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SN Comprehensive Clinical Medicine

, Volume 1, Issue 11, pp 855–860 | Cite as

The Effect of Kidney Transplantation on Carotid Artery Intima-Media Thickness in End-Stage Renal Disease Patients

  • Leila Aghaghazvini
  • Monirsadat Hakemi
  • Armin Vaghardoost
  • Majid Shakiba
  • Amir Saberi-DemnehEmail author
  • Mona Fathi
Imaging
  • 145 Downloads
Part of the following topical collections:
  1. Topical Collection on Imaging

Abstract

Cardiovascular events are the main cause of mortality in chronic kidney disease (CKD) patients. Increased carotid artery intima-media thickness (C-IMT) is a strong predictor for cardiovascular events. The present study aimed to evaluate the effect of kidney transplantation on C-IMT in CKD patients. Eligible end-stage renal disease (ESRD) patients were evaluated by B-mode ultrasonography regarding C-IMT (mm) and atherosclerotic plaque size (mm2) 1 week before and 6 months after the hemodialysis or kidney transplantation. Also, peak systolic velocity (PSV, cm/s) of carotid artery was accessed with duplex ultrasonography. 38 hemodialysis and 56 kidney transplantation patients were enrolled in the study. The mean age of the patients was 55.1 ± 10.4 years. 32 (34%) cases were female, and the rest were male. The mean of C-IMT before and 6 months after hemodialysis - transplantation was 0.71 ± 0.2 - 0.71 ± 0.2 mm (p = 0.8) and 0.75 ± 0.2 - 0.66 ± 0.2 mm (p = 0.01), respectively. The mean of PSV before and after hemodialysis - transplantation was 58 ± 13.9 - 58.3 ± 15.6 cm/s (p = 0.9) and 60.9 ± 12.7 - 59.3 ± 12.4 cm/s (p = 0.6), respectively. The mean of atherosclerotic plaque size before and after hemodialysis - transplantation was 64.6 ± 34.3 - 50.1 ± 31.2 mm2 (p = 0.2) and 59.3 ± 31.1 - 48.8 ± 30.3 mm2 (p = 0.4), respectively. After 6 months, kidney transplantation in comparison with hemodialysis was associated with a significant decrease in C-IMT and was not effective on improving the size of atherosclerotic plaque and PSV.

Keywords

ESRD Kidney Transplantation Intima-media thickness Carotid artery Peak systolic velocity 

Introduction

Chronic kidney disease (CKD, GFR ≤ 59 ml/min/1.73 m2) is one of the health problems that affects about 10.6% of people in the communities [1]. CKD has no specific treatment, and its management includes etiology elimination, prevention of progression of the disease, control of complications, and supportive care. As the disease progresses and reaches end-stage renal disease (ESRD), dialysis or kidney transplantation is vital for the patients [2].

In the course of CKD progression, the rate of admission, cardiovascular events, and mortality increases in the affected patients [3]. Cardiovascular events are one of the most common causes of mortality in CKD cases [4]. Significant prevalence of the atherosclerosis risk factors in CKD patients, such as aging, diabetes, hypertension, dyslipidemia, inactivity, and inflammation, increases the arteriosclerosis severity and cardiovascular events risk [4, 5]. On the other hand, CKD with metabolic disorders and toxic conditions sets up a defective cycle to exacerbate or develop the atherosclerosis risk factors [6, 7].

One of the indices that have been shown to be an indicator of atherosclerosis is the carotid artery intima-media thickness (C-IMT), which is a predictor of cardiovascular and cerebrovascular events, even in people without a history of vascular disease [8, 9, 10].

The CKD cases have a higher level of C-IMT, indicating an increase in atherosclerosis, endothelial dysfunction, and inflammatory conditions [11]. It has been also observed that C-IMT with a cutoff point of 2.6 mm, independent of diabetes and hypertension, significantly increases the risk of cardiovascular events and mortality in CKD patients [12].

According to available evidence, kidney transplantation can potentially decrease arteriosclerosis severity by reducing the toxicity and subsequently modulating the inflammatory process and metabolism [13]. There are still a few studies regarding the effect of kidney transplantation on C-IMT of CKD patients. The present study aimed to investigate changes in C-IMT before and 6 months after hemodialysis or kidney transplantation in ESRD patients. In addition, we evaluated the carotid artery peak systolic velocity as a potential indicator of the atherosclerotic plaque instability [14, 15, 16]. The results of this study can add to the evidence.

Methods

This prospective study was conducted at Tehran Shariati Hospital, Iran, in 2014 after the Ethics Committee approval of Tehran University of Medical Sciences. Patients were the known cases of ESRD who had kidney transplantation or only hemodialysis. The inclusion criteria were GFR < 15 ml/min/1.73 m2, written consent, and history of constant hemodialysis. The exclusion criteria include the history of carotid artery surgery, unavailability of carotid arteries during ultrasonography due to technical or anatomical problems, stenosis of more than 50% of carotid artery lumen, prohibition of carotid massage due to cardiovascular events such as arrhythmia, and failure of transplantation during 6 months after surgery.

By a sequential selection, patients who have undergone kidney transplantation examined regarding inclusion criteria 1 week before surgery and eligible subjects were enrolled in the study. The hemodialysis group was matched with the transplanted group according to age, sex, past medical history, passed time of CKD, and hemodialysis duration.

Demographic information included age, sex, past medical history of diabetes, hypertension, hyperlipidemia, smoking (at least one cigarette per day), passed time of CKD, and hemodialysis duration. In addition, patients’ fasting blood sugar, systolic and diastolic blood pressure, LDL, HDL, triglyceride, and total cholesterol were recorded before and 6 months after the study.

Ultrasonography machine, MyLab™ 70 XVision (Esaote, Genoa, Italy), with a 7–12-MHz, linear array transducer, was used to investigate C-IMT, the size of atherosclerotic plaque, and peak systolic velocity (PSV). An expert radiologist performed ultrasonography a week before the study, and another expert radiologist performed ultrasonography 6 months after the study. The anatomical regions for ultrasonography included 2 cm before the common carotid artery bulb (CCA), the bulb of the common carotid artery (BCCA), and the internal carotid artery (ICA) at 2 cm after the bulb, bilaterally. Patients first laid on the bed in a supine position, and their neck was positioned in partial extension and the left and right rotation during the ultrasonography.

Three seconds of consecutive radiologist-targeted images at each area of the carotid artery was stored on the ultrasound’s hard disk and transferred to MATLAB software (Math Software Co., MathWorks, MATLAB USA, ver. 7.0.1). Then, IMT in the selected frames were measured in the systolic phase (images with maximal luminal diameter). The IMT was measured from the hyperechoic luminal area to the external hyperechoic surface of the artery wall (near and far walls) [17]. In this regard, three randomized points of near or far walls without an atherosclerotic plaque were evaluated in each mentioned anatomical regions at the transverse sections; the IMT (mean of three points in each area) was recorded in millimeter.

Atherosclerotic plaque was defined with an increase of more than 50% in localized IMT relative to its surrounding in B-mode ultrasonography images [18]. If an individual had more than one plaque in the anatomical areas, all of them were considered, and their average size was recorded (mm2). PSV was measured bilaterally in duplex ultrasonography in the three anatomical regions, and its mean was reported in cm/s.

SPSS17 software was used to analyze the data. Quantitative data were expressed as mean ± standard deviation and qualitative data were expressed as percentage. Student’s t test was used to compare the C-IMT, plaque size, and PSV before and 6 months after the study. Spearman or Pearson tests were used to measure the relationships among variables. The p < 0.05 was considered statistically significant.

Results

Ninety-four eligible individuals (38 hemodialysis and 56 transplanted patients) were enrolled in the study. The range and median age of the patients were 26–73 and 56 years, respectively. Table 1 shows the patient’s basic information. Most of the patients were male and non-smokers. The passed time of CKD diagnosis was 1–11 years and hemodialysis duration was 1–90 mounts. Hypertension and diabetes were the most common underlying comorbidities. The levels of fasting blood sugar (FBS), systolic blood pressure, LDL, HDL, triglyceride, and total cholesterol were not significant between the groups before the study (p > 0.05). The transplanted group has lower diastolic blood pressure before the study (p = 0.02). The transplanted group showed higher levels of LDL (p = 0.02), triglyceride (p = 0.02), and FBS (p = 0.000) and lower levels of systolic blood pressure (p = 0.0001) 6 months after the study (Table 1).
Table 1

Patient’s basic information (n = 94)

Variables

Hemodialysis (n = 38)

Transplantation (n = 56)

p

Age, year (mean ± SD)

54 ± 11.7

55.8 ± 9.4

0.4

Sex, number (%)

   

  Male

27 (71.1)

35 (62.5)

0.4

  Female

11 (28.9)

21 (37.5)

 

Diabetes, number (%)

13 (34.2)

18 (32.1)

0.8

Hypertension, number (%)

27 (71.1)

39 (69.6)

0.9

Hyperlipidemia, number (%)

8 (21.1)

5 (8.9)

0.1

Smoking, number (%)

7 (18.4)

7 (12.5)

0.4

CRF duration, year (mean ± SD)

5.7 ± 2.5

4.9 ± 2.1

0.2

Dialysis duration, mount (mean ± SD)

31 ± 23.5

22.3 ± 18

0.06

Fasting blood sugar, mg/dl

  Before

89.7 ± 22.4

97.1 ± 27.4

0.2

  After

85.6 ± 28.2

109.9 ± 26.1

0.000

Systolic blood pressure, mmHg

  Before

140.8 ± 20.1

139 ± 16.8

0.6

  After

141.4 ± 15.4

131.2 ± 13.7

0.001

Diastolic blood pressure, mmHg

  Before

91.4 ± 13.1

85 ± 12.3

0.02

  After

82.8 ± 13.2

78.8 ± 12.5

0.1

LDL, mg/dl

  Before

98.1 ± 30.3

95.8 ± 25.8

0.7

  After

91.6 ± 24.6

103 ± 24.5

0.02

HDL, mg/dl

  Before

36.5 ± 14.8

31.3 ± 13.4

0.09

  After

36.2 ± 14.6

35.1 ± 13

0.7

Triglyceride, mg/dl

  Before

172.9 ± 60.4

164.5 ± 34.7

0.4

  After

154.5 ± 63.5

185.7 ± 60.7

0.02

Total cholesterol, mg/dl

  Before

173.7 ± 43.1

175.9 ± 35

0.8

  After

169.3 ± 29.8

179.9 ± 28.8

0.09

The mean of IMT and PSV, regarding the anatomic areas or in total, is given in Table 2. These two variables had an increasing trend in the hemodialysis group and a decreasing trend in the transplanted group totally. After 6 months of kidney transplantation, the mean of IMT decreased significantly in all measured areas except left CC (p = 0.6). In comparison with the hemodialysis group, kidney transplantation decreased C-IMT totally (p = 0.01). PSV showed a significant lower scale in the transplanted group only in the right IC (p = 0.01) and left BCC (p = 0.02) in comparison with the hemodialysis group. Generally, PSV changes were not significant between the groups (p = 0.3).
Table 2

The changes in C-IMT, PSV, and size of arteriosclerotic plaque of carotid artery 1 week before and 6 months after kidney transplantation or hemodialysis

Variables

Hemodialysis (n = 38)

Transplantation (n = 56)

p

Hemodialysis (n = 38)

Transplantation (n = 56)

p

Before

After

Right C

CC-IMT1,2

0.79 ± 0.2

0.7 ± 0.2

0.08

0.84 ± 0.17

0.67 ± 0.17

0.000

BCC3-IMT

0.77 ± 0.2

0.68 ± 0.2

0.05

0.8 ± 0.2

0.64 ± 0.17

0.000

IC4-IMT

0.7 ± 0.2

0.68 ± 0.2

0.7

0.7 ± 0.2

0.75 ± 0.25

0.03

CC-PSV5

57.2 ± 16.2

53.3 ± 19.6

0.6

62.9 ± 17.6

57.9 ± 15.4

0.2

BCC-PSV

52.6 ± 14

53.9 ± 19

0.7

57.6 ± 15.4

53.6 ± 13.9

0.2

IC-PSV

61.3 ± 13.3

58.8 ± 19.1

0.5

68.1 ± 14.4

60 ± 14.2

0.01

Left C

CC-IMT

0.7 ± 0.25

0.74 ± 0.26

0.5

0.71 ± 0.3

0.68 ± 0.2

0.6

BCC-IMT

0.74 ± 0.2

0.72 ± 0.2

0.6

0.78 ± 0.2

0.67 ± 0.2

0.003

IC-IMT

0.72 ± 0.2

0.71 ± 0.2

0.8

0.75 ± 0.2

0.66 ± 0.2

0.04

CC-PSV

58.4 ± 13.5

60.9 ± 20.8

0.5

59.5 ± 14.5

57.8 ± 15.4

0.6

BCC-PSV

54.1 ± 13.3

59.3 ± 20.8

0.1

63.8 ± 13.3

56.9 ± 15.7

0.02

IC-PSV

58 ± 13.9

58.3 ± 15.6

0.9

60.9 ± 12.7

59.3 ± 14.2

0.6

Total

C6-IMT

0.71 ± 0.2

0.71 ± 0.2

0.8

0.75 ± 0.2

0.66 ± 0.2

0.01

C-PSV

55.5 ± 12.4

58.4 ± 17.6

0.4

60.6 ± 13.1

57.6 ± 13.3

0.3

Plaque size, mm2

64.6 ± 34.3

50.1 ± 31.2

0.2

59.3 ± 31.1

48.8 ± 30.3

0.4

1CC common carotid artery

2IMT intima-media thickness (mm)

3BCC bulb of common carotid artery

4IC internal carotid artery

5PSV peak systolic velocity (cm/s)

6C carotid artery

The atherosclerotic plaque was observed in 23 (41.7%) patients of the transplanted group and 12 (31.8%) patients of the hemodialysis group. After 6 months, the average of plaque size decreased in both groups without any significant difference between them (p = 0.4) (Table 2).

Regarding variables of Table 1, PSV correlated with the passed time of CKD (r = 0.33, p = 0.037) and male gender (r = 0.37, p = 0.021) in the hemodialysis group before the study. Six months after hemodialysis, PSV correlated with the passed time of CKD (r = 0.35, p = 0.03) and male gender (r = 0.33, p = 0.04). In the transplanted group before the study, the higher PSV correlated with male gender (r = 0.34, p = 0.02) and higher C-IMT correlated with age (r = 0.22, p = 0.04), and 6 months after, higher PSV correlated with male gender (r = 0.35, p = 0.008). Kidney transplantation was associated with the increased levels of FBS (r = 0.4, p = 0.000), LDL (r = 0.2, p = 0.02), and triglyceride (r = 0.2, p = 0.02) and the decreased levels of systolic blood pressure (r = 0.3, p = 0.001).

Discussion

The present study evaluated the effect of kidney transplantation on C-IMT changes in ESRD patients. In the results, 6 months after the kidney transplantation, IMT in common carotid arteries and internal carotid arteries showed a significant decrease in comparison with hemodialysis. In other results of this study, kidney transplantation did not affect the PSV and arteriosclerotic plaque size.

A few studies have been conducted on the role of kidney transplantation on C-IMT as a risk factor for cardiovascular complications and mortality in CRF patients [12], which is generally consistent with the results of the present study.

Bilginer et al. after a 12-month follow-up of kidney-transplanted patients with an average age of 16.5 years reported that the C-IMT of the patients was more than that of healthy individuals [17]. They did not compare C-IMT before and after transplantation, so in their results, the effect of transplantation on the C-IMT changes is unclear. Litwin et al. observed that kidney transplantation in 34 adolescents is associated with a significant reduction in C-IMT in carotid artery bulb. Comparing these individuals with hemodialysis and non-hemodialysis patients with CKD as well as healthy people showed that C-IMT in kidney-transplanted patients was significantly lower than that of the hemodialysis patients and higher than that of healthy subjects and it is similar to non-advanced stages of CKD [19]. In a study by Yilmaz et al., C-IMT decreased less than 3 months after kidney transplantation in 58 patients. In their results, the increase in stages of renal failure was directly related to the increase in C-IMT [20]. Saedi et al. after 6–12-month monitoring of 75 kidney-transplanted patients observed that the C-IMT of the transplanted cases was significantly lower than that of the hemodialysis patients [21]. C-IMT in a 1.5–4-year follow-up of 22 kidney-transplanted patients had a descending trend in the study of De Lima et al. as well as our study [22].

Fortunately, according to the results of published studies, kidney transplantation in CKD patients leads to arteries’ return to the earlier stages of renal failure in the early months after transplantation [20, 21, 23]. Accordingly, kidney transplantation in CKD patients who are waiting for a kidney is ideal than the hemodialysis.

The most important probability in justifying the effectiveness of kidney transplantation on C-IMT reduction is the reduction or elimination of the toxic conditions. Changes in modifiable arteriosclerosis frisk actors, such as metabolism disorders especially imbalance in calcium and phosphorus, hypertension, and inflammation [24, 25], can reduce C-IMT. On the contrary, immunosuppressive drug consumption after transplantation may create some metabolic challenges such as hyperlipidemia [26] and increased blood sugar [27] in some cases, as well as the present results, which can reduce the positive effect of kidney transplantation on the arteriosclerosis intensity and metabolic conditions.

Up to now, various risk factors, associated with increasing C-IMT in CKD patients, have been reported. Aging, diabetes, hypertension, CRF length, hemodialysis, dyslipidemia, male gender, blood phosphorus level, and Ca × P are among these risk factors [17, 20, 21, 28, 29, 30, 31]. In the present study, the increase in age was associated with an increase in C-IMT, which is consistent with other studies [22, 31].

PSV tends to increase with decreasing lumen diameter of a vessel as occurred in the process of atherosclerosis [32, 33]. Hemodialysis patients have an increased PSV level compared with healthy individuals [34]. According to our knowledge, there is no study which compared PSV between hemodialysis and kidney transplant patients. In the present study, kidney transplantation did not lead to significant changes in PSV. Also, further analysis showed no association between presence of the atherosclerotic plaque in the evaluated areas and PSV. The mean PSV in the present study was less than 80 cm/s, which is close to healthy persons and is lower than persons with carotid stenosis ≥ 50% who are at risk of cerebrovascular events [32, 33]. Higher PSV, independent to degree of the common carotid artery stenosis, may increase risk of atherosclerotic plaque rupture and bleeding slightly [14]. In justifying the present finding, regardless of the possibility of a short-term follow-up effect, vascular stiffness and decrease in vasodilation ability [22, 35], especially due to the deposition of calcium and phosphorus in the vascular walls [35], can prevent significant changes in the PSV.

The main limitations in this study were the lack of long-term follow-up and the lack of a non-hemodialysis-dependent CKD group.

In summary, the results of this study showed that kidney transplantation in ESRD patients in comparison with hemodialysis reduced the carotid artery IMT after 6 months.

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical Statement

The study protocol was approved by the medical ethics board of the Tehran University of Medical Sciences, Iran. The study included only adults and written informed consents were provided by all the subjects who participated in the study.

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of RadiologyTehran University of Medical SciencesTehranIran
  2. 2.Department of NephrologyTehran University of Medical SciencesTehranIran
  3. 3.Faculty of MedicineTehran University of Medical SciencesTehranIran
  4. 4.Advanced Diagnostic and Interventional Imaging Research CenterTehran University of Medical SciencesTehranIran
  5. 5.Faculty of MedicineSemnan University of Medical SciencesSemnanIran

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