Published online before print November 8, 2007, 10.1148/radiol.2463061942
(Radiology 2008;246:299-305.)
© RSNA, 2007
Clinically Immature Arteriovenous Hemodialysis Fistulas: Effect of US on Salvage1
Prabhleen Singh, MD,
Michelle L. Robbin, MD,
Mark E. Lockhart, MD, MPH, and
Michael Allon, MD
1 From the Division of Nephrology and Hypertension, University of California San Diego, VA Health Care System, San Diego, Calif (P.S.); and Division of Nephrology (M.A.) and Department of Radiology (M.L.R., M.E.L.), University of Alabama at Birmingham, 619 19th St South, JTN350, Birmingham, AL 35249-6830. Received November 14, 2006; revision requested Januaury 17, 2007; revision received February 23; accepted March 21; final version accepted May 1. M.A. supported in part by grant 1 K24 DK59818-01 from the National Institute of Diabetes and Digestive and Kidney Diseases.
Address correspondence to M.L.R. (e-mail: mrobbin{at}uabmc.edu).
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ABSTRACT
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Purpose: To retrospectively determine whether postoperative ultrasonography (US) of clinically immature dialysis fistulas can be used to identify potential anatomic origins of immaturity and whether correction of immature fistulas promotes fistula maturation.
Materials and Methods: Institutional review board approval was obtained for this retrospective study, with waiver of informed consent. Postoperative US was performed in 95 consecutive subjects (52 men, 43 women; mean age, 58 years) with clinically immature fistulas. Fistulas were deemed sonographically mature if they had a diameter of at least 4 mm, an access flow of at least 500 mL/min, and a depth of no more than 5 mm from the skin surface. Fistulas were deemed clinically mature if they could be used for dialysis for at least 1 month. The proportion of subjects in different US subgroups with fistulas that matured during follow-up was compared with 
2 analysis.
Results: Sixty-seven clinically immature fistulas were deemed sonographically immature. One or more remediable anatomic problems were detected with US in 60 subjects with sonographically immature fistulas; these problems included focal stenosis in 23, accessory veins in 34, and excessively deep veins in 19. Multiple abnormalities were present in 13 subjects. Of 58 subjects with sonographically immature fistulas and known clinical outcomes, 32 underwent an intervention. In those subjects who did not undergo a salvage procedure, only eight fistulas were usable for dialysis. Among those who underwent a salvage procedure, 25 fistulas were subsequently usable for dialysis (P < .001).
Conclusion: Clinically immature fistulas frequently have one or more potentially remediable problems seen at postoperative US. Problem-specific salvage procedures increase the proportion of fistulas that are usable for dialysis.
© RSNA, 2007
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INTRODUCTION
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Arteriovenous fistulas are the preferred vascular access site for hemodialysis (1). Mature fistulas require far fewer interventions to maintain their long-term patency for dialysis than do arteriovenous grafts (2). There has been a concerted initiative (Fistula First) to increase the proportion of patients who undergo dialysis with a fistula (3). Routine preoperative ultrasonographic (US) vascular mapping has been shown to increase substantially the proportion of patients in whom a fistula is created (4–7). However, 20%–50% of new fistulas are never usable for dialysis owing to failure to mature, despite the use of routine preoperative vascular mapping (4–6).
To allow successful dialysis, a fistula must have both an adequate diameter for safe cannulation and sufficient blood flow to permit adequate blood circulation through the dialysis circuit. An increase in the diameter and blood flow of the draining vein occurs rapidly after fistula creation and is maximal within a few weeks (8,9). Postoperative US measurement of the blood flow and fistula diameter is helpful in predicting the likelihood of successful cannulation for dialysis. Specifically, a draining vein diameter smaller than 4 mm and a blood flow of less than 500 mL/min indicated a fistula that was unlikely to mature in two-thirds of subjects (10).
Failure to mature may result from one or more anatomic problems (2). First, there may be a stenosis at or near the arteriovenous anastomosis that impairs blood flow into the draining vein. Second, the presence of one or more accessory veins branching off of the main draining vein near the arterial anastomosis may result in the redirection of a portion of the fistula blood flow out of the main draining vein. A blood flow of approximately 500 mL/min in the main draining vein is needed for a functional fistula, with 350 mL/min of blood flow withdrawn at hemodialysis and 100–150 mL/min of blood flow needed to keep the fistula patent. Finally, the draining vein may be located too deep within the subcutaneous tissues to allow safe cannulation. Each of these problems can be remedied with an imaging or surgical intervention. Specifically, stenosis may be treated with angioplasty or surgical revision, accessory veins can be ligated, and excessively deep fistulas can be surgically placed in the more superficial soft tissues (11). With correction of an underlying anatomic problem, an immature fistula may be converted into a fistula that can be used for dialysis (12–16).
It is less clear in the published literature (a) how often postoperative US depicts a potentially remediable problem in a clinically immature fistula and (b) how treatment of a sonographically identified problem affects the rate of successful salvage of immature fistulas. Thus, the goal of our study was to retrospectively determine whether postoperative US of clinically immature dialysis fistulas can be used to identify potential anatomic origins of immaturity and whether correction of immature fistulas promotes fistula maturation.
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MATERIALS AND METHODS
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Patients
Institutional review board approval was obtained for this Health Insurance Portability and Accountability Act–compliant retrospective study, with waiver of informed consent. A computerized vascular access database maintained by dialysis access coordinators (17) was used to retrospectively obtain a comprehensive list of all new arteriovenous fistulas created during the 2-year period between January 1, 2002, and December 31, 2003, at a hemodialysis center. During the study period, 95 consecutive subjects (52 men, 43 women; mean age, 58 years ± 13 [standard deviation]; range, 21–85 years) underwent postoperative US to evaluate a clinically immature upper extremity fistula. If more than one fistula was created in a subject during the study period, only the first fistula was included. The access database was used to collect information about specific fistula events or interventions, race, and the presence of diabetes or peripheral vascular disease. Two authors (P.S., M.A.) searched the database and collected information.
All subjects underwent routine preoperative US vascular mapping with HDI 3000 or HDI 5000 (Philips Ultrasound, Bothell, Wash) or Sequoia (Siemens Ultrasound, Mountain View, Calif) US machines operated by registered diagnostic medical sonographers (some were also registered vascular technologists) in an American College of Radiology–accredited laboratory to assess vessel diameter and exclude vein stenosis or thrombosis (2,4,18). The sonographers had 3–15 years of experience (average, 7 years). The US protocol required a minimum arterial diameter of 2.0 mm and a minimum venous diameter of 2.5 mm. Fistulas were initially cannulated 8–12 weeks after they were created, provided they were deemed adequately mature at clinical assessment.
The dialysis nurses attempted fistula cannulation on the basis of their clinical judgment, without relying on postoperative imaging results. If the surgeon, nephrologist, or dialysis nurse believed that the fistula was clinically immature, the subject was referred for postoperative US assessment of the fistula. Subjects with a sonographically immature fistula and a remediable anatomic problem diagnosed at US were referred for corrective radiologic or surgical interventions. The salvage procedures included angioplasty or surgical revision of a stenotic problem, ligation of one or more large accessory veins, or surgical placement of draining veins that were too deep to be cannulated safely in a more superficial location. Stenotic problems were treated initially with angioplasty or surgical revision of the fistula at the discretion of the surgeon. Twelve patients in whom postoperative US revealed an immature fistula with severe stenosis underwent an intervention to correct the problem at the discretion of the surgeon. Two patients with fistulas underwent angioplasty. Angioplasty was successful in one patient; however, it was unsuccessful in the other and was followed by surgical revision. The other 10 patients underwent surgical revision directly (ie, creation of a new native anastomosis at a more proximal site or placement of a bypass graft around the anastomosis). Accessory veins and fistulas that were too deep always were treated surgically.
Clinical Definition of Fistula Immaturity and Fistula Outcomes
A clinically immature fistula was defined as a fistula having one or more of the following characteristics, as determined at physical examination by the dialysis nurse, nephrologist, or surgeon: (a) small-caliber vein at palpation, such that it would be difficult to cannulate the vein with a 17-gauge dialysis needle; (b) less than 10 cm of palpable or visible draining vein length to allow cannulation with two dialysis needles, with adequate separation to minimize recirculation; and (c) vein located too deep to cannulate safely with a 2.5-cm dialysis needle (2,10).
The reference standard for clinical outcomes of new fistulas was defined on the basis of use for dialysis (2). A fistula may appear to be adequate at inspection, palpation, and auscultation; however, unless it can be used to perform dialysis thrice weekly, it is not considered successful. Fistulas were considered adequate for dialysis if they were cannulated successfully within 6 months of their creation for dialysis with two needles over a period of at least 1 month (19). Fistulas were deemed to have failed to mature if they were unusable for dialysis within 6 months of creation. The fistula outcome was considered indeterminate if the subject had not yet started dialysis at the time of data analysis (n = 10), if the subject died (n = 3), or if the subject was lost to follow-up before initiation of dialysis (n = 2). The 15 patients with indeterminate fistula outcomes included six with sonographically mature fistulas and nine with immature fistulas. Thus, fistula outcomes were determined in 80 patients who underwent postoperative US.
Postoperative US Evaluation of Arteriovenous Fistulas
Clinically immature fistulas were evaluated with either an HDI 3000 or an HDI 5000 US scanner (Philips Ultrasound) in the same American College of Radiology–accredited laboratory where preoperative mapping was performed. Data collection was based on information found in the reports. All fistula US scans were performed 20–483 days (mean, 99 days ± 88) after fistula creation, and one of 10 board-certified radiologists with special interest and training in vascular US (M.L.R., M.E.L.) and 4–28 years of experience (average, 13 years) interpreted images on the day of the US examination. Information pertaining to the initial surgery performed to create the fistula and any other pertinent angiographic or clinical history was available to the radiologist when the fistula US images were interpreted. After surgical creation, no angiograms of these fistulas were obtained prior to US. A high-frequency (9–14-Hz) linear transducer with an angle of insonation no larger than 60° was used to evaluate the fistula with use of both gray-scale and color Doppler techniques and a standard protocol (10).
Briefly, abundant gel and minimal pressure on the skin from the transducer were used to minimize vessel deformation. The largest anteroposterior diameter of the draining vein was measured in the transverse dimension, even if the vessel was not perfectly round. It should be noted that the vein wall usually does not have a perceptible thickness, so neither the outer nor the inner diameter was usually perceived or measured. Thus, the diameter of the vein was measured by placing the cursors on (within) the opposing vein walls (Fig 1). The distance of the draining vein from the skin was measured from the skin surface to the anterior vein wall. Both the vein diameter and the distance to the skin surface were measured at three locations in the forearm for a forearm fistula or at three locations in the arm for an arm fistula.
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Figure 1: Normal diameter fistula. Transverse gray-scale image of draining vein shows adequate 6.6-mm diameter for hemodialysis (crosshairs). The depth (x) is 4.8 mm, which is less than the 5.0-mm threshold.
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All veins branching off the main draining vein of the fistula within the first 10 cm of the anastomosis (the usual length of fistula used for the two needles used during hemodialysis) were identified. The distance of the vein branch(es) from the anastomosis was measured, and the anteroposterior dimension of the branch(es) was measured at the takeoff from the main draining vein (Fig 2). To calculate flow volume, the flow velocity profile across the fistula diameter was obtained, the diameter was measured, and the flow volume was calculated with the US scanner (HDI 3000 or HDI 5000) by using an average of three cardiac cycles. The flow volume was measured three to five times in a vein segment with a constant diameter above any accessory branches, and the average was calculated. A straight segment of vein was necessary for flow volume measurement, so the distance from the anastomosis varied. For peak systolic velocity, each measurement was determined from one representative waveform.
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Figure 2: Accessory vein. Transverse gray-scale image of draining vein shows a large accessory vein (crosshairs), which may limit maturation of the fistula for dialysis by sumping blood flow from the draining vein.
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A fistula was deemed sonographically mature if it met the following three predetermined criteria: the minimal diameter was at least 4 mm, the access blood flow was at least 500 mL/min, and the distance from the skin was no less than 5 mm (10). If any criterion was not met, the fistula was considered sonographically immature (Figs 2, 3). Additional parameters assessed at US included the presence of juxtaanastomotic and draining vein stenoses. Morphologic narrowing was identified by following the vein longitudinally with color Doppler US to identify visual narrowing of more than 50% or turbulent flow, which suggests potential sites of stenosis. Criteria for stenosis of 50% or more were visual narrowing and (a) a peak systolic velocity ratio of at least 3:1 at or within 2 cm of the arteriovenous anastomosis, as determined by using the maximal peak systolic velocity at or distal to the stenosis compared with the peak systolic velocity 2 cm proximal to the anastomosis in the feeding artery, or (b) a peak systolic velocity ratio of at least 2:1 at a draining vein stenosis (20).
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Figure 3a: Immature fistula. (a) Transverse gray-scale image of draining vein (crosshairs) shows the vein is too small and too deep for consistent cannulation at hemodialysis. (b) Longitudinal spectral Doppler US image with volume flow calculation demonstrates slow flow, consistent with fistula immaturity.
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Figure 3b: Immature fistula. (a) Transverse gray-scale image of draining vein (crosshairs) shows the vein is too small and too deep for consistent cannulation at hemodialysis. (b) Longitudinal spectral Doppler US image with volume flow calculation demonstrates slow flow, consistent with fistula immaturity.
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Statistical Analyses
An author (M.A.) performed statistical analyses with statistical software (GraphPad Prism 4, version 4.0a, May 2003; GraphPad Software, San Diego, Calif). We determined the demographic and clinical characteristics of all 95 subjects who underwent postoperative US for evaluation of a clinically immature fistula. For the subset of subjects in whom fistulas were sonographically immature, we recorded the fistula diameter, flow rate, and presence of potentially remediable anatomic defects (stenosis, accessory veins, or excessive depth [>5 mm from the skin]). We also documented those subjects in whom US revealed more than one coexisting anatomic problem. Subjects with sonographically immature fistulas were divided into two groups: those with a forearm fistula and those with an arm fistula. These two groups were compared in terms of frequency of subthreshold diameter, flow rate, and frequency of potentially remediable anatomic defects by using the 2 test.
We first compared the clinical outcomes (usability for dialysis) between subjects with sonographically mature fistulas and those with sonographically immature fistulas. The 2 test was then used to compare the frequency of fistulas that were subsequently usable for dialysis between patients with immature fistulas who underwent an intervention and those with immature fistulas who did not undergo an intervention. Additional subset analysis was performed with the 2 test to compare the frequency of usable fistulas among subjects with fistulas having specific anatomic abnormalities (stenosis, accessory veins, or excessively deep) who did or did not undergo a salvage procedure. A P value of less than .05 was considered to indicate a significant difference.
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RESULTS
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Subject Characteristics
The majority of subjects in this study were black, reflecting the racial composition of the dialysis population (Table 1). One-third of the subjects were aged 65 years or older. More than half the subjects had diabetes, and 13 (14%) had documented peripheral vascular disease. A similar number of fistulas were located in the forearm (n = 49) and arm (n = 46) (Table 1).
US Findings in Immature Fistulas
Twenty-eight (29%) of the 95 fistulas were considered sonographically mature and 67 (71%) were deemed sonographically immature with the predetermined US criteria. Reasons for failure to mature included stenosis, accessory veins, and inaccessibility owing to vein depth from the skin (Table 2). In the 67 sonographically immature fistulas, a stenosis was seen in 23 (34%), accessory veins were seen in 34 (51%), and a deep vein was seen in 19 (28%). The sum of frequencies for all three categories was more than 100% because nearly 20% of subjects had more than one anatomic problem seen at US. In seven (10%) immature fistulas, no specific anatomic problem was found to explain the lack of maturation. These fistulas were considered unsalvageable, but they were not evaluated with angiography.
With use of the predetermined definition, a higher proportion of forearm (80% [n = 39]) than arm (61% [n = 28]) fistulas were deemed sonographically immature (Table 3). This difference was primarily due to a higher likelihood of subthreshold vein diameters in the forearm fistulas (68% [n = 24]) than in the arm fistulas (36% [n = 10]). In addition, the frequency of anatomic defects varied between sonographically immature forearm and arm fistulas. Accessory veins were more likely to be found in immature forearm fistulas (67% [n = 26]) than in immature arm fistulas (28% [n = 8]). Conversely, excessively deep veins were a more common finding in arm fistulas (46% [n = 13]) than in forearm fistulas (15% [n = 6]). The frequency of stenotic problems was similar in both types of fistulas (36% [n = 14] and 32% [n = 9] in forearm and arm fistulas, respectively).
Outcome of Salvage Procedures on Fistula Maturation
In the 95 subjects with clinically immature fistulas who underwent postoperative US, 28 (29%) fistulas were deemed sonographically mature. The fistula outcome was indeterminate in six of these subjects (Table 4). In the 22 subjects with sonographically mature fistulas and known clinical outcomes, 20 (91%) fistulas were subsequently usable for dialysis. Among the 67 subjects with sonographically immature fistulas, 40 (60%) underwent a surgical or radiologic procedure to correct the anatomic problem revealed by US. The frequency of a salvage procedure was similar between the immature forearm (56% [n = 22]) and arm (64% [n = 18]) fistulas (P = .52). The remaining 27 (40%) subjects with a sonographically immature fistula refused to undergo an intervention. The proportion of sonographically immature fistulas that were ultimately successfully used for dialysis was similar (P = .90) between the forearm (58% [n = 19]) and arm (56% [n = 14]) fistulas. (In this comparison, nine subjects with indeterminate fistula outcomes were excluded.)
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Table 4. Outcomes of Fistulas Sorted by Postoperative US Category and by Whether Salvage Procedures Were Performed
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Of 26 subjects with fistulas that were deemed immature at US who refused to undergo a salvage procedure, only eight (31%) had a fistula that was subsequently usable for dialysis (P < .001 for comparison with fistulas deemed mature). In contrast, of 32 subjects in whom fistulas were deemed immature at postoperative US who underwent a surgical or radiologic salvage procedure, 25 (78%) had fistulas that subsequently were used successfully for dialysis (P < .001 for comparison with patients with immature fistulas who did not undergo a salvage procedure). Moreover, interventions to correct an underlying problem were associated with a higher fistula success rate, regardless of the type of problem observed at postoperative US (Table 5). Specifically, among patients with a known clinical outcome and a documented stenosis, subsequent usability of the fistula for dialysis was achieved in seven (70%) of those who underwent an intervention (angioplasty or surgical revision) compared with none of those who did not undergo an intervention (P = .001). Likewise, among patients with sonographically immature fistulas with an accessory vein treated with surgical ligation, subsequent usability for dialysis was achieved in 15 (83%) of 18 patients compared with four (33%) of 12 patients who did not undergo an intervention (P = .005). Finally, among seven fistulas that were determined to be too deep (>5 mm from the skin) and underwent surgical superficialization, five (71%) were subsequently usable for dialysis compared with two (28%) in subjects who did not undergo an intervention (P = .11).
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Table 5. Outcomes of Sonographically Immature Fistulas Sorted by Type of Anatomic Problem and by Whether an Intervention Was Performed
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DISCUSSION
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In 90% of fistulas considered immature with predefined US criteria in our study, one or more remediable anatomic problems that may have contributed to the fistula immaturity were identified. A subset of the subjects with these fistulas (40 of 67 subjects [60%]) was triaged to the appropriate surgical or radiologic intervention to correct the underlying problem. The success of these salvage procedures is evident from the observation that 25 (78%) of 32 immature fistulas in which such an intervention was performed were subsequently usable for dialysis, as compared with only eight (31%) of 26 immature fistulas in which an intervention was not performed. Moreover, correction of any type of anatomic problem (stenosis, accessory vein, or deep veins) seen at US appeared to improve the success rate of immature fistulas. Seven (22%) of the 32 sonographically immature fistulas failed to mature adequately for dialysis, despite an appropriate problem-specific intervention. Owing to the retrospective nature of our study, the cause of the continued fistula immaturity after intervention could not be determined.
Previous studies have revealed a lower success rate for forearm fistulas than for arm fistulas, despite routine use of preoperative vascular mapping to ensure the adequacy of the vessels used (4,10,11,19). The findings of this study are in keeping with these findings, in that a higher proportion of forearm fistulas than arm fistulas were deemed sonographically immature. However, with aggressive intervention to correct the remediable problems depicted by US, the salvage rate was similar for immature forearm and arm fistulas (58% [19 of 33] vs 56% [14 of 25], respectively).
Postoperative US was performed to evaluate the immature fistulas a mean of 3 months after fistula creation, as the policy at our dialysis center was to wait 2–3 months after fistula creation before attempting cannulation for the first time. It has been previously reported that fistula diameters and blood flow rates are similar in the 2nd, 3rd, and 4th postoperative months (10). This suggests that obtaining postoperative US images of the fistulas at 4–6 weeks could have led to earlier salvage procedures and earlier fistula maturation. This is a subject for future research. In subjects in whom a fistula was created before initiation of dialysis, the delay in obtaining postoperative US images was greater, as there was less frequent medical follow-up and a lower sense of urgency in promoting fistula maturation.
Our study had some limitations. First, the retrospective design may have introduced bias into the interpretation of fistula outcomes since the US findings were available to the surgeon and dialysis team. In other words, the dialysis staff may have been reluctant to cannulate a fistula that was deemed sonographically immature. However, this does not seem to be the case, as one-third of sonographically immature fistulas were used successfully for dialysis, even though the subjects did not undergo a salvage procedure. Second, the US criteria used in the current study have been verified at only our institution and have not been independently confirmed at other dialysis centers.
Third, despite the availability of resources and personnel, 40% of subjects with sonographically immature fistulas with remediable anatomic problems refused to undergo a salvage procedure. Asif et al (14) reported similar numbers, reporting that 45 (37%) of 121 patients who were undergoing catheter-consigned hemodialysis refused to undergo interventions aimed at establishing a functioning fistula.
Fourth, seven (11%) of 67 sonographically immature fistulas without a demonstrable anatomic defect were considered unsalvageable, and a fistulogram was not obtained in these subjects. It is possible that a focal fistula stenosis or a central vein stenosis may have been missed at US in some of these subjects and that correction of the problem might have promoted fistula maturation.
Fifth, the clinical outcome was indeterminate in 15 (16%) subjects in our study, and this could have potentially affected the interpretation of the outcomes. However, given the national guidelines promoting early fistula creation in patients before dialysis (1), it is not uncommon for some patients to die before the need for dialysis arises and for others not to require dialysis for a few years after fistula creation. Given that our definition of clinical fistula success required successful cannulation of the fistula for 1 month, it was unavoidable to have indeterminate clinical outcomes in a minority of subjects.
Sixth, an angiogram was not obtained in all fistulas, and there may have been additional problems in the sonographically mature group. However, it can be argued that stenoses or accessory veins in mature fistulas, if present, are not clinically important. Identification of a stenosis would then be useful only for follow-up for possible progression, which is a topic for future research (21). Seventh, this study represents the experience of one dialysis center, and our results may not generalizable to all dialysis units.
In conclusion, our findings indicate that most immature fistulas have one or more remediable anatomic problems that are demonstrable at postoperative US. Moreover, salvage procedures to correct these defects can substantially increase the proportion of fistulas that are usable for dialysis. Postoperative fistula US may be useful in triaging the subsequent treatment of the immature fistula to the appropriate surgical or interventional service. These preliminary findings need to be validated in future multicenter prospective studies.
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ADVANCES IN KNOWLEDGE
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- US can be used to assess clinically immature arteriovenous dialysis fistulas for potentially correctable causes of immaturity.
- Intervention based on US findings increased the proportion of sonographically immature fistulas that became useable for dialysis from 31% to 78%.
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IMPLICATION FOR PATIENT CARE
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- US can be used to assess clinically immature arteriovenous dialysis fistulas and may enable triage to the appropriate intervention to increase the percentage of fistulas that mature.
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ACKNOWLEDGMENTS
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The authors thank Patricia Thurman for her administrative assistance in preparing this manuscript.
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FOOTNOTES
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Author contributions: Guarantors of integrity of entire study, M.L.R., M.A.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, all authors; clinical studies, all authors; statistical analysis, M.A.; and manuscript editing, all authors
Authors stated no financial relationship to disclose.
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References
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ABSTRACT
INTRODUCTION
