Prevalence and correlates of vascular disease at ultrasound examination in patients on hemodialysis

Abstracts

FUNDAMENTO: Pacientes em hemodiálise (HD) apresentam risco aumentado de morte cardiovascular. A espessura íntima-média (EIM) e a presença de calcificações arteriais são fatores de risco bem conhecidos para morte cardiovascular em pacientes em HD. OBJETIVO: Avaliar a prevalência de EIM e calcificações em pacientes em HD e correlacionar achados de imagem com dados clínicos e laboratoriais. MÉTODOS: Estudo transversal de 75 pacientes em HD por > 12 meses. Os pacientes foram submetidos à ultrassonografia (US) modo-B para determinação da EIM do terço distal das artérias carótidas comuns. As calcificações arteriais foram avaliadas por US de artérias carótidas, femorais e tibiais e consideradas positivas se calcificações fossem encontradas em qualquer sítio arterial. RESULTADOS: Os pacientes tinham 52 ± 13 anos, 57% eram do sexo masculino e 16% eram diabéticos. EIM > 0,9 mm foi encontrada em 57% dos cases e calcificações arteriais na US em 48%. Envelhecimento (décadas) e tabagismo estavam associados com aumento da EIM (odds ratio ajustado [aOR] = 3,4, p < 0,001; aOR = 4,4, p = 0,045, respectivamente) e presença de calcificações vasculares (aOR = 3,0, p < 0,001; aOR = 6,8, p = 0,011, respectivamente). Altos níveis de hormônio paratireoidiano intacto (iPTH) (por 100 pg/ml) estavam associados de forma significante com aumento na EIM (aOR = 1,7, p = 0,021), mas não com calcificação vascular. Em contraste, diabete e tempo de diálise (anos) foram determinantes significantes para calcificações na US (aOR = 15,0, p = 0,009; aOR = 1,39, p = 0,020), mas não para o aumento da EIM. CONCLUSÃO: EIM aumentada e calcificações à US são achados comuns em pacientes em HD. Envelhecimento e tabagismo são determinantes consistentes para ambas as alterações de imagem. Aumento nos níveis de iPTH está associado com aumento na EIM. Diabete e tempo de diálise aumentam de forma substancial o risco de calcificação arterial.

Diálise renal; doenças vasculares; calcinose; ultrassonografia

FUNDAMENTO: Pacientes en hemodiálisis (HD) presentan riesgo aumentado de muerte cardiovascular. El espesor íntima-media (EIM) y la presencia de calcificaciones arteriales son factores de riesgo bien conocidos de muerte cardiovascular en pacientes en HD. OBJETIVO:Evaluar la prevalencia de EIM y calcificaciones en pacientes en HD y correlacionar hallazgos de imagen con datos clínicos y de laboratorio. MÉTODOS:Estudio transversal de 75 pacientes en HD por >12 meses. Los pacientes fueron sometidos a ultrasonografia (US) modo-B para determinación de la EIM del tercio distal de las arterias carótidas comunes. Las calcificaciones arteriales fueron evaluadas por US de arterias carótidas, femorales y tibiales y consideradas positivas si fuesen encontradas calcificaciones en cualquier sitio arterial. RESULTADOS:Los pacientes tenían 52±13 años, 57% eran del sexo masculino y 16% eran diabéticos. EIM > 0,9mm fue encontrada en 57% de los casos y calcificaciones arteriales en la US en 48%. Envejecimiento (décadas) y tabaquismo estaban asociados a aumento de la EIM (odds ratio ajustado [aOR] = 3,4, p < 0,001; aOR = 4,4, p = 0,045, respectivamente) y presencia de calcificaciones vasculares (aOR = 3,0, p < 0,001; aOR = 6,8, p = 0,011, respectivamente). Altos niveles de hormona paratiroidea intacta (iPTH) (por 100 pg/ml) estaban asociados de forma significativa a aumento en la EIM (aOR = 1,7, p = 0,021), pero no a calcificación vascular. En contraste, diabetes y tiempo de diálisis (años) fueron determinantes significativos para calcificaciones en la US (aOR = 15,0, p = 0,009; aOR = 1,39, p = 0,020), pero no para el aumento de la EIM. CONCLUSIÓN:EIM aumentada y calcificaciones en la US son hallazgos comunes en pacientes en HD. Envejecimiento y tabaquismo son determinantes consistentes para ambas alteraciones de imagen. Aumento en los niveles de iPTH está asociado a aumento en la EIM. Diabetes y tiempo de diálisis aumentan de forma sustancial el riesgo de calcificación arterial.

Diálisis renal; enfermedades vasculares; calcinosis; ultrasonografía

^IClinefron Clínica de Doenças Renais, Niterói, RJ - Brasil

^IISanto Antonio de Pádua, RJ, Divisão de Nefrologia, Faculdade de Medicina, Universidade Federal Fluminense, Niterói, RJ - Brasil

^IIINiterói, RJ, Departamento de Estatística, Instituto de Matemática e Estatística, Universidade Federal Fluminense, Niterói, RJ - Brasil

Mailing address

ABSTRACT

BACKGROUND: Patients on hemodialysis present an increased risk of cardiovascular death. Intimal media thickness (IMT) and presence of arterial calcifications are well-known risk factors for cardiovascular death in hemodialysis patients.

OBJECTIVE: To assess the prevalence of IMT and arterial calcifications in HD patients and to correlate image findings with clinical and laboratory data.

METHODS: Cross-sectional study involving 75 patients on dialysis for >12 months. Patients underwent B-mode ultrasound scan (US) for determination of IMT of the distal third of the common carotid arteries. Arterial calcifications were assessed by US of carotids, femoral and tibial arteries, and labeled positive if calcification was found in any arterial site.

RESULTS: Patients were 52±13 years old, 57% were males and 16% were diabetics. IMT > 0.9 mm was found in 57% of cases and arterial calcifications at US in 48%. Aging (decades) and smoking were associated with both increased IMT (adjusted odds ratio [aOR] = 3.4, p < 0.001; aOR = 4.4, p = 0.045, respectively) and presence of vascular calcifications (aOR = 3.0, p < 0.001; aOR = 6.8, p = 0.011, respectively). High intact parathyroid hormone levels (per each 100 pg/ml) were significantly associated with increased IMT (aOR = 1.7, p = 0.021), but not with vascular calcification. In contrast, Diabetes and time on dialysis (years) were significant determinants for calcifications at US (aOR = 15.0, p = 0.009; aOR = 1.39, p = 0.020), but not for increased IMT.

CONCLUSION: Increased IMT and calcifications at US are common findings in hemodialysis patients. Aging and smoking are consistent determinants for both image alterations. Parathyroid hormone elevation is associated with increased IMT. Diabetes and time on dialysis substantially increase the risk for arterial calcification.

Keywords: Hemodialysis, vascular diseases, calcinosis, Doppler ultrasonography.

Introduction

End-stage renal disease (ESRD) patients have a high mortality rate, mainly related to cardiovascular disease¹. The development of non-invasive strategies for early detection of vascular disease could provide opportunities for an early patient approach. B-mode ultrasonography (US), which carries the potential for detection of early stages of vascular disease, can be used for the measurement of intimal-media thickness (IMT), considered a marker of atherosclerosis, and for detection of arterial calcifications², which have been shown to be associated with a poorer survival rate on dialysis^3,4. Currently, other diagnostic methods are available for the identification of arterial calcification in the clinical setting, including x-rays, echocardiography and electron-beam computer tomography^5-7. However, B-mode ultrasonography is a low-cost and easy-to-perform technique.

The objectives of the present study were to assess the prevalence of increased IMT and vascular calcifications using B-mode US and to correlate the findings with clinical and laboratory data.

Methods

This is a cross-sectional, single-center study in which patients from a single dialysis center aged between 18 and 75 years, who had been on hemodialysis for at least 12 months, were approached for enrollment. The study was approved by the local Ethics Committee and all patients signed the informed consent form. Evaluation was accomplished between March 2006 and September 2007.

Imaging studies

B-mode US was always performed by the same experienced physician, using high resolution B-mode (7.5-MHz transducer) ultrasonography devices (Medison 8000, and Esaote Caris Plus). IMT measurements were performed in the distal third of the common carotid arteries as previously suggested². Cases with any value > 0.9 mm, a cutoff previously associated with elevated incidence of cardiovascular events in a non-dialysis population^8,9, were labeled positive. At the ultrasonographic evaluation of vascular calcification, a highly echogenic vascular wall or intraluminal structure producing bright echoes with shadowing were considered to be calcifications¹⁰. The sites investigated were: the distal third of the common carotid arteries; carotid and proximal third of the internal and external branches; the whole length of common femoral arteries, proximal third of superficial and deep femoral arteries; and distal half of posterior tibial arteries¹⁰. If a calcification was found in any arterial site, the case was labeled positive¹¹.

Demographic, clinical and laboratory data

Demographic and clinical data were derived from chart examination. Hypertension was defined as current pre-dialysis systolic BP > 140 mmHg and/or diastolic BP > 90 mmHg and/or use of antihypertensive medications. Patients were classified as diabetics if they had diabetes previously to renal replacement therapy. Hemoglobin, creatinine, and equilibrated Kt/V (eKt/V) values represent the mean of the last three determinations before evaluation. To better estimate the impact of mineral metabolism disturbances on findings, cumulative exposure was assessed through calculation of the mean of all values for serum calcium, phosphorus and intact parathyroid hormone (i-PTH) measurements along a 36-month period just before evaluation or since hemodialysis initiation for patients on renal replacement therapy for less than 3 years. Calcium and phosphorus serum levels were measured on a monthly basis and i-PTH every six months. Routine blood analyses were performed in the same laboratory. An ultra-sensitive immunoturbidimetric assay for C-reactive protein (CRP) was specifically performed for the study and the values shown here correspond to a single determination by the time of study enrollment.

Statistical analyses

Continuous variables are presented as mean ± SD or median and range as appropriate. Categorical variables are shown as frequencies. Differences between frequencies were analyzed by the Chi-square test. Associations between variables were assessed by backward conditional logistic regression analysis, in which all potentially relevant variables are included in the first step. Only variables presenting P values lower than 0.10 persisted in the next step. In case of significant collinearity between two variables, only the more relevant persisted in the next step. The decision about which variables should be excluded from the analysis in each step was made by the software. P values lower than 0.05 were considered significant. The software SPSS, version 17.0 was used for all statistics.

Results

Of 128 patients on hemodialysis, 75 were enrolled in this study. The main reasons for exclusions were: dialysis time lower than one year (18 patients); age older than 75 years (14 patients); and refusal to participate in the study (12 patients). Patients enrolled in the study were 52 ± 13 years old, 43 (57%) males, 59 ± 34 months on hemodialysis, and 12 (16%) were diabetics. Demographic and clinical characteristics of patients are shown in Table 1. Patients presented a wide range of age (Figure 1) and time on dialysis. Forty patients (53%) were on hemodialysis for less than 5 years, 30 (40%) for 5 to 10 years and 5 (7%) for more than 10 years. Laboratory data are shown in Table 2.

B-mode US was performed in all 75 patients. Increased IMT was present in 43 (57%) and arterial calcifications were detected in 36 (48%), Table 3. Calcification was present in more than three arteries in 23 of these 36 patients and 33 of them also exhibited increased IMT. Ten patients (22%) with increased IMT did not have ultrasonographic calcifications.

In search for determinants of the image findings, two models of backward conditional regression analysis were developed, with each one using IMT > 0.9 mm and calcifications at US as the dependent variables. Clinical and laboratory data were used as the independent variables. Age (adjusted odds ratio [aOR] = 3.36 per decade, p < 0.001), smoking (aOR = 4.49, p = 0.046), and high iPTH levels (1.67 per 100 pg/ml) were significantly associated with IMT > 0.9 mm, Table 4. Age (aOR = 2.96 per decade, p < 0.001) and smoking (aOR = 6.77, p = 0.011) were also associated with calcifications at US, Table 5. Diabetes (aOR = 1.67, p = 0.021) and time on dialysis (aOR = 1.39, p = 0.020) were associated with a significant risk for calcifications at US (aOR = 1.67, p = 0.021 and aOR = 1.39, p = 0.020, respectively), but not for increased IMT. Phosphorus, calcium, Ca'P product and iPTH were not found to be risk factors for vascular calcification at US. C-reactive protein levels were not associated with IMT > 0.9 mm or calcifications at US.

To better explore the relationship between i-PTH levels and IMT an additional multivariate regression analysis model was used, in which i-PTH levels were stratified in 3 categorical ranges: < 150 pg/ml, 150 to 300 pg/ml, and > 300 pg/ml. In this analysis, a significant elevated risk was restricted to the highest band (> 300 pg/ml) in comparison to the middle band (aOR = 6.26 [1.05 - 37.50], P = 0.045).

Discussion

It is well known that ESRD patients bear an elevated risk for cardiovascular diseases, which represent the leading cause of death in this population¹. The arterial disease is generalized and the presence of carotid structural defects^2,8, as well as peripheral vascular disease^2,12 are strongly correlated with coronary disease and mortality. The objective of this study was to assess vascular disease in ESRD patients using non-invasive imaging studies and to correlate the findings with clinical and laboratory data. The profile of our patients is roughly similar to the overall population on dialysis in Brazil¹³.

The frequency of IMT > 0.9 mm, a recognized marker of atherosclerosis, was very high, affecting 43 (57%) of patients. Although a number of studies had already addressed the issue of IMT determination in ESRD patients^14,15, we could not find the incidence of IMT > 0.9 mm in a non-selected hemodialysis sample for an appropriate prevalence comparison. It should be emphasized that the rate of 57% was obtained with a cutoff of 0.9 mm, which is associated with increased incidence of cardiovascular events⁸, but is, in some way, conservative. In a recent study, for instance, it was found that the upper limits (97.5 percentile) of IMT in a healthy population aged 50 to 59, and 60 to 75 years were 0.71 and 0.81 mm, respectively¹⁶.

Calcifications at US were also common, affecting 36 (48%) of patients, a proportion comparable to the ones reported in previous studies, which varied from 50 to 64%^17-19. Thirty-three out of our 36 patients with calcifications also exhibited increased IMT, whereas 10 patients with increased IMT did not have ultrasonographic calcifications. These findings are consistent with the present view that increased IMT can be seen as a preclinical marker of atherosclerosis that precedes plaque formation^2,20.

To check for potential determinants of image findings in our study, we resorted to two models of logistic regression analysis, using selected clinical and laboratory data as independent variables against each one of the image findings. Age uniformly influenced image parameters, in a way that each decade of age was associated with approximately a three-fold increase in the chance of a positive finding in the studied image parameters. This finding is consistent with the extensive information available in the literature, highlighting the role of age on the development of vascular disease^16,21. Similarly, smoking influenced both image parameters, with a four-fold increase in the chance of a positive IMT and an almost seven-fold increase in the chance of a calcification. Studies addressing smoking as a risk factor for vascular calcification in ESRD patients are scarce, but the smoking habit is a traditional risk factor for cardiovascular disease, with the risk being strongly dose-related²². The effects of time on dialysis, as well as of diabetes, however, were only seen towards the presence of calcifications. A recent study showed that patients on hemodialysis have roughly an eight-fold increased risk of having vascular calcification, when matched to subjects in general population²³. Diabetes is a well-known risk factor for vascular calcifications²⁴ and the absence of its influence on increased IMT allows us to speculate whether the uremic environment can prevail upon glucose metabolism derangements during the early phase of vascular structural abnormalities in ESRD²⁵ patients. However, caution is advised in this regard, as the size of the sample may have contributed to the lack of impact of this factor upon IMT enlargement. High levels of i-PTH levels were associated with increased IMT. In an attempt to better clarify this issue, we resorted to an additional regression model employing i-PTH stratification. Significant association between i-PTH levels and increased IMT was restricted to the comparison between the group with PTH levels > 300 pg/ml and the one with i-PTH values between 150 and 300 pg/ml.

Interestingly, we did not find a correlation between vascular calcifications and cumulative mineral metabolism disturbances in our study. However, this finding cannot be seen as an argument against the reported role of phosphate overload in the development of vascular calcification^26,27, as phosphate serum levels may not be a precise marker of the oral phosphate load²⁸. In addition, it does not refute the extensive literature placing mineral metabolism disturbances as pivotal risk factors for the high cardiovascular mortality among ESRD patients^29,30, as mortality was not addressed in our study. It should be mentioned that, in agreement to our findings, absence of correlation between Ca ' P product and IMT had already been reported¹⁵.

Our study carries limitations and the negative data should be interpreted with caution. The cross-sectional character of the design and the low number of patients may have contributed to the lack of significance in some statistics. However, the positive findings reinforce the role of some traditional risk factors such as aging, smoking, and diabetes as determinants of vascular disease in the ESRD population. They also show that some non-traditional factors, such as time on dialysis and elevated i-PTH levels can have an impact upon vascular abnormalities in such patients.

Conclusions

Both increased IMT and calcifications at US are common findings in hemodialysis patients, but increased IMT was more frequent. Smoking was a consistent determinant for both image findings. The major impact was seen with age, so that each decade of age was associated with a three-fold increase in the chance of a positive finding in any of the imaging studies. Diabetes and time on dialysis substantially increase the risk for arterial calcification.

Potential Conflict of Interest

No potential conflict of interest relevant to this article was reported.

Sources of Funding

There were no external funding sources for this study.

Study Association

This article is part of the thesis of master submitted by Sebastião Baptista Miguel, from Universidade Federal Fluminense.

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Prevalence and correlates of vascular disease at ultrasound examination in patients on hemodialysis

Sebastião Baptista Miguel^{I, II}; Jair Baptista Miguel^{I, II}; Luis Guillermo Velarde^III; Elisa de Albuquerque Sampaio^II; Jorge Paulo Strogoff de Matos^II; Jocemir Ronaldo Lugon^II

Publication Dates

• Publication in this collection
  04 Mar 2011
• Date of issue
  Apr 2011

History

• Received
  05 July 2010
• Accepted
  30 Nov 2010
• Reviewed
  20 Oct 2010