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Int Urol Nephrol (2010) 42:773–780 DOI 10.1007/s11255-009-9697-8

NEPHROLOGY - ORIGINAL PAPER

Vascular calcification score on plain radiographs of the feet as a predictor of peripheral arterial disease in patients with chronic kidney disease Won Suk An • Young Ki Son • Seong-Eun Kim • Ki-Hyun Kim • Seong Kuk Yoon • Hae-Rahn Bae Seo-Hee Rha



Received: 23 May 2009 / Accepted: 10 December 2009 / Published online: 30 December 2009 Ó Springer Science+Business Media, B.V. 2009

Abstract Background The incidence of lower extremity amputation is increasing in patients with chronic kidney disease (CKD), but symptoms of peripheral arterial disease (PAD) in patients with CKD are uncommon. The aim of the current study was to assess the value of the vascular calcification (VC) score on plain radiographs of the feet for the prediction of PAD in patients with CKD. Methods We recruited 102 patients with CKD (24 pre-dialysis, 58 hemodialysis [HD], and 20 peritoneal dialysis [PD]). We defined the VC score on the plain radiographs of the feet as follows: score 0, no calcification; score 1, the length of the VC is \5 cm in a single foot or\2 cm in both feet; and score 2, the length of the VC is[5 cm in a single foot or[2 cm in W. S. An (&)  Y. K. Son  S.-E. Kim  K.-H. Kim Department of Internal Medicine, Dong-A University, 3 Ga-1, Dongdaesin-Dong, Seo-Gu, Busan 601-715, Korea e-mail: [email protected] S. K. Yoon Department of Radiology, Dong-A University, Busan, Korea H.-R. Bae Department of Physiology, Dong-A University, Busan, Korea S.-H. Rha Department of Pathology, Dong-A University, Busan, Korea

both feet. We evaluated the atherosclerotic calcified plaques of the femoral or popliteal artery with Doppler ultrasonography and compared it with the VC score. Results Patients with high VC scores showed more atherosclerotic calcified plaques in the femoral or popliteal artery (P \ 0.01). The prevalence of PAD in patients with CKD was closely related with the VC score (P \ 0.01). PAD was associated with diabetes, a higher hsCRP, and a lower total cholesterol level (P \ 0.01). The VC score was a significant predictor of the presence of PAD (odds ratio: 6.66, P \ 0.001). Conclusions Asymptomatic CKD patients, including those on HD and PD, may have PAD and routine testing by plain radiographs of the feet followed by Doppler ultrasonography are of pivotal significance, especially if the patients are diabetic. Keywords Diabetes  Dialysis  Peripheral artery disease  Radiograph  Vascular calcification

Introduction Patients with chronic kidney disease (CKD) have a higher prevalence of cardiovascular diseases, including ischemic heart disease [1, 2]. Vascular calcifications (VCs) have been shown to be independent predictors of all-cause and cardiovascular mortality in patients with CKD [3]. Various VC scores have been evaluated in hemodialysis (HD) patients using

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B-mode ultrasonography [4, 5], electron beam computed tomography [6], and plain radiographic films of the pelvis and hands [7]. Medial artery calcifications have been differentiated from intimal calcifications by plain radiography in diabetic patients and have been associated with allcause and cardiovascular mortality [8]. Typical linear railroad calcifications that outline the vessel walls are considered to be medial artery calcification [3]. The presence of VCs in end-stage renal disease (ESRD) patients is associated with increased stiffness of the arteries [9]. The simple VC score of plain radiographic films of the pelvis and hands is independently associated with coronary artery disease (CAD) and peripheral arterial disease (PAD) at the end of follow-up [3]. The prevalence of PAD is high among patients with CKD and ESRD. Lower extremity amputation rates in ESRD patients are nearly 10-fold greater than in the general population [10, 11]. However, PAD of the lower limbs has received little attention. Many studies have demonstrated that ESRD is a risk factor for cardiovascular death, CAD, and cerebrovascular disease, but most studies have not examined the association of ESRD with PAD. Compared with reports on CAD, reports on lower extremity vascular disease in CKD patients and data on PAD among peritoneal dialysis (PD) patients in particular are rare [12]. Furthermore, most ESRD patients with PAD do not exhibit symptoms [11]. History and physical examinations are insensitive indicators of the presence of PAD [11, 13]. Therefore, a simple screening diagnostic test is essential in deciding whether further diagnosis and evaluation is necessary. The aim of our study was to assess the value of the VC score on plain radiographs of the feet for the prediction of PAD in CKD patients, including HD and PD patients.

Patients and methods Patients We recruited 58 HD patients (25 patients with diabetes mellitus; 33 patients without diabetes mellitus; duration of HD, 84.0 ± 60.2 months) from the Dong-A University Dialysis Center and a neighboring local dialysis center. Twenty PD patients (duration of PD, 20.0 ± 15.5 months) with diabetes mellitus and 24 pre-dialysis patients (CKD stages 3–5) with diabetic

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nephropathy were enrolled at Dong-A University. Inclusion criteria were CKD patients who were predialysis and maintained on HD or PD. Patients with a glomerular filtration rate of[60 ml/min/1.73 m2 were excluded. Informed consent was obtained in accordance with the guidelines set forth by the Declaration of Helsinki. We reviewed the medical histories and records by chart reviews and interviews. Patients with a history of lower extremity amputation for PAD or patients diagnosed with PAD with ulceration and necrosis of the foot were defined as having PAD. Enrolled HD patients received regular HD thrice weekly. Bicarbonate-based dialysate and polysulphone dialyzers (Fresenius, Bad Homburg, Germany) were used. PD patients received four exchanges per day using a standard regimen (8 L/day). Laboratory measurements Routine laboratory tests, such as hemoglobin, blood urea nitrogen (BUN), creatinine, albumin, calcium, phosphate, intact parathyroid hormone (iPTH), high sensitivity C-reactive protein (hs-CRP), and lipid levels were obtained using fasting blood samples. VC score and Doppler ultrasonography Standard radiographs of both feet were obtained to determine VC. AXIOM Aristos MX/VX (SIEMENS, Erlangen, Germany) radiographic equipment with a digital imaging system was used (exposure conditions, 45–50 kVp [4 mAs]). Calcifications outlining the dorsalis pedis artery on the plain radiographs were tipically presenting as ‘‘railroad-track’’ angiography-like lines or as rings (Fig. 1). One nephrologist and one radiologist measured the VCs of the dorsalis pedis arteries on plain radiographs of the feet, without access to other patient data. Consensus was reached on the interpretation of all radiographs. We defined the VC score of the plain radiographs of the feet, as follows: score 0, no calcification; score 1, length of VC \5 cm in a single foot or \2 cm in both feet; and score 2, length of VC [5 cm in a single foot or [2 cm in both feet. The length of the VC was measured with a ruler, focusing on the course of the dorsalis pedis artery. We randomly selected 28 of the 82 patients without PAD by using the table of random sampling (score 0, 10 patients; score 1, 8 patients; and score 2, 10

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Fig. 1 Standard radiograph of the right foot shows definite vascular calcification in the course of dorsalis pedis artery. (a) High density of ring-like form indicates vascular media calcification of dorsalis pedis artery (score 1). (b) Angiography-

like calcifications on the plain radiographs of the feet that outline the vessel walls are considered as medial artery calcifications (score 2)

patients) and evaluated the arteries of the lower limbs with color Doppler ultrasonography. Nine patients were also selected and evaluated to confirm PAD with color Doppler ultrasonography from the 20 patients with PAD. Both the popliteal and femoral arteries were carefully examined by one radiologist. The radiologist mentioned whether or not the atherosclerotic calcified plaques occluded the femoral or the popliteal artery by more than 30%. We chose the 30% cut-off value because on color Doppler ultrasonography levels above 30% indicate a partially obstructed artery. Femoral or popliteal artery occlusions [30% found by color Doppler ultrasonography were considered as diagnostic for PAD in patients without clinical evidence of PAD. The ankle brachial index (ABI) and the body mass index (BMI) were also determined in the enrolled patients.

method. We included variables for the linear logistic regression model, such as age, gender, smoking history, BMI, diabetes, ABI, and laboratory variables. Significant variables identified by univariate analysis were entered into a multiple logistic regression analysis to identify variables associated with the presence or absence of PAD and positive Doppler ultrasonography finding or VC score (VC score of 0 or 1 and VC score of 0 or 2). P values \0.05 were considered significant. All statistical calculations were performed with SPSS software, version 12.0 (SPSS Inc, Chicago, IL, USA).

Statistical Analysis

The VC data are summarized in Table 1. A ring-like appearance due to a medial artery calcification is frequently seen on standard radiographs of the feet in patients with VCs (Fig. 1a). VCs on plain radiographs of feet were more commonly found in diabetic patients than in non-diabetic patients. Patients with VCs had significantly higher hs-CRP levels than patients without VCs. Age, gender, calcium, phosphate, iPTH, serum albumin, lipid levels, smoking history, BMI, and ABI were not significantly different between groups with and without VCs. The

Data are presented as the mean ± SD, except for iPTH, which is expressed as the mean ± SE. Comparisons of unpaired data were performed using Student’s t-test for parametric data. The non-parametric Mann–Whitney U test was used if the value was not normally distributed. Comparisons of more than two sets of unmatched data were performed by one-way ANOVA using the Tukey test. We used a linear logistic regression model by a stepwise

Results Comparison of data according to VCs

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776 Table 1 Clinical and Biochemical characteristics in patients with or without vascular calcification

Data are expressed as mean ± SD; iPTH is expressed as mean ± SE BMI body mass index, DM diabetes mellitus, PAD peripheral artery disease, ABI ankle brachial index, iPTH intact parathyroid hormone, BUN blood urea nitrogen, HDL high density lipoprotein cholesterol, LDL low density lipoprotein cholesterol, hs-CRP high sensitivity C-reactive protein

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Calcification (-)

Calcification (?)

P-value

Number

51

51



Age (years)

56.6 ± 12.4

59.9 ± 8.5

0.119

Male/female

27/24

34/17

0.157

Smoking History

17/51(33%)

26/51(51%)

0.071

BMI (kg/m2)

21.5 ± 2.9

22.2 ± 3.2

0.295

DM

25/51(49%)

44/51(86%)

0.000

PAD

1/51(2%)

19/51(37%)

0.000

ABI Calcium (mg/dl)

1.07 ± 0.15 8.6 ± 1.1

1.07 ± 0.17 8.9 ± 1.1

0.908 0.134

Phosphate (mg/dl)

5.0 ± 1.6

4.7 ± 1.6

0.333

2

CaXP (mg/dl)

43.1 ± 14.9

42.2 ± 15.6

0.773

iPTH (pg/ml)

171.8 ± 28.3

130.1 ± 20.0

0.235

BUN (mg/dl)

70.9 ± 29.7

62. 6 ± 22.4

0.122

Creatinine (mg/dl)

8.5 ± 4.0

8.1 ± 3.5

0.605

Albumin (g/dl)

3.8 ± 0.5

3.7 ± 1.0

0.946

Total cholesterol (mg/dl)

176.8 ± 61.0

170.6 ± 47.2

0.576

Triglycerides (mg/dl)

151.7 ± 148.6

117.7 ± 65.6

0.245

HDL (mg/dl)

38.4 ± 12.0

35.1 ± 11.1

0.217

LDL (mg/dl)

94.9 ± 37.9

85.7 ± 31.1

0.278

hs-CRP (mg/dl)

0.44 ± 0.69

0.86 ± 1.12

0.040

prevalence of PAD was significantly higher in the group with VCs than in the group without VCs. All PAD patients had diabetes mellitus. Patients with PAD had significantly higher hs-CRP levels, lower total cholesterol, and lower LDL cholesterol than patients without PAD (Table 2). Ten percent of patients without VCs showed atherosclerotic calcified plaques occluding the femoral or popliteal artery by [30% by color Doppler ultrasonography findings. Seventy percent of patients with VCs had such findings, which was significantly higher compared to patients without VCs (Fig. 2a).

different according to the VC score. Color Doppler ultrasonography findings showing atherosclerotic calcified plaque occlusion of the femoral or popliteal artery by [30% were significantly higher in patients with a VC score of 2 than in patients with a VC score of 0 (P \ 0.001, Fig. 2b). A VC score of 0, 1, and 2 was found in 14, 9, and 1 patient, respectively, among pre-dialysis CKD patients (calculated GFR was 24.3 ± 14.5 ml/min/1.73 m2 [range: 9–59 ml/min/ 1.73 m2]). All nine patients with PAD had atherosclerotic calcified plaque occlusion of the femoral or popliteal artery by [30%.

Comparison of data according to the VC score

Logistic regression analysis results

The data are summarized in Table 3. VC scores of 1 and 2 were significantly more frequent than a VC score of 0 in the diabetic CKD patients (pre-dialysis, HD, and PD patients). In addition, patients with PAD and a VC score of 2 were significantly more frequent than a VC score of 0 or 1. Hs-CRP levels were higher among patients who had a VC score of 2 compared to patients with a VC score of 0. Age, gender, calcium, phosphate, iPTH, serum albumin, lipid levels, smoking history, BMI, and ABI were not significantly

Significant predictors detecting the presence of PAD were hs-CRP (odds ratio [OR], 3.67; 95% confidence interval [CI], 1.6–8.5; P = 0.003) and a VC score (OR, 6.66; 95% Cl, 2.3–19.4; P \ 0.001) in CKD patients (pre-dialysis, HD, and PD patients). A significant predictor in detecting the presence of a positive finding of color Doppler ultrasonography was a VC score (OR, 4.19; 95% Cl, 1.4–14.0; P = 0.013) in CKD patients. A significant predictor detecting atherosclerotic calcified plaque occlusion of

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Int Urol Nephrol (2010) 42:773–780 Table 2 Comparison of clinical and biochemical data according to peripheral artery disease

Data are expressed as mean ± S.D. iPTH is expressed as mean ± SE PAD peripheral artery disease, BMI body mass index, DM diabetes mellitus, ABI ankle brachial index, iPTH intact parathyroid hormone, BUN blood urea nitrogen, HDL high density lipoprotein cholesterol, LDL low density lipoprotein cholesterol, hs-CRP high sensitivity C-reactive protein

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PAD (-)

PAD (?)

P-value

Number

82

20



Age (years)

57.8 ± 11.5

59.8 ± 6.7

0.317

Male/female

48/34

13/7

0.597

Smoking History (%)

33/82 (40%)

10/20 (50%)

0.428

BMI (kg/m2)

21.5 ± 2.9

22.2 ± 3.2

0.586

DM

49/82 (60%)

20/20 (100%)

0.001

ABI

1.07 ± 0.15

1.07 ± 0.21

0.961

Calcium (mg/dl) Phosphate (mg/dl)

8.7 ± 1.0 4.8 ± 1.4

9.2 ± 1.4 5.0 ± 2.1

0.038 0.825

CaXP (mg/dl)2

41.9 ± 13.6

45.9 ± 20.4

0.411

iPTH (pg/ml)

153.8 ± 20.1

140.0 ± 33.9

0.762

BUN (mg/dl)

67.5 ± 27.6

63. 2 ± 21.1

0.457

Creatinine (mg/dl)

8.2 ± 4.0

9.0 ± 2.4

0.404

Albumin (g/dl)

3.7 ± 0.5

3.8 ± 1.5

0.936

Total cholesterol (mg/dl)

178.8 ± 57.4

151.4 ± 30.6

0.006

Triglycerides (mg/dl)

141.5 ± 124.6

84.4 ± 49.6

0.314

HDL (mg/dl)

37.6 ± 11.7

30.9 ± 9.8

0.145

LDL (mg/dl)

93.4 ± 35.5

63.8 ± 13.9

0.048

hs-CRP (mg/dl)

0.43 ± 0.60

1.61 ± 1.52

0.008

Fig. 2 (a) Comparison of Doppler ultrasonography findings between chronic kidney disease patients with and without vascular calcifications. Findings were significantly different. (b) Comparison of Doppler ultrasonography findings according to vascular calcification scores. Findings were significantly

different. \30%: atherosclerotic calcified plaques occluded the femoral or popliteal artery \30%; [30%: atherosclerotic calcified plaques occluded the femoral or popliteal artery [30%

the femoral or popliteal artery by [30% was a VC score on plain radiographs (OR, 6.51; 95% Cl, 1.7– 24.5; P = 0.006) in CKD patients. Diabetes mellitus was a significant independent factor forming a VC score of 1 (OR, 6.93; 95% Cl, 1.8–26.3; P = 0.004) and a VC score of 2 (OR, 6.24; 95% Cl; 1.9–20.6; P = 0.003) in CKD patients.

Discussion Even patients without symptomatic PAD had partial atherosclerotic calcified plaque occlusion of the femoral or popliteal artery [30% if they had VCs and 95% of PAD patients had VCs on plain radiographs of feet in our study. These results suggest

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Table 3 Clinical and Biochemical characteristics according to vascular calcification score Score 0

Score 1

Score 2

Number

51

23

28

Age (years)

56.6 ± 12.4

57.0 ± 6.9

62.2 ± 9.0

Male/female DM

27/24 25/51 (49%)

13/10 20/23 (86%)*

21/7 24/28 (87%)*

Smoking History

17/51 (33.3%)

11/23 (48%)

15/28 (54%)

BMI (kg/m2)

21.5 ± 2.9

22.9 ± 3.4

21.9 ± 3.0

PAD

1/51 (2%)

4/23 (17%)

15/28 (54%)* 

ABI

1.07 ± 0.15

1.09 ± 0.16

1.05 ± 0.19

Calcium (mg/dl)

8.6 ± 1.1

8.6 ± 1.1

9.2 ± 1.1

Phosphate (mg/dl)

5.0 ± 1.6

4.5 ± 1.0

4.9 ± 2.0

CaXP (mg/dl)2

43.1 ± 14.9

38.7 ± 9.6

45.1 ± 18.8

iPTH (pg/ml)

171.8 ± 28.3

116.0 ± 28.6

142.0 ± 28.2

BUN (mg/dl)

70.9 ± 29.7

57.6 ± 21.0

66. 9 ± 23.2

Creatinine (mg/dl)

8.5 ± 4.0

6.9 ± 4.0

9.2 ± 2.7

Albumin (g/dl)

3.8 ± 0.5

3.6 ± 0.6

3.8 ± 1.2

Total cholesterol (mg/dl)

176.8 ± 61.0

184.6 ± 47.1

155.7 ± 44.5

Triglycerides (mg/dl)

151.7 ± 148.6

143.7 ± 69.9

83.8 ± 41.0

HDL (mg/dl)

38.4 ± 12.0

35.0 ± 11.8

35.2 ± 10.8

LDL (mg/dl) hs-CRP (mg/dl)

94.9 ± 37.9 0.44 ± 0.69

99.3 ± 34.0 0.62 ± 0.83

71.3 ± 20.1 1.31 ± 0.27*

Data are expressed as mean ± SD; iPTH is expressed as mean ± SE Score 0, vascular calcification score 0; Score 1, vascular calcification score 1; Score 2, vascular calcification score 2; PD peritoneal dialysis, HD hemodialysis, BMI body mass index, DM diabetes mellitus, PAD peripheral artery disease, ABI ankle brachial index, iPTH intact parathyroid hormone, BUN blood urea nitrogen, HDL high density lipoprotein cholesterol, LDL low density lipoprotein cholesterol, hs-CRP high sensitivity C-reactive protein *P \ 0.05(mean values are significantly different from score 0 group)  P \ 0.05 (score 2 group is significantly different from score 1 group)

that CKD patients, including HD and PD patients, already have a high probability of PAD if they have VCs, despite having no symptoms related to PAD. The probability of PAD increases with the VC score on the plain radiographs of feet and in the presence of diabetes mellitus. As expected, 43% of pre-dialysis patients with diabetic nephropathy had VCs on plain radiographs of feet in the current study. One predialysis patient with mild VCs, such as a score of 1, also showed atherosclerotic calcified plaque occlusions of the femoral or popliteal artery [30%. Symptoms of claudication may be masked by neuropathy among diabetic patients. Therefore, diabetic patients may ignore early lesions of feet and fail to report foot problems at an early stage. In addition, foot ulcers in diabetic patients may impair the quality of life and increase morbidity and mortality [14].

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Therefore, early screening and detection is very important to prevent the progression of PAD, even in pre-dialysis diabetic CKD patients. Routine ABI measurement could be used to identify patients with PAD, but without clinical symptoms. Patients with moderate reductions in ABI (0.90–1.10) or high ABI ([1.30) had increased all-cause and cardiovascular mortality when compared with patients having an ABI of 1.10–1.30 [15]. The ABI was not different according to PAD or VC score in the CKD patients, including those patients maintained on HD and PD. This result may be the result from medial artery calcification of the enrolled patients. A high or normal ABI value suggests the presence of medial artery calcification, which makes a diagnosis of PAD by ABI measurement unreliable. In this case, a toe brachial index (TBI) is recommended for the

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detection of PAD in CKD patients because the toepressure measurement is not disturbed by medial artery calcification [16]. Although ABI is the optimal test for screening of PAD, the ABI results must be carefully analyzed if patients have VCs on the radiographs of the feet. A further study is needed to elucidate the relationship with ABI, TBI, and medial artery calcification of the feet. Many risk factors for VC are found in the dialysis population: age, gender, duration of dialysis, inflammation, mineral metabolic abnormalities, and diabetes [17–19]. In the CKD patients, including patients maintained on HD and PD, the hs-CRP levels were significantly higher in patients with VCs or with PAD. Therefore, it is necessary to check the plain radiographs of feet as a simple screening test for PAD if the patients have high hs-CRP levels, even in predialysis patients with diabetic nephropathy. A high serum cholesterol level is a well-known cardiovascular disease (CVD) risk factor in the general population. However, a low cholesterol level is associated with high CVD in dialysis patients and this phenomenon has been referred to as reverse epidemiology [20]. In the current study, CKD patients, including those patients maintained on HD and PD with PAD, had significantly lower total cholesterol and lower LDL-cholesterol than in CKD patients without PAD, although the BMI and serum albumin level was not different between CKD patients with and without PAD. Wang et al. [21] confirmed the link between malnutrition, markers of inflammation, atherosclerotic vascular disease, and cardiac calcifications in PD patients. Recently, inflammation has been increased in CKD patients and it has been proposed as the explanatory cause for reverse epidemiology with respect to cholesterol [22]. This study showed that reverse epidemiology with respect to cholesterol is meaningful only when inflammation or malnutrition is present, but other studies have not shown the same results [23, 24]. Our results of low total cholesterol and lower LDLcholesterol may be related with high hs-CRP, but cannot explain malnutrition. A further evaluation is needed to support the relationship between low serum cholesterol level and PAD. The positive findings on the color Doppler ultrasonography that atherosclerotic calcified plaques occluding the femoral or popliteal artery [30% was shown in 56% of the patients with a VC score of 1

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and 83% of the patients with a VC score of 2. This observation suggests the high presence of partial obstruction of the peripheral artery in CKD patients, including those patients maintained on HD and PD without evidence of PAD. Thus, if a VC score of 2 is found on the plain radiographs of the feet in CKD patients, the patient should be evaluated for PAD. Patients with VCs had a high prevalence ([65%) of CAD, but showed no significant difference compared to patients without VC in our study. A recent report suggested that VC detected by single foot radiography was not an adequate alternative-screening marker for identifying patients with coronary artery calcification (CAC) [25]. These findings indicate that the prevalence of CAD or CAC is slightly different with peripheral artery calcification or PAD. Nevertheless, the authors mentioned that co-existence of coronary and peripheral artery calcification was common, particularly in patients with diabetes and CKD stages 3 and 4 [23]. Further studies are needed to find the associations between CAC and peripheral artery calcification. Typical linear railroad calcifications that outline the dorsalis pedis artery were found on the plain radiographs of feet with VC scores of 1 and 2 in the current study. VCs of ring-like forms were another finding that was frequently shown on the plain radiographs of the feet in patients with VC scores of 1 and 2. This VC form was formed by medial artery calcification in the transverse-sectioned vascular wall of the dorsalis pedis artery. Sometimes, this ring-like form was found without definite linear railroad calcifications in patients with a VC score of 1. This finding may suggest that the ring-like form may be an early detection marker of VC on the plain radiographs of feet. This study used the VC score based on the length of calcification of the dorsalis pedis artery, and not based on the number of calcification lesions on plain radiographs of the feet. This VC scoring method was determined by our preliminary investigation because no report regarding the degree of VC on the plain radiographs of the feet. Linear railroad calcifications were more prominent and longer when correlated to VC progression in our preliminary investigation. Usually patients with diabetes are interested in problems of the feet. We checked the radiographs of both feet and color Doppler ultrasonography of lower extremities. Thus, only pre-dialysis patients with

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diabetic nephropathy and PD patients with diabetes were recruited in this study, which might lead to selection bias. In conclusion, asymptomatic CKD patients, including patients maintained on HD and PD, may have PAD and routine testing by plain radiographs of the feet and followed by Doppler ultrasonography are of pivotal significance, especially if they are diabetic. Acknowledgments This study was supported by research funds from Dong-A University.

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