll A. Webers, Coen D.A. Stehouwer, Joachim H. Ix
CJASN Sep 2019, CJN.02610319; DOI: 10.2215/CJN.02610319
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Keywords

  • endothelium
  • phosphate
  • microvascular dysfunction
  • capillaroscopy
  • laser-Doppler flowmetry
  • retinal microvessels
  • Humans
  • microscopic angioscopy
  • hyperemia
  • Cross-Sectional Studies
  • Reference Values
  • linear models
  • Dilatation
  • Hot Temperature
  • venules
  • arterioles
  • Capillaries
  • retinal vessels
  • phosphates
  • Cohort Studies
  • male
  • Female

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