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Vol. 28. Issue. 3.July 2008
Pages 241-359
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Peripheral vascular disease: prevalence, mortality and association with inflammation in haemodialysis
Enfermedad vascular periférica: prevalencia, mortalidad y asociación con inflamación en hemodiálisis
Almudena Vega Martíneza, R.. Pérez Garcíaa, S.. Abada, E.. Verdea, J. M.. López Gómeza, R.. Jofréa, M.. Puertaa, P.. Rodrígueza
a Servicio de Nefrología, Hospital General Universitario Gregorio Marañón, Madrid, Madrid, España,
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La enfermedad vascular periférica es una complicación frecuente en la población en hemodiálisis que contribuye a aumentar su morbi-mortalidad, al favorecer el estado inflamatorio, la malnutrición y las complicaciones severas como la isquemia y la sepsis secundaria. El objetivo del estudio fue analizar la prevalencia de enfermedad vascular periférica en nuestra población en hemodiálisis, su repercusión en la mortalidad y su asociación con parámetros de inflamación y malnutrición. Fueron incluidos 220 pacientes prevalentes en hemodiálisis, del área perteneciente a nuestro centro hospitalario. Se realizó un estudio basal en el año 2001 y se siguieron durante 48 meses. La enfermedad vascular periférica fue diagnosticada en función de los datos recogidos de las historias clínicas. Se clasificó en ausencia, claudicación intermitente, úlceras o necrosis. De los 220 pacientes, el 39,5% padecía EVP. La clínica más frecuente fue claudicación intermitente (30%), seguida de úlceras (6,5%) y necrosis (3%). El 95% recibió tratamiento médico, el 0,5% fue tratado con angioplastia, el 2% con by-pass y se amputó al 2,5%. En el análisis univariante los pacientes con EVP eran más mayores, con mayor índice de Charlson, diabéticos, tenían niveles séricos más elevados de PCR, fibrinógeno y menores de albúmina y prealbúmina; con respecto a los libres de enfermedad. La supervivencia de los pacientes con EVP fue significativamente menor, analizando la curva Kaplan-Meier (log rank = 12,4; p < 0,000). En el análisis de Cox, los factores que se asocian de forma independiente a la mortalidad son la EVP (p = 0,034; OR = 2,10; IC [1,06 ; 4,23]), la edad (p = 0,001; OR=1,06; IC [1,03; 1,09]) y los niveles bajos de prealbúmina (p = 0,012; OR = 0,93; IC [0,89; 0,98]). La enfermedad vascular periférica es una complicación frecuente en la población en HD, que se asocia frecuentemente a un estado inflamatorio y a un mayor riesgo de mortalidad. Su diagnóstico precoz, mediante interrogatorio dirigido o con exploraciones complementarias, es obligado para iniciar tratamiento.
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Enfermedad vascular periférica
Peripheral vascular disease (PVD) is a common disease among patients undergoing hemodialysis leading to increase morbidity and mortality with a high risk of inflammation and sepsis. The aim of the present study was to determinate PVD prevalence in our hemodialysis population and association with inflammation. The study sample consisted of 220 patients prevalents in hemodialysis. A basal study was made in 2001 and a follow up for 47 months. Data were collected retrospectively. PVD diagnosis was made attending to limb pulses and doppler in revisions. Diagnosis was classified as rest pain, ischemic ulceration and gangrene. Among a total of 220 patients, 89 had prevalent PVD. Thirty per cent had rest pain, 6,5% had ischemic ulceration and 3% had gangrene. Ninety five per cent underwent medical treatment, 0,5% were treated by percutaneous transluminal angioplasty (PTA), 2% were treated with surgical revascularization and 2,5% were treated with amputation. Patients with PVD were older, with higher Charlson index, diabetes, they hay higher CRP and fibrinogen serum levels; and lower albumin and prealbumine serum levels. Survival PVD was decreased in Kaplan-Meier (log rank 012,4; p < 0,000). Adjusted Cox regression analysis revealed that PVD (p = 0,034; OR = 2,10; IC [1,06; 4,23]) ; age (p = 0,001; OR = 1,06; IC [1,03; 1,09]) and low serum albumin levels (p = 0,012; OR = 0,93; IC [0,89; 0,98]) predicted significantly the risk of mortality. PVD is an independent mortality risk factor in hemodialysis patients. An early diagnosis and treatment are able with examination and doppler. In our sample, a few patients are treated with PTA or surgical revascularization. There is an association between PVD and inflammation.
Peripheral vascular disease
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Peripheral vascular disease (PVD) is a common condition in the population on haemodialysis, with an estimated prevalece ranging  from 17% and 48%  in  the different  series  reported.1,2 The reason for such a wide range is not clear. It is probably due to the great incident and prevalent variability existing  in  the literature because of  the different forms  in which diagnosis is made, i.e. the wide variation in diagnostic criteria and the high percentage of cases with silent PVD in its early stages that is not always considered as disease.

PVD  causes  an  increased morbidity  and mortality  in  the general population because of both the triggering factors (age, smoking, high blood pressure, dyslipidemia, or diabetes mellitus) and its potential complications (ischaemia and sepsis),3 but its estimated mortality in the haemodialysis population is even greater because of the influence of a number of additional factors, including the chronic inflammation and malnutrition status secondary to both kidney disease and renal replacement  therapy,  and  increase  in  the  calcium-phosphorus product  and  development  of  secondary  vascular  calcifications.1,4 The crude annual mortality rate from stage V chronic kidney disease on haemodialysis in Spain is 14%, and is associated to the presence of cardiovascular events.5

In any case, patients  in haemodialysis units are older and have  several  associated diseases  and  a high  rate of diabetes mellitus. The prevalence of PVD may therefore be expected to  gradually  increase  in  the  coming  years. However, while universally accepted guidelines are established for early diagnosis and management of coronary disease associated to haemodialysis, no protocols that could contribute to improve survival and quality of life are available for patients with PVD.

The  objective  of  this  study  is  to  report  the  prevalence  of PVD in our setting and to analyse its relationship to comorbidity, the inflammatory status, and mid-term mortality.


Prevalent HD patients aged 18 years or older ascribed to a health area of Madrid as of June 2001 (a total of 220 patients) were enrolled into the study.

This was  a  descriptive,  retrospective  study  that  analysed whether patients had  in June 2001 PVD, of what grade, and the treatment administered, if any. A number of variables that could influence the risk of death were analysed. Patients were followed up for 48 months, i.e. until June 2005, when the status of each patient was analysed.

The  clinical  records of  all patients were  reviewed  for  the following data: sex, age, cause of renal failure, diabetes mellitus, grade of PVD, treatment of PVD, Charlson comorbidity index,  C-reactive  protein,  albumin,  prealbumin,  fibrinogen, erythropoietin resistance index, interleukin-6, and patient status at study end.

PVD was diagnosed based on patient  symptoms or when the disease was detected by supplemental examinations at revisions in asymptomatic patients. In all patients with clinical signs,  diagnosis was  confirmed  using  imaging  tests  such  as echo-Doppler of lower limbs or segmental pressures.

The grade of PVD was rated based on clinical criteria: none, intermittent claudication, ischaemia/ulcers, and necrosis.

Treatment  for  PVD  was  classified  as medical  treatment, angioplasty, bypass, and amputation. Medical  treatment was based on antiplatelet aggregants and pentoxyfylline.

The Charlson comorbidity index is a widely used index to measure patient morbidity. It  is particularly useful and commonly  used  in  the  population  on haemodialysis. The  following  personal  history  data  are  considered  to  calculate  the Charlson index: acute myocardial infarction, congestive heart failure, chronic pulmonary disease,  rheumatological disease, hepatic disease, gastroduodenal ulcer, renal disease, diabetes mellitus,  cerebrovascular disease, dementia, hemiplegia, peripheral vascular disease, neoplasm, or VIH disease.6

The erythropoietin resistance index is a parameter calculated as the weekly erythropoietin dose received by each patient (in international units per kg of weight) divided by haemoglobin (in g/dL).

The status of each patient as of May 2005 was classified as death,  active  on  haemodialysis,  transplanted,  or  mover  to another unit. The date of the event causing patient withdrawal from follow-up was also recorded.


A Kolgomorov test was used to identify normally distributed variables,  that were expressed as  the mean and standard deviation (SD). A logarithmic transformation was used to achieve normal distribution of some variables, such as CRP. Variables  not  having  a  normal  distribution  were  expressed  as median and 95% confidence  interval. To analyse qualitative variables and compare proportions, a Chi-square test or a Fisher¿s exact test was used as appropriate. A Student¿s t test for independent samples was used to compare quantitative variables. Survival curves were calculated using the Kaplan-Meier method and compared using a log-rank test. Independent variables predicting for mortality were studied using a Cox regression. All probability values  less  than 0.05% were considered  significant.  SPSS.13  software  was  used  for  data processing and analysis.


Characteristics of the study population

Among  the  220  patients  enrolled  into  the  study,  124  were males (56%) and 96 females (44%), with a mean age (SD) at study start of 62 ± 14 years. Age ranged from 23 and 88 years. Time  of  patients  on  haemodialysis  ranged  from  one month and 26 years, with a mean (SD) of 69.9 ± 67,3 months. The most common cause of renal failure was chronic glomerulonephritis  in  41  patients  (18.6%),  followed  by  an  unknown etiology  in 37 patients  (16.8%) and diabetic nephropathy  in 18  cases  (8.2%).  Forty-seven  patients  had  diabetes mellitus (21.4%).  The mean  Charlson  comorbidity  index was  6.0  ± 5.1.  The erythropoietin  resistance  index  was  10.7  ± 8.8 IU/kg/week/g/dL,  with  a  mean  haemoglobin  value  of 12.9±1.7. Table 1 describes  the characteristics of the  laboratory parameters found in he study.

Characteristics of patients with PVD as compared to healthy subjects

Prevalence of PVD was 39.5%, i.e. 89 of the 220 patients studied

Information  about  the  grade  of  PVD was  collected  from 212 patients. Of these, 89 patients had PVD.

The most common clinical sign was intermittent claudication,  seen  in  65  patients  (30%).  In  asymptomatic  patients, PVD  was  diagnosed  using  imaging tests.  Fifteen  patients (6.5%) had ischaemia or ulcers in lower limbs, and 9 patients (3%) showed signs of necrosis.

As regards treatment, 95% received medical treatment, while 1  patient was  treated with  angioplasty  (0.5%),  4 were  treated with bypasses (2%), and 5 underwent amputations (2.5%). All patients undergoing amputations had diabetes mellitus.

A significant  association was  seen  between  patients with PVD and the following variables: age, etiology of renal failure, diabetes mellitus, Charlson comorbidity index, C-reactive protein, albumin, prealbumin, and fibrinogen (table II).

No statistically significant association was  found between the presence of PVD and sex, follow-up time of each patient, time on haemodialysis, and erythropoietin resistance index.

Status at study end, mortality, and associated factors

The study population was followed up for 47 months. At the end of the study, 36.8% of patients continued on haemodialysis, 37.3% had died, 22.7% had undergone a  transplant, and 3.2% had been transferred to another hospital. A higher mortality was seen  in  the group of patients with more  severe PVD, as shown  in  figure 1. Crude mortality  in the  study population was 6%, 18%,  and 24%  at 1, 2,  and 3 years respectively.

Mortality associated to PVD

Forty-eight  of  the  87  patients with  PVD  had  died  (55.2%). Survival  of  patients with  PVD was  significantly  shorter,  as shown by the Kaplan-Meier curve (Figure 2), with a log-rank of 12.42 (p = 0.0004) as compared to subjects with no PVD.

A higher mortality was found among patients with an older age, higher Charlson indices, greater CRP and fibrinogen levels, and low albumin and prealbumin levels. The presence of PVD, advanced age, and low prealbumin levels was independently related to mortality.

With  regard  to  relationship between  treatment  and  status, the patient treated with angioplasty (0.5%) continued on haemodialysis,  while  among  the  4 patients  undergoing  bypass surgery (1.9%), 2 continued on haemodialysis (50%), one had died (25%), and one had received a transplant (25%). Of the 5 patients  undergoing  amputations  (2.5%),  4  had  died  (80%) and one continued on haemodialysis (20%).


The prevalence of PVD in the population on haemodialysis in our study was 40%, which is in the upper normal range reported in the literature (from 17% to 48% depending on the series).1,2 While enrolment criteria in both these studies were similar  to  those used  in our  study,  including personal history, physical examination  findings, and diagnostic  tests,  they  reported that the proportion doubled when diagnostic tests were used as the screening method. The high prevalence of chronic glomerulonephritis and  the  low prevalence of diabetic nephropathy  in  our  population  should  be  noted.  In  our  opinion, this  is related to  the high mortality  in patients with diabetic nephropathy on haemodialysis.

This study has a number of limitations. It was a descriptive, retrospective study, which makes it difficult to determine the incident  cases  of  PVD. A search  for prevalent  cases  could only be made. The  time of diagnosis,  the  time since disease onset, and whether  the condition was present  in prior stages of chronic kidney disease were difficult to establish. All cases of PVD had been documented with  imaging  tests. However, due to the design characteristics, there may be a proportion of asymptomatic patients with silent vascular disease who were not performed imaging tests at revisions. Diagnosis of PVD is therefore difficult and requires objective assessments, mainly in  early disease  stages. Supplemental  tests  are not  routinely performed  in all patients because of  their high costs and no proven benefits.

An analysis of risk factors in patients developing PVD showed that this was associated to both classical risk factors, similar  to  those  of  the  general population,1,3,4,7 and  to  factors unique  to  the  uremic  population. Moreover,  chronic  kidney disease,  together with diabetes mellitus,  is a  risk marker  for PVD occurrence and poor outcomes. Our study showed PVD to be associated to elderly and diabetic patients, but no significant sex association was seen.

Patients on haemodialysis have a number of additional risk factors related  to chronic kidney disease and  to  treatment  itself.1,3 The calcium-phosphorus product increases in early stages of kidney disease, with development of vascular calcifications.  Inflammation  and  malnutrition  also  occur  in  early kidney disease stages, and worsen when replacement therapy is started because proteins and water soluble vitamins are lost in  each  session  and  blood  contact with dialyser membranes also  trigger  an  inflammatory  response with  increased  levels of C-reactive protein and proinflammatory cytokines that stimulate protein catabolism.8 This results in increases in oxidative stress, endothelial dysfunction, and secondary atherosclerosis.9,10 Our study tried to focus on epidemiological, comorbidity, and inflammation data, and significant factors such as smoking,  calcium-phosphorus  product,  or  characteristics  of haemodialysis were therefore not studied. A significant association was found between PVD and  inflammation and malnutrition markers such as C-reactive protein, fibrinogen, and decreased albumin and prealbumin levels A very high proportion of patients on dialysis, higher than 30%, have malnutrition,11 which  has  an  unfavourable  influence  on  survival.12 Among  all  poor  prognostic markers,  plasma  albumin  levels lower  than 4 g/dL were  the  laboratory  finding most  closely associated to risk of mortality. Such association was substantial when  plasma  albumin  levels were  lower  than  3  g/dL.13 One of the main criticisms made to hypoalbuminemia as a determinant of mortality is that it may not only be a marker of malnutrition, but may also  indirectly  indicate an  increase  in circulating volume (haemodilution) or result from a systemic inflammatory  response  (decrease hepatic synthesis).14 Together with serum albumin, a non-specific inflammation marker such as serum levels of C-reactive protein has been related to mortality and morbidity in patients with renal failure.15 Under normal  conditions,  C-reactive protein (CRP)  levels  are  0.2 mg/dL, but may be up to 1 mg/dL in some individuals. Values above 1 mg/dL are  considered  indicative of  clinical  inflammation. Vascular wall inflammation is essential for onset and progression of atherosclerosis  related  to vascular  rarefaction events, replacement of contractile fibres by fibrotic areas, and calcification of the latter.16 The source of this systemic inflammatory response in uremic patients is uncertain, but has been closely  related  to malnutrition and atherosclerotic complications  (malnutrition-  inflammation-atherosclerosis  syndrome [MIA]).17 Results of the F. Caravaca et al study18 show the association between  the malnutrition,  inflammation,  and  atherosclerosis  syndrome  and  uremic  patients  before  dialysis  is started. MIA development may therefore not be fully attributed  to  the  potential  inflammation  triggers  inherent  to  the dialysis procedure  (exposure  to non-biocompatible materials or bacterial toxins in the dialysis fluid) as suggested by some researchers.19 Similarly, uremia severity per se does not appear to explain this association either, since patient populations studied with  the  same  severity  of  renal  failure may  show  a very wide range of C-reactive protein levels. Classification of malnutrition  of  patients  on  dialysis  into  two  types  has  recently been proposed.20 Type 2, associated to other comorbid processes and inflammation, could be the most prevalent and difficult  to  treat  if  no  satisfactory  control  of  the  associated conditions is achieved. One of the most salient findings in the F. Caravaca et al study18 demonstrates the great impact of vascular disease on early mortality on dialysis in the younger population, suggesting  the significance of  rigorous control and prevention of vascular disease  from  the earliest  renal  failure stages.

As  regards  survival,  our  study  showed  that  patients with PVD have a higher mortality rate as compared to disease-free patients, as demonstrated by the Kaplan-Meier curve. Most of our patients were in early disease stages, i.e., with symptoms of  intermittent  claudication.  The  risk  of  death  was  already significantly greater at this stage.2,21

Early  diagnosis  of  PVD may  be  difficult,  as  the  disease may develop in a silent form.2 Savage et al22 found in a study that 75% of 24 patients with stage V chronic kidney disease, but with no clinical signs of PVD, had calcified plaques in the carotid  and  femoral  arteries.  In  addition,  the  standard  diagnostic methods  used  once  symptoms  have  already  occurred may not be helpful due to small vessel calcifications.2,23 In any case,  screening methods  should be implemented at our haemodialysis units to monitor and control the disease, and a segmental pressure study should be performed if distal pulses are absent or routinely in patients with risk factors.

As regards treatment, the low proportion of patients undergoing  interventional  treatment  in our study should be noted: bypass surgery, angioplasty, or amputation were performed in only 5% of patients probably because of late disease diagnosis or a high morbidity making an invasive approach difficult. There are no studies available about whether bypass or angioplasty should be performed. Angioplasty is generally used in cases of intermittent claudication, but bypass is being increasingly  used  at  this  stage  of  disease.2,24-26 A study27 showed  a greater  increase  in overall mortality among patients on haemodialysis  treated with bypass as compared  to  those  treated with angioplasty.

Incidence of  amputation  in  the United States  is  ten  times higher in patients on haemodialysis as compared to the general population.2,28 Diabetes mellitus  is known  to be  the main risk  factor  for amputation  in  the haemodialysis population.29 Male  sex,  a  prior  diagnosis  of  PVD,  systolic  hypertension, and hyperphosphoremia are also predictors of amputation  in the newt two years.30 Special attention must therefore be paid to patients with these characteristics, and an attempt must be made  to  control  or  treat  modifiable  risk  factors.  Since  the mortality rate after amputation is extremely high in the population  on haemodialysis,10,28,31-34 strategies  should  be  implemented  to prevent  amputation,  i.e.  to  slow disease development.31,35,36

In summary, PVD is a common complication in the HD population that is often associated to an inflammatory state and an increased mortality risk. Early diagnosis of PVD by oriented  questioning  or  supplemental  examinations  is  therefore mandatory to start treatment.

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