Original ArticlesMaintenance Dialysis

Association of Preexisting Arterial Intimal Hyperplasia with Arteriovenous Fistula Outcomes

Michael Allon, Silvio H. Litovsky, Yingying Zhang, Ha Le, Alfred K. Cheung and Yan-Ting Shiu
CJASN September 2018, 13 (9) 1358-1363; DOI: https://doi.org/10.2215/CJN.13431217

Abstract

Background and objectives Preoperative arterial function is associated with arteriovenous fistula (AVF) development. Because arterial pathology may correlate with its function, preexisting arterial intimal hyperplasia may be associated with AVF development.

Design, setting, participants, & measurements Vascular specimens obtained from 125 patients (with minimal 2 mm arterial diameter and 2.5 mm venous diameter) undergoing AVF creation were quantified for arterial intimal hyperplasia, arterial medial fibrosis, arterial microcalcification, and venous intimal hyperplasia. A 6-week postoperative ultrasound quantified AVF diameter, blood flow, and stenosis. Clinical AVF maturation was assessed using a predefined protocol. In a prospective cohort study design, we investigated the association of preexisting arterial intimal hyperplasia with the postoperative AVF diameter, blood flow, stenosis, and clinical maturation failure, after controlling for baseline demographics, comorbidities, and preoperative vein diameter. Additional analyses evaluated whether other vascular pathologies interacted with arterial intimal hyperplasia in affecting AVF outcomes.

Results The median intimal thickness of the native artery was 22.0 μm (interquartile range, 14.8–37.1 μm). The median postoperative AVF diameter was 4.8 (interquartile range, 3.7–6.8) mm, blood flow was 796 (interquartile range, 413–1036) ml/min, and stenosis was present in 37 out of 98 patients with ultrasound data (38%). AVF nonmaturation occurred in 37 out of 125 patients (30%). Preexisting arterial intimal thickness was not significantly associated with AVF blood flow (−12 ml/min; 95% confidence interval [95% CI], −55 to 30 ml/min), diameter (−0.04 mm; 95% CI, −0.21 to 0.14 mm), stenosis (odds ratio, 0.93; 95% CI, 0.75 to 1.14), or clinical maturation failure (odds ratio, 1.07; 95% CI, 0.90 to 1.28), all per 10 μm increase. There was no significant interaction of preexisting arterial intimal thickness and postoperative AVF outcomes with arterial medial fibrosis, arterial microcalcification, or venous intimal hyperplasia.

Conclusions Preexisting arterial intimal hyperplasia is not associated with the 6-week AVF blood flow, diameter or stenosis, or clinical maturation when the preoperative arterial diameter is ≥2 mm.

Introduction

A substantial proportion of newly created arteriovenous fistulas (AVFs) in patients with CKD fail to mature adequately to be used successfully for dialysis (1). AVF maturation requires a progressive increase in its diameter and blood flow during the first few postoperative weeks, which can be quantified by ultrasound (2). Nonmaturing AVFs are frequently found to have a juxta-anastomotic stenosis that may limit access blood flow (3). Although there is a poor correlation between preoperative arterial and venous diameters on AVF outcomes (4), several preexisting vascular pathologies (arterial medial fibrosis, arterial microcalcification, or venous intimal hyperplasia) have been suggested to affect AVF development (5). In contrast, there has been relatively little emphasis on the potential effect of preexisting arterial intimal hyperplasia on AVF outcomes. It is plausible that preexisting arterial intimal hyperplasia may directly affect the vascular reactivity of the artery, or indirectly predispose to severe neointimal hyperplasia after AVF creation, leading to flow-limiting juxta-anastomotic stenosis. A small single-center study observed that the presence of preexisting intimal hyperplasia in the radial artery was associated with early clinical failure of radiocephalic AVFs, but did not address early sonographic changes (6).

The primary goal of this study was to determine, in a large cohort of patients with CKD undergoing AVF creation, whether the magnitude of arterial intimal thickness in the native artery is associated with postoperative AVF diameter, blood flow, stenosis, or clinical maturation. A second goal was to investigate whether arterial intimal thickness interacts with other preexisting vascular pathologies (arterial medial fibrosis, arterial microcalcification, or venous intimal hyperplasia) to affect AVF outcomes. This study is important because although preexisting venous intimal hyperplasia had long been postulated to affect AVF outcomes negatively, several recent and large clinical studies found no association between preexisting venous intimal hyperplasia and AVF outcomes (7–9). Whether preexisting arterial intimal hyperplasia has any role in AVF outcomes is not yet completely clear.

Materials and Methods

Overview of Study Protocol

This study prospectively enrolled patients with CKD followed at the University of Alabama at Birmingham who were scheduled for surgical creation of a new AVF for dialysis between October 2008 and April 2012, as previously described (10). None of these patients were enrolled in the National Institutes of Health–funded, multicenter Hemodialysis Fistula Maturation (HFM) Study. Four experienced transplant surgeons created the AVFs. Standardized preoperative sonographic vascular mapping was performed to assist the surgeons in planning the AVF surgery (11,12). Our protocol required a minimal 2 mm diameter of the artery and 2.5 mm of the vein, as well as the absence of stenosis or thrombosis in the draining vein. At the time of their preoperative visit, the patients were invited to participate in a clinical study protocol approved by the local Institutional Review Board. Among patients consenting to the study, the surgeon obtained small specimens of the artery and vein at the time of AVF creation. These were immediately fixed in formaldehyde for subsequent histologic studies.

The patients underwent standardized ultrasounds of their AVFs 6 weeks postoperatively, which quantified the AVF diameter and blood flow and detected the presence or absence of a juxta-anastomotic stenosis (13). The University of Alabama at Birmingham postoperative ultrasound protocol has been validated extensively, and was the one adopted by the HFM Study (2). Patient follow-up was ascertained through March 2014. Clinical AVF maturation was defined prospectively as the ability to use the AVF reproducibly with a dialysis blood flow ≥300 ml/min on at least six dialysis sessions over a 4-week period within 6 months after AVF creation (14). If the patient had not yet started dialysis, AVF maturation was determined in the first month after initiation. Patient comorbidities were ascertained from the electronic medical records by a single experienced clinical nephrologist (M.A.).

Histologic Studies

The vascular specimens obtained at AVF surgery were subjected to a number of stains to quantify various pathologies. The hematoxylin and eosin stain was used to quantify the maximal intimal thickness. The Masson trichrome stain was used to quantify medial fibrosis. It stains collagen blue, and medial fibrosis was quantified as the proportion of total media staining blue using the Bioquant system. The von Kossa stain was used to quantify microcalcification. It stains calcium black, and calcification was quantified as the proportion of total media staining black also by the Bioquant system. All histologic quantifications were performed by a single pathologist (S.H.L.), who was blinded to the clinical characteristics of the study patients and to AVF outcomes.

Statistical Analyses

The study cohort included a total of 125 patients, of whom 43 patients had at least one missing value in one of the following variables: preoperative vein diameter (n=7), arterial intimal thickness (n=13), postoperative AVF diameter (n=28), and postoperative AVF blood flow (n=27). Multiple imputation was performed to impute the indicated missing values using the Markov chain Monte Carlo method under the assumption that the variables with missing data followed a multivariable normal distribution. In total, ten imputed datasets were created. The imputation model included the following variables: arterial medial fibrosis, age, sex, race, diabetes, hypertension, coronary artery disease, peripheral vascular disease, cerebrovascular disease, and congestive heart failure. The imputed postoperative AVF diameter and blood flow rate were set to missing after imputation if they were missing as a result of early AVF thrombosis (within 6 weeks of creation) because they were viewed as structurally missing.

Linear regressions were performed to investigate the association of postoperative AVF diameter and blood flow separately with arterial intimal thickness. Logistic regressions were performed to investigate the association of postoperative AVF stenosis and AVF nonmaturation separately with arterial intimal thickness. Separate models were performed without adjustment and with adjustment for age, sex, race, diabetes, hypertension, coronary artery disease, peripheral vascular disease, cerebrovascular disease, heart failure, and preoperative vein diameter.

To investigate whether there is any interaction between arterial intimal thickness and other vascular pathologies (arterial medial fibrosis, arterial microcalcification, or venous intimal thickness) in determining AVF outcomes, a multiplication term (i.e., arterial intimal thickness×arterial medial fibrosis, arterial microcalcification, or venous intimal thickness) was included together with both continuous individual variables in each unadjusted regression. Linear regressions were used to explore whether there is any association between arterial intimal thickness and other vascular pathologies (arterial medial fibrosis, arterial microcalcification, and venous intimal thickness). The interaction term was tested in the overall group.

Data were analyzed using appropriate procedures in Stata 15 (StataCorp. 2017; Stata Statistical Software: Release 15; StataCorp., College Station, TX). P values were two-sided, with P<0.05 considered significant.

Results

Clinical Features of the Study Population

The study flow is summarized in Figure 1. We invited 245 patients scheduled for AVF creation to participate in the study, and 216 were enrolled. After excluding participants who received an AVG rather than an AVF, those in whom vascular tissue was not obtained during AVF surgery, and patients in whom clinical AVF outcome was unknown because of early death or relocation to a nonparticipating dialysis unit, we were left with 125 participants, who comprised the study cohort.

Figure 1.
Figure 1.

Flow of the participants enrolled in a prospective study of AVF maturation. AVG, arteriovenous graft; Postop US, postoperative ultrasound; Vasc., vascular.

The clinical characteristics of this study population are summarized in Table 1. In brief, the mean age was 53 years, 46% were women, and 67% were black. Comorbidities included diabetes in 49%, hypertension in 90%, coronary artery disease in 13%, peripheral artery disease in 10%, cerebrovascular disease in 10%, and congestive heart failure in 17%. Nearly 60% of the patients had initiated maintenance dialysis before AVF creation, and 37 patients (30%) had a prior nonmaturing AVF. Approximately two thirds of the AVFs were placed in the upper arm. The preoperative and postoperative ultrasound measurements, as well as the vascular histology measurements, are also displayed in Table 1. The median intimal thickness of the native artery was 22.0 μm (interquartile range [IQR], 14.8–37.1 μm).

View this table:
Table 1.

Baseline clinical, sonographic, and histologic features of the 125 participants enrolled in a prospective study of AVF maturation

Figure 2 illustrates the distribution of arterial intimal thickness in the study population. Representative images of an artery with mild and severe arterial intimal hyperplasia are presented in Figure 3. Although it has been reported that diabetes is an independent predictor of in-stent restenosis in coronary arteries because of exaggerated intimal proliferation (15,16) and arterial intimal hyperplasia increases with age in patients without CKD (17,18), we found that arterial intimal thickness was not associated with diabetes (P=0.39) and increased age (P=0.89). Arterial intimal thickness also was not associated with any other comorbidities or sex. Furthermore, arterial intimal thickness was not associated with preoperative artery diameter, after adjusted for location of access (−4.20 μm [−10.69, 2.29] per 1 mm increase in preoperative arterial diameter).

Figure 2.
Figure 2.

Distribution of intimal thickness in preoperative arterial samples.

Figure 3.
Figure 3.

Representative images of an artery with mild and severe intimal hyperplasia (IH). Hematoxylin and eosin stain shows (A) an artery with significant IH and (B) an artery with mild IH from patients receiving arteriovenous fistula creation surgery. (C and D) Masson trichrome stain of these samples shows their respective internal elastic lamina.

Postoperative AVF Outcomes

Clinical nonmaturation was observed in 37 out of 125 AVFs (30%). The proportion of patients with nonmaturing AVFs did not differ significantly among the four participating surgeons (21%, 26%, 30%, and 36%, respectively; P=0.63). Postoperative ultrasounds were not done in 13 patients with early AVF thrombosis and in 14 patients who missed their appointment. Among the remaining 98 participants, the postoperative AVF ultrasound revealed a median AVF diameter of 4.8 (IQR, 3.7–6.8) mm, a blood flow of 796 (IQR, 413–1036) ml/min, and stenosis in 37 participants (38%).

Correlation of Arterial Intimal Thickness with AVF Outcomes

In the statistical analysis adjusted for patient demographics, comorbidities, and preoperative vein diameter, the preexisting arterial intimal thickness was not significantly associated with the 6-week AVF blood flow (−12 ml/min; 95% confidence interval [95% CI], −55 to 30 ml/min per 10 μm increase) or AVF diameter (−0.04 mm; 95% CI, −0.21 to 0.14 mm per 10 μm increase) (Table 2). Similarly, the preexisting arterial intimal thickness was not associated with the likelihood of AVF stenosis (odds ratio, 0.93; 95% CI, 0.75 to 1.14 per 10 μm increase) or clinical AVF maturation failure (odds ratio, 1.07; 95% CI, 0.90 to 1.28 per 10 μm increase). We performed sensitivity analysis of the results including only patients with available outcome data and excluding patients for whom the outcome was imputed. The clinical characteristics of this subpopulation are summarized in Supplemental Table 1. Results of the sensitivity analysis (Supplemental Table 2) are very similar to those from analysis with imputation. Considering the somewhat skewed distribution of the arterial intimal thickness, we also used this subpopulation to perform analyses with logarithm transformation and the results (Supplemental Table 3) are similar to those from analysis without logarithm transformation. Finally, we considered the possibility that the influence of preexisting arterial intimal thickness may be more pronounced in patients with smaller presurgery artery. To this end, we performed analyses including only patients with available outcome data and separating them by preoperative arterial diameters (2.0–2.9, 3.0–3.9, and ≥4 mm). The results show no statistically significant association between arterial intimal thickness and AVF outcomes in any arterial diameter subgroup (Supplemental Table 4).

View this table:
Table 2.

Association between preexisting arterial intimal thickness and AVF outcomes

The Combined Interactions of Other Vascular Pathologies with Preoperative Arterial Intimal Hyperplasia and Its Association with AVF Outcomes

There was no significant association of preexisting arterial intimal hyperplasia with arterial medial fibrosis (0.07; −0.29, 0.44; P=0.69), arterial microcalcification (0.04; −1.15, 1.24; P=0.94), or venous intimal hyperplasia (−0.02; −0.16, 0.11; P=0.74). Thus, these four factors are likely independent of each other and we performed additional analyses to investigate whether there was an interaction between arterial intimal hyperplasia and other vascular pathologies in determining postoperative AVF outcomes. These analyses found no statistically significant interactions between arterial intimal hyperplasia and arterial medial fibrosis, arterial calcification, or venous intimal hyperplasia on each of the AVF outcomes (AVF blood flow, diameter, stenosis, or clinical AVF maturation failure) (all P values >0.1). We performed sensitivity analysis of the results including only patients with available outcome data. Results of the sensitivity analysis are very similar to those from analysis with imputation (all P values >0.1). We also used this subpopulation to perform analyses with logarithm transformation and found no statistically signification association (all P values >0.1).

Discussion

Our study found substantial variation among patients in the magnitude of preexisting arterial intimal hyperplasia. However, there was no significant association between the preoperative arterial intimal thickness and postoperative AVF blood flow, diameter, stenosis or clinical AVF maturation failure. Other vascular pathologies (arterial medial fibrosis, arterial microcalcification, and venous intimal hyperplasia) were not significantly associated with arterial intimal hyperplasia, and had no statistically significant interactions with the association of arterial intimal thickness with clinical AVF outcomes.

Although the arterial and venous limbs of an AVF are likely both important in AVF maturation, previous human and animal studies have largely focused on the vein. Indeed, most of the previous clinical research that investigated the possible effect of preexisting vascular pathology on AVF maturation considered only the veins used to create the AVF. To the best of our knowledge, our research team and a team in South Korea (6) were the only two groups to examine the association of arterial pathology with AVF maturation. A previous single-center study by Kim et al. (6) obtained radial artery specimens from 59 South Korean patients undergoing placement of a radiocephalic AVF. They found that arterial intimal thickness was approximately twice as high in patients with early AVF failure, as compared with those without failure. This study included patients receiving forearm and upper arm AVF creation surgery. There was also no association between the preoperative arterial intimal thickness and AVF outcomes when patients with forearm and upper arm AVFs were analyzed separately (data not shown). Why did our results differ from those reported by Kim et al.? There are several notable differences between the two study populations. First, there were substantial demographic differences: the patients in the study by Kim et al. were all Asian, whereas those in this study were black or white. A previous study associated race with differences in arterial function (19). Second, hypertension was present in 90% of the current cohort, as compared with 78% of the cohort in Kim et al., and hypertension is associated with arterial dysfunction (20). Third, to exclude vascular injury before AVF creation as a cause of early AVF failure, the study by Kim et al. excluded patients with a history of central venous cannulation or arterial puncture ipsilateral to the AVF surgical site. In contrast, we did not exclude such patients in the current cohort. Fourth, the study by Kim et al. did not control their analyses for baseline demographics or comorbidities, which may themselves be associated with arterial intimal hyperplasia in the Asian population. In contrast, our study adjusted all analyses for patient demographics and comorbidities. Fifth, our protocol precluded use of arteries with diameters <2 mm for AVF creation. It is possible that preexisting intimal hyperplasia may have a deleterious effect on AVF outcomes only when the preoperative diameter is smaller. The study by Kim et al. did not specify the preoperative radial diameters used to create AVF; to the extent that the study included participants with arterial diameter smaller than 2 mm, this may explain the discrepancy between our findings and those of Kim et al.

We have previously reported that arterial microcalcification was marginally associated AVF nonmaturation (P=0.08) (14), and arterial medial fibrosis was positively associated with 6-week AVF diameter and flow rate and a lower risk of clinical maturation failure (10). A previous large multicenter and prospective study has also associated preoperative arterial function with postoperative AVF diameter and blood flow (21). In this study, we found no association of preexisting arterial intimal hyperplasia with arterial microcalcification or arterial medial fibrosis, likely because of different underlying pathobiological mechanisms. Because AVF outcomes were not associated with the combination of preexisting arterial intimal hyperplasia with either micro-calcification or medial fibrosis, the distinctive pathobiological mechanisms underlying intimal hyperplasia, medial fibrosis, and microcalcification do not appear to have additive effects on AVF maturation.

Three previous studies have reported a lack of association between preoperative venous intimal hyperplasia and clinical AVF outcomes (7–9). Our study similarly found no association between preexisting arterial intimal hyperplasia and AVF outcomes. Neointimal hyperplasia is commonly observed after AVF creation (8,14,22), and is thought to contribute to AVF maturation failure (23). The dissociation between preexisting vascular intimal hyperplasia and the neointimal hyperplasia observed postoperatively suggests that these two pathologies are mediated by different cellular mechanisms. Preexisting intimal hyperplasia may reflect vascular health, and intimal hyperplasia naturally occur as a result of aging (17,18). In contrast, the formation of postsurgery neointimal hyperplasia may be induced by surgery-associated injury/inflammation and the extremely high and aberrant AVF blood flow (24).

Strengths of this study include prospective data collection, a relatively large patient population, standardized postoperative ultrasound technique, prespecified definitions of clinical AVF maturation, and blinding of the pathologist to the clinical features and AVF outcomes. Additionally, although the study by Kim et al. and our study both focused on the role of arterial intimal thickness in AVF maturation, the study by Kim et al. evaluated only clinical AVF maturation (6) whereas we also included intermediate steps preceding clinical maturation, including the 6-week postoperative AVF blood flow, diameter, and stenosis. We also considered vascular pathologies more broadly, beyond arterial intimal hyperplasia in the Kim et al. study.

This study also has some weaknesses. First, it was a single-center study, and the results may not generalize to some dialysis centers. Second, the intimal thickness may vary along the length of the artery, and the thickness measured in the small specimens may not be representative of the thickness at other locations. Third, a single pathologist quantified all of the histologic abnormalities, and the reproducibility of these measurements is unknown. Fourth, the multiple imputation of missing values may have limited our ability to identify associations of vascular histology with AVF outcomes. However, the results were quite similar in a sensitivity analysis that excluded missing values. Finally, the relatively small study population limited our statistical power to detect interactions.

In conclusion, preexisting arterial intimal hyperplasia is not associated with postoperative changes in the AVF when the preoperative arterial diameter is ≥2 mm. Additionally, the combination of arterial intimal thickness and other vascular pathologies was also not associated with AVF outcomes. This finding suggests that the magnitude of arterial intimal hyperplasia does not correlate with the vascular reactivity of the artery.

Disclosures

M.A. is a consultant for CorMedix. A.K.C. was a member of the Data and Safety Monitoring Board for a trial on vascular graft cosponsored by Humacyte, Inc. and the National Heart, Lung, and Blood Institute, as well as a member of the Clinical Events Committee and Data Safety and Monitoring Board for the Novel Endovascular Access Trial sponsored by TVA Medical, Inc.

Acknowledgments

This study was supported by the National Institute of Diabetes, Digestive, and Kidney Diseases (NIDDK) grants R01DK085027 to M.A. and R01DK100505 to Y.-T.S. We also acknowledge the statistical assistance from the University of Utah Study Design and Biostatistics Center, with funding, in part, from the US National Center for Research Resources and the National Center for Advancing Translational Sciences, National Institutes of Health grant 8UL1TR000105 (formerly UL1RR025764).

Footnotes

  • Received December 3, 2017.
  • Accepted June 18, 2018.

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Association of Preexisting Arterial Intimal Hyperplasia with Arteriovenous Fistula Outcomes
Michael Allon, Silvio H. Litovsky, Yingying Zhang, Ha Le, Alfred K. Cheung, Yan-Ting Shiu
CJASN Sep 2018, 13 (9) 1358-1363; DOI: 10.2215/CJN.13431217
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