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5 Epidemiology of Vitamin D Deficiency in End-Stage Chronic Kidney Disease

5 Epidemiology of Vitamin D Deficiency in End-Stage Chronic Kidney Disease

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Accelerated Mortality on Renal

Replacement (ArMORR),

prospective cohort of 10,044

incident HD patients, random

sample of 907 patients

Comprehensive Dialysis Study

(CDS), 1432 incident dialysis

patients, 192 of them with 25(OH)D

measurements, 90 % HD and 10 %

PD.



Cross-sectional study (2 dialysis

units) of 84 HD patients, no vitamin

D supplementation

25(OH)D measured at the end of

winter



Single-center cross-sectional study

of 104 HD patients, no vitamin D

supplementation



[66], USA,

2004–2005



[87], Argentina, year

NR



[88], Italy, year NR



[67], USA,

2005–2007



Study/Population/Number

Single-center clinical trial, 131 HD

patients included



Ref, Country, Year

[86], USA 2005



Mean age 53 years, 59 % men,

4 % with diabetic nephropathy,

mean duration on dialysis

8 years



Mean age 59 years, 57 % men,

33 % with “moderately fair

skin′, 15 % with diabetic

nephropathy, mean duration on

dialysis 3.4 years



Mean age 62 years, 52 % men,

27 % non-white, 60 % DM.



Mean age 64 years, 53 % men,

32 % black, 43 % with diabetic

nephropathy



Characteristics

Mean age 59 years, 37 % men,

90 % black, 41 % DM, mean

duration on dialysis 5.6 years



Mean ± SD:

32 ± 18.1 ng/mL

<15 ng/mL: 14.4 %

16–30 ng/mL: 36.5 %



Mean ± SD: 24.4 ng/

mL

15 ng/mL: 22.6 %

15–30 ng/mL: 53.5 %



25(OH)Da

Mean ± SD:

16.9 ± 8.5 ng/mL

<30 ng/mL: 92 %

<15 ng/mL: 51 %

Median (IQR): 18.2

(11.3–28.0)

<30 ng/mL: 79 %

<20 ng/mL: 57 %

<10 ng/mL: 20 %

Median: 12.6 ng/mL

15–30 ng/mL: 33 %

<15 ng/mL: 65 %

<20 ng/mL: 89 %



No association with age



Characteristics’ associated

with low vitamin D after

adjustment: younger age,

women, winter season, current

smoker, higher BMI, PD,

lower albumin

No association with race,

diabetes, or creatinine

Low sun exposure, high BMI,

and female sex (multivariable

analysis)



Risk factors for low vitamin D

No association with gender,

diabetic status or dialysis

duration

Crude association with race

Black race, female sex, winter

season, and hypoalbuminemia

(multivariable analysis using

20 ng/mL cutoff)



Table 2.6 Circulating vitamin D level or prevalence of low values in adult patients on hemodialysis (HD) or peritoneal dialysis (PD)



38

M. Metzger and B. Stengel



Prospective cohort study of 600 HD

patients from 7 HD centers. N = 600



Multicenter cross-sectional study of

273 PD patients from 20 centers

Single-center cross-sectional study

of 113 HD patients

25(OH)D measured at the end of

winter



[92], Greece and

Turkey

[93], Algeria, year

NR



ARNOS prospective cohort (24

dialysis centers in the Rhônes-Alpes

region), subset of 648 (of 1348) HD

prevalent patients with a 25(OH)D

measurement

PHOTO-GRAPH (French

Phosphorus and Calcium

Observatory), 130 centers across

country, 9,125 HD patients

NECOSAD, prospective cohort

study of incident dialysis patients,

762 patients (of 1,743) with blood

sample available 1 year after

inclusion, 64 % HD



[91], Romania, 2010



[20], Netherlands,

year



[90], France 2008



[89], France,

2005–2009



Median: 19 ng/mL

(range 1–68)



Mean age 39 years, 48 % men,

mean duration on dialysis

3.7 years



Mean age 62 years, 55 % men



In patients with and

without DM, median:

21 ng/mL and 15 ng/

mL

<12 ng/mL: 37 % and

24 %

<15 ng/mL: 92 %



Mean ± SD:

18.2 ± 11.0 ng/mL

≤10.0 ng/mL: 25.3 %

10–30 ng/mL: 61.5 %



Mean ± SD:

21.7 ± 20 ng/mL



Mean ± SD: 27 ± 18 ng/

mL

Median: 18 ng/

mL < 30 ng/mL: 73 %



Median age 56 years, 55 % men,

15 % DM, median duration on

dialysis 2.8 years



Mean age 68 years, 58 % men,

28 % DM, mean duration on

dialysis 3.2 years, 32 % with

native vitamin D

Mean age 59 years, 61 % men,

20 % DM



Mean age 67 years, 60 % men,

32 % DM, mean duration on

dialysis 5.2 years, 22 % with

vitamin D supplementation



(continued)



Diabetes and older age

(multivariable analysis)

NR



Characteristics associated with

vitamin D deficiency: older

age, DM, and coronary heart

disease



Crude association with

diabetes, female sex, and PD

No association with age,

albumin level, or BMI



Not associated with age

Other associations NR



NR



2

Epidemiology of Vitamin D Deficiency in Chronic Kidney Disease

39



Single-center cross-sectional study

of 242 ESRD patients treated by

HD (n = 150) or PD (n = 56) or not

on dialysis (n = 36), admitted for

kidney transplantation and not

treated with native vitamin D



[71], Australia,

2002–2005



Characteristics

Mean age 55 years, 51 % men,

100 % Asian, 24 % with diabetic

nephropathy, 30 % with DM,

mean duration on dialysis

2.2 years

Mean age 43 years, 61 % men,

88 % white and 6 % Asian, 36 %

with diabetic nephropathy

(mainly type 1), median time on

dialysis 1.9 years



Risk factors for low vitamin D

Diabetes, female sex, and low

residual GFR (multivariable

analysis)



25(OH)D level was

significantly higher in CKD

patients stage 1–4 than in HD

patients



No crude association between

eGFR and 25(OH)D in CKD

stage 1–4

However, HD patients were

significantly more VD

-deficient (<15 ng/mL) than

CKD stage 1–4 patients



Mean ± SD: 26.8 ± 13.6 Diabetes, female sex, and

<15 ng/mL: ~18 % (28 % patients on PD (multivariable

vs 12 % for patients with analysis)

vs without DM)



25(OH)Da

Median (IQR): 18.3

(14.4–24.3) ng/mL

<15 ng/mL: 30 %

15–30 ng/mL: 57 %



Clinical study including hemodialysis patients and non-end-stage chronic kidney disease CKD patients

Single-center cross-sectional study

Mean age 59.1 and 54.6 years,

Mean ± SD: 18.5 ± 11.2

[56], USA, year NR

of 43 CKD patients stage 1–4 and

37 % and 60 % men, 56 % and

and 10.7 ± 6.8 ng/mL in

103 HD patients, no vitamin D

85 % African American, 33 %

participants with CKD

prescription

and 39 % with diabetic

stage 1–4 and HD

nephropathy, in CKD stage 1–4 <15 ng/mL: 44 % and

and HD participants respectively 80 %

(mean duration on dialysis

3.8 years)

Single-center cross-sectional study, Mean age 59 years, 59 % men,

Mean ± SD: 25.7 ± 13.4

[70], USA,

2010–2011

58 HD patients vs 648 CKD

67 % black, 40 % DM, 4 years

vs 23.6 ± 15.5 ng/mL in

patients stage 1– 4

on HD (characteristics of CKD

CKD stage I–V vs HD

patients NR)

patients

In HD patients:

<30 ng/mL: 96.6 %

<20 ng/mL: 70.7 %

<10 ng/mL: 20.7 %



Study/Population/Number

Single-center longitudinal study of

230 patients receiving PD



Ref, Country, Year

[94], China, year NR



Table 2.6 (continued)



40

M. Metzger and B. Stengel



Single-center study, 203 CKD

patients stage 1–5D (simple random

sampling from one center)



[69], UK, 2007



CKD stage 2–5 days:

8 %,26 %,26 %,7 %,33 %, mean

age 67 years, 61 % men, 100 %

white, 42 % DM, 36 % vitamin

D supplementation

Median eGFR 32 mL/

min/1.73 m2 (CKD stage 1 to

5D: 6 %, 16 %, 33 %, 18 %, 9 %

and 18 %)

median age 64 years, 64 % men,

88 % white, 20 % DM

Median (IQR): 18

(13–36), by CKD

stages 1–5: 19 (15–22),

16 (12–20), 22

(16–29),15 (12–23), 17

(9–21),16 (11–25)

<20 ng/mL: 62 %



Mean ± SD: 20.5 ± 13.6

Median: 13.6

<15 ng/mL: 42 %



NR not reported, HD hemodialysis, PD peritoneal dialysis, eGFR estimated glomerular filtration rate, DM diabetes mellitus

a

Prevalence of low vitamin D status and/or mean ± SD, mean (95 % CI), median(IQR) level of 25(OH)D



Single-center longitudinal study,

140 patients with CKD stage 2–5

days



[68], France,

2006–2007



No crude association between

CKD stage and 25(OH)D



No crude association between

CKD stage and 25(OH)D



2

Epidemiology of Vitamin D Deficiency in Chronic Kidney Disease

41



42



M. Metzger and B. Stengel



Table 2.5), but their sample sizes were too small for multivariate analysis. Among

them, a single-center study including 103 patients on hemodialysis and 43 with

CKD stages 1–4 showed much lower vitamin D levels among the former, but the

two groups were not comparable for age, gender, or race [56].

Risk factors for vitamin D deficiency are similar among patients with end-stage

and non-end-stage CKD: winter season, race/ethnicity, older age, high BMI, and

diabetes (Table 2.5). In the US ArMORR cohort of incident dialysis patients, 57 %

of patients had 25(OH)D levels <20 ng/mL, but 100 % of black patients with hypoalbuminemia beginning dialysis in winter had 25(OH)D levels <20 ng/mL [66].

Peritoneal dialysis is likely to be an additional risk factor for vitamin D deficiency because of the potential loss of 25(OH)D through peritoneal fluid [35]. A

study of 192 incident dialysis patients, 10 % on peritoneal dialysis, showed that this

technique is associated with a 25(OH)D level 20 % lower than in patients on hemodialysis, independent of gender, age, race/ethnicity, body mass index, diabetes, and

season of the assay [67]. Other studies found similar overall differences between

peritoneal dialysis and hemodialysis [20, 68–71].

Relatively few studies have examined this question among patients living with a

kidney transplant (Table 2.7). These patients are usually advised to avoid sun exposure because their immunosuppressive treatments create a high risk of skin cancer.

In a British study comparing 31 kidney transplant patients with 31 age- and gendermatched controls without CKD, the median serum 25(OH)D level among the transplant patients was half that of the controls [72].



2.6



Discussion and Conclusions



This review shows that vitamin D deficiency is commonly observed both in CKD

patients and the general population. This finding is expected given the high frequency among these patients both of known risk factors for vitamin D deficiency,

such as old age, dark skin, and obesity, and of associated comorbidities, such as

diabetes. It is uncertain, however, whether the relation between 25(OH)D deficiency

and CKD is causal. Epidemiological studies currently provide sparse evidence

about the relation between kidney function or damage and circulating 25(OH)D

level.

Overall, findings from the general population and clinical studies are inconsistent.

Some studies report a significant, positive, and independent association between GFR

and 25(OH)D. One potential mechanism suggested to explain this association might

be that CKD diminishes the skin’s ability to convert 7-dehydrocholesterol into previtamin D3, but thus far this mechanism has been demonstrated only in hemodialysis

patients, compared with healthy controls [65]. Another potential mechanism, shown

in an experimental study using a uremic animal model [73], involves a reduction in

the rate at which the liver converts cholecalciferol into 25(OH)D, mediated by PTH

secretion. However, a few studies have also showed no or even an inverse association

between GFR and 25(OH)D, with paradoxically higher levels of 25(OH)D in



Single-center cross-sectional study,

31 kidney transplant outpatients

were matched with 31 dermatologic

patients without CKD according to

age and gender. Not treated with

vitamin D

Single-center study, 320 kidney

transplant recipients of whom 244

were not treated with vitamin D,

parathyroidectomy or corticosteroid

before transplantation



[72], Germany,

year NR



[97], United

Kingdom,

1999–2006



Single-center cross-sectional study

of 173 kidney transplant outpatients



Study/Population/Number

Single-center study, 129 kidney

transplant recipients at

2,3,5,8,12,18, and 24 months after

transplantation. Not treated with

vitamin D



[96], Denmark,

2005–2006



Ref, Country,

Year

[95], Germany,

1992–1993



Mean eGFR 45 mL/min/1.73 m2,

median age 46 years, 62 % men,

mainly white.



Median eGFR 38.9 mL/

min/1.73 m2. Mean age 53 years,

50 % men, 14 % diabetic

nephropathy, 9 % with dark skin,

median graft age 7.4 years.

Mean age 52 years, 55 % men,

mean graft age of 7 years



Population characteristics

Mean age 45.4 years, 59 % men



Geometric mean

(95 %CI): 10.9 (8.2–14.3)

ng/mL in kidney

transplant recipient vs

20.0 (15.7–25.5) ng/mL in

control group

<15 ng/mL: 58.2 %

15–30 ng/mL: 36.9 %



25(OH) vitamin Da

Mean ± SD: 14.1 ± 0.9 ng/

mL, 20.3 ± 1.3 and

23.7 ± 1.7 ng/mL,

respectively 3, 12 and

24 months after

transplantation.

Insufficiency (15–30 ng/

mL): 51 %

Deficiency (<15 ng/mL):

29 %



Table 2.7 Circulating vitamin D level or prevalence of low values in adult kidney transplant recipients



(continued)



No association with age

Other associations NR



NR



Older age, smoking, sun

avoidance, high serum

albumin, high BMI, low

daily intakes



Risk factors for low vitamin

D

Winter measurement

No association with renal

function

Other association NR



2

Epidemiology of Vitamin D Deficiency in Chronic Kidney Disease

43



Single-center study, 100 kidney

transplant recipients without any of

DM, impaired graft function and

vitamin D supplementation



Study/Population/Number

Single-center study, 509 kidney

transplant recipients, 378 of whom

were treated with vitamin D



52 % stage 1–2, 48 % stage 3a,

42 years, 62 % men, mean graft age

1.5 years



Population characteristics

Mean eGFR 47.0 mL/min/1.73 m2,

mean age 45.4 years, 58 % men,

mean graft age 9.4 years



<15 ng/mL: 12 %

15–30 ng/mL: 57 %



25(OH) vitamin Da

Mean ± SD:

20.0 ± 10.6 ng/mL

<15 ng/mL: 38.3 %

15–30 ng/mL: 46.9 %



NR not reported, eGFR Estimated glomerular filtration rate

a

Prevalence of low vitamin D status and/or mean ± SD, mean (95 % CI), median(IQR) level of 25(OH)D



[99], Brazil, year

NR



Ref, Country,

Year

[98], Spain, year

NR



Table 2.7 (continued)

Risk factors for low vitamin

D

No association with

supplementation

Women and winter

measurement (multivariate

analysis in untreated

participants)

Winter measurement and

high percentage of body fat

in multivariate analysis



44

M. Metzger and B. Stengel



2



Epidemiology of Vitamin D Deficiency in Chronic Kidney Disease



45



individuals with moderate CKD than in those without CKD [50–52]. In the NHANES

III study for example, the adjusted mean level of vitamin D did not differ between

participants with GFR >90 and 30–59 mL/min/1.73 m2, but it was significantly lower

in those with GFR <30 mL/min/1.73 m2 [17]. It is established that CKD patients have

increased serum FGF23 levels and potentially an increased vitamin D catabolism

through the stimulation of 24 hydroxylase activity; paradoxically, a reduced vitamin

D catabolism has been proposed to explain the nonlinear association between eGFR

and 25(OH)D observed in some studies [53]. Several recent studies have showed

lower levels of 24,25-dihydroxyvitamin D, the product of 25(OH)D catabolism, in

CKD patients, independent of circulating 25(OH)D level; they suggest that 24-hydroxylase regulation is impaired in patients with reduced kidney function [74–76].

Only a few epidemiological and clinical studies have examined the relations

between proteinuria or albuminuria and circulating 25(OH)D levels, and they report

significant negative associations [48, 50, 60, 63]. These findings tend to support the

hypothesis that subnephrotic levels of proteinuria are associated with low circulating

vitamin D levels [11]. Renal hydroxylation of 25(OH)D depends on the process of

filtration of the vitamin D-vitamin D binding protein complex in the glomerulus followed by its active reabsorption in the proximal tubule (see Chap. 1). This process

might be disturbed by increased albumin filtration and could increase vitamin D loss

in urine [64]. Nonetheless, recent clinical studies in children with CKD, which have

examined correlations between serum and urinary vitamin D binding protein, and

total serum 25(OH)D level [77, 78], appear to have ruled out this hypothesis.

Another possible reason for the cross-sectional association of vitamin D deficiency with GFR decline or kidney damage as assessed by albuminuria is that vitamin

D deficiency may be a cause rather than a consequence of CKD progression. Some

recent studies have indeed found 25(OH)D and/or 1,25(OH)2D to be significantly

associated with a decline in GFR and/or end-stage renal disease [22, 24, 25, 79],

although others failed to find any of these associations [23, 52, 80].

In conclusion, the questions about the relation between kidney damage or function and circulating 25(OH)D levels have yet to be resolved. Further investigations

are needed: they should include individuals with and without CKD; they should

measure GFR, albuminuria, and circulating level of total 25(OH)D longitudinally,

together with 1,25(OH)2D, 24,25(OH)2D, PTH and FGF-23; and they should collect

information about treatments and dietary, ecological and lifestyle risk factors for

vitamin D deficiency. A better understanding of when the impairment of the vitamin

D metabolism begins would help to establish evidence-based recommendations for

the measurement and treatment of vitamin D deficiency in the early stages of CKD.



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5 Epidemiology of Vitamin D Deficiency in End-Stage Chronic Kidney Disease

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