Clinical validation of glucose pump test (GPT) compared with ultrasound dilution technology in arteriovenous graft surveillance

Alberto Magnasco1, Giuseppe Bacchini2, Antonio Cappello3, Vincenzo La Milia2, Brigida Brezzi1, PierGiorgio Messa1 and Francesco Locatelli2

1 Department of Nephrology and Dialysis, S. Andrea Hospital, La Spezia, Italy and 2 Department of Nephrology and Dialysis, 3 Radiology Unit, A. Manzoni Hospital Lecco, Italy

Correspondence and offprint requests to: Alberto Magnasco, Department of Nephrology and Dialysis, S. Andrea Hospital, La Spezia, Italy, e-mail alberto.magnasco{at}au515.la.spezia.it



   Abstract
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Background. Blood flow (Qa) measurements are an important step in the surveillance protocol of haemodialysis vascular access (VA). The glucose pump test (GPT) is a new test for Qa measurement based on the dilution of a constant glucose infusion. The aim of this study is to verify the clinical accuracy of GPT in a graft surveillance protocol with sequential Qa measurements.

Methods. In 30 chronic haemodialysis patients with graft, we compared monthly sequential Qa measurements performed with GPT in pre-dialysis and the ultrasound dilution technique (HD01 device Transonic Systems Inc., USA) during dialysis. The colour Doppler ultrasonography study (CDU) was our reference standard for the diagnosis of stenosis. The endpoints were the graft thrombosis or PTA treatment.

Results. According to the K/DOQI guidelines we could identify the thrombosis high-risk grafts when Qa was <600 ml/min or <1000 ml/min with a decrease >25% in serial Qa measurements. HD01 yielded 27 of 112 high-risk Qa measurements (21 Qa <600 ml/min; mean 406±145 ml/min; 6 {Delta}Qa >25%; mean 43±7%). In 12 of 27 cases the CDU control did not show haemodynamically significant stenoses (false positive); 15 of 27 cases were confirmed high-risk accesses by CDU and did PTAs (HD01 specificity 86%). GPT yielded 14 of 112 high-risk Qa measurements (8 Qa <600 ml/min; mean 404±135 ml/min; 6 {Delta}Qa >25%; mean 38±8%) and all had severe stenoses and underwent PTA treatments showing a GPT specificity of 100%. The CDU study allowed us to correctly assess the Qa negative cases. HD01 method had 10 false negative cases (treated or clotted grafts with a Qa >600 ml/min and {Delta}Qa <25%) with a sensitivity of 60%, while GPT had 11 false negative cases with a sensitivity of 56%. The diagnostic accuracy tested with the ROC curves was similar with both tests (area under the curve was 0.762 and 0.752 with GPT and ultrasound dilution, respectively; P = 0.985). The diagnostic efficiency (percentage of grafts with agreement between test result and factual situation) was 90 and 80% (P = 0.056) for GPT and HD01, respectively.

Conclusion. Compared with HD01, the GPT had a lower false positive rate and similar diagnostic accuracy and efficiency. The clinical implication is a smaller number of unnecessary, invasive procedures (angiographies or PTAs), without increasing the thrombosis risk. This study has shown that GPT is an accurate, quick and economic test for Qa monitoring.

Keywords: colour Doppler ultrasound; haemodialysis; vascular access; ultrasound dilution technology



   Introduction
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Vascular access (VA) for haemodialysis patients is provided by the use of endogenous (native) or synthetic arteriovenous fistulas (AVF). Maintaining patent VA is a major problem, especially in an aging haemodialysis population with poor vasculature. Once fully matured, AVF rarely clot [1]. In contrast, polytetrafluroethylene (PTFE) grafts show a thrombosis rate of 0.5–2.5 per patient-year [2], resulting in considerable morbidity, frequent hospitalization and even increased mortality. In almost all cases, thrombosis is associated with one or more stenoses, usually located at the venous anastomosis of the graft or in the venous outflow tract. The presence of stenosis results in increased resistance and a subsequent decline in access blood flow (Qa). The pre-emptive treatment of stenosis before thrombosis occurs prolongs the secondary patency of grafts and reduces the need for temporary catethers and patients hospitalization [3]. This is the rationale for monitoring Qa as an early indicator of stenosis [2]. The ideal Qa test should be accurate, simple, fast, well tolerated, safe and possibly economic. Recently, we have presented a new test for Qa measurements [4] based on the dilution of a glucose infusion (glucose pump test, GPT) that is quick, non-invasive, reproducible and inexpensive. Preliminary data have shown a good performance of GPT using an in vitro model of VA, and a good in vivo correlation of single Qa measurements with the ultrasound dilution method (HD01) (Transonic Systems Inc., Itacha, NY, USA) [4].

The aim of this study is to verify the clinical accuracy of GPT in a graft surveillance protocol with sequential repeated Qa measurements in comparison with the HD01 device. The direct morphological and haemodynamic study by colour Doppler ultrasonography (CDU) was the reference standard to confirm the presence and severity of stenosis. Although angiography has long been the ‘gold standard’ in diagnosing vascular stenosis, recently CDU has yielded equivalent results [57], without its invasiveness, risks associated with iodinated contrast and cost. In order to correctly calculate the sensitivity and specificity of Qa results, it needs to assess also the Qa negative cases with the reference standard. CDU is the best choice for this screening assessment because it is safe. In addition, CDU study contemporary performs an accurate morphological study plus haemodynamic measurements, helping in a clinical decision-making [6,810].



   Subjects and methods
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Study plan
After informed consent, we prospectively studied serial Qa measurements in 30 haemodialysis patients with grafts (17 PTFE and 13 mesenteric bovine grafts). Twenty-three out of 30 enrolled patients underwent monthly Qa measurements (4.6±2.2 mean sequential measurements per patient; range 2–9) using the GPT technique immediately before the start of dialysis and the ultrasound velocity dilution test during the first hour of the same session. Seven patients were studied only once for an overall 112 comparisons GPT-HD01. We recorded the blood pressure (MAP) before each Qa measurements using an automated oscillometric cuff method (BP 100, Gambro Lundia, Lund, Sweden).

We followed the current Dialysis Outcomes Quality Initiative (DOQI) guidelines [2] to define grafts at high risk of thrombosis. When Qa measured with GPT or HD01 was below the threshold of 600 ml/min, or under 1000 ml/min with a decrease of >25% in serial Qa measurements ({Delta}Qa), the patients were considered at high risk for thrombosis and promptly referred for CDU study to confirm the presence and severity of stenosis. CDU assessment (see below) was the diagnostic testing and it determined the need to treat or not the stenosis. In all patients we performed a basal CDU repeating it after 3 months from the last Qa measurements to confirm the diagnosis of true negative cases and to calculate the sensitivity and specificity.

GPT protocol
The GPT technique has been described and validated previously [4]. Briefly, it consists of a constant glucose infusion by a syringe pump into the arterial needle. Two blood samples are taken from the venous needle, the first one (basal, C1) before the glucose infusion; the second one (C2) 11 s during the infusion. Knowing the infused glucose concentration (Ci = 10% glucose) and the pump infusion rate (Qi = 1000 ml/h with a pump Asena-GH, Alaris Medical System, Basingstoke, UK) it is possible to calculate the blood flow by the following equation [4]:

1
Qa, access blood flow (ml/min); Qi, constant infusion rate (ml/min); Ci, glucose concentration infused (mg/ml); C1, basal blood glucose concentration (mg/ml); C2, during infusion blood glucose concentration (mg/ml).

When basal C1 glucose was high (>250 mg/dl), or C2 glucose was out of the glucometer range (600 mg/dl with the Accu-Chek Active, Roche Diagnostics GmbH, Mannheim, Germany) GPT was repeated with a lower glucose solution (5% glucose rather than 10%). The single pre-dialysis GPT protocol is the quickest, reducing to the minimum the procedures to the patient, not delaying the start of dialysis session more than a few minutes (total test time 4 min).

Transonic HD01 technique
The technique of ultrasound dilution has been described and validated previously [11].

It uses two reusable clip sensors applied on arterial and venous blood line, connected to a HD01 device. For blood flow measurements, dialyser blood lines are reversed and a temporary recirculation created. Thereafter, 10 ml of isotonic saline are quickly injected into the venous line diluting the blood. After a few seconds, the saline dilutes also the arterial blood line proportionally to the recirculation rate. The HD01 monitor records these changes in ultrasound velocity plotting the dilution curves and calculating the fraction of recirculated blood (R) as ratio between the area under the dilution curves generated by the arterial and venous sensors.

A more detailed explanation of this method can be found elsewhere [11]. HD01 measurements were done in duplicate.

Colour-flow Doppler Ultrasonography
Evaluations of VAs were performed using an ultrasound unit with colour and spectral flow Doppler capability (HDI-5000, ATL Ultrasound Bothell, WA, USA). The VAs were examined with a 10 MHz transducer in the longitudinal and transverse planes with and without colour Doppler. The flow was scanned across the arterial anastomosis, through the entire graft until the central venous system. When a graft showed a visual diameter reduction >50% (corresponding to a 70–75% decrease in the cross-sectional area) confirmed by colour flow imaging and haemodynamic criteria of intra-stenosis elevation of the peak systolic velocity (PSV) in comparison with the pre-stenosis PSV (PSV-intrastenosis >2 PSV-pre-stenosis) [6], the stenosis was considered critical and underwent PTA treatment. The CDU accuracy in treatment decision-making has already been shown [9,10].

Statistical analysis
Data were reported as mean±SD. The two data groups were compared by the paired Student's t-test, significance was set at P<0.05. The relationship between groups was analysed by the Bland–Altman test [12]. The percentage of change in Qa ({Delta}Qa) between the first Qa1 and the following Qai was computed by the formula: {Delta}Qa = 100 x (Qa1 – Qai)/Qa1. When the patients had a PTA or a post-thrombosis surgical revision, we considered the post-treatment Qa as a new first Qa1.

The percentage of change in MAP ({Delta}MAP) was computed similarly.

We summarized the standard deviations of MAPs by pooling the individual (SDi) of the N individual patients (Ni):

2

From the pooled SD we obtained the pooled coefficient of variation (CV = pooled SD/mean) for MAP.

The sensitivity was calculated from the ratio: 100 * true-positive test results/all patients with events.

The specificity was the ratio: 100 * true-negative test results/all patients without any events. Diagnostic accuracy of the predictors (Qa and {Delta}Qa) was tested by plotting sensitivity vs false positive rates (1 – sensitivity) using the ROC curves generated with SPSS for Windows 11.5 (SPSS Inc., Chicago, USA). The area under the ROC curve (AUC) gave the overall predictive accuracy of the test. z test was used to compare AUCs. Finally, the efficiency of the tests in diagnosing high-risk VAs was calculated as percentage of (true-positive + true-negative test results)/all measurements.



   Results
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 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
Basic demographics, co-morbidities and type of VA's are listed in Table 1.


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Table 1. Basic demographic and graft characteristics

 
During the study we had only four thromboses and 21 PTA treatments in 20 patients (one patient had one thrombosis and one PTA; another one had three PTAs and two patients had two PTAs). The mean Qa before these events was 801±390 and 612±351 ml/min for GPT and HD01, respectively. Twelve of 25 positive cases yielded low Qa results with both tests. Another five patients with stenosis were separately identified by one of the blood flow tests (three by HD01, two by GPT; see Table 2 for discordant results). The mean Qa in cases without events (87 Qa measurements) was significantly higher with both methods: 1119±285 and 904±297 ml/min for GPT and HD01, respectively (Figure 1). The high standard deviations of Qa results with both methods showed a wide Qa overlap between grafts with or without events. GPT identified all 87 negative cases while HD01 had 12 low Qa results (HD01 = 518±63 ml/min), which did not show haemodynamically significant stenosis at the CDU assessment. Furthermore, none of these 12 HD01 false-positive cases developed thrombosis in the following clinical observation period (mean 250±134 days; range 150–528 days).


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Table 2. GPT and HD01 discordant cases

 


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Fig. 1. Comparison of Qa results (n = 112; {square}, Qa-HD01; {diamond} Qa-GPT) between grafts with and without events (PTA-thrombosis) showing large overlap although with significantly different mean values (dashes): {checkmark}P = 0.00003 Qa-GPT results in events group vs no events; *P = 0.0001 Qa-HD01 results in events group vs no events; dot line is the K/DOQI cut-off of 600 ml/min.

 
In summary, the GPT showed no false positive case (specificity of 100%) but had 11 false negative cases (sensitivity of 56%) while the HD01 had 12 false positive cases (specificity of 86%) and 10 false negative cases (sensitivity of 60%) (Table 3).


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Table 3. Accuracy of HD01 and GPT in predicting VA outcomes

 
Table 4 shows how sensitivity, specificity and diagnostic efficiency (percentage of grafts with agreement between test results and factual situations) vary with changing Qa or {triangleup}Qa cut-off. The HD01 sensitivities at different Qa levels were higher than GPT but with a worse specificity. Average diagnostic accuracy was better for GPT, especially in serial monitoring protocol considering the double indication of Qa values and Qa variations ({Delta}Qa) as suggested by K/DOQI.


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Table 4. Diagnostic accuracy of GPT and HD01 for different Qa and {Delta}Qa thresholds

 
The ROC curves of GPT and HD01 Qa (Figure 2) and {Delta}Qa (Figure 3) show their accuracy. There was no statistical difference between the AUC of GPT and HD01 showing that the two Qa tests had similar poor diagnostic accuracy.



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Fig. 2. ROC curves show similar accuracies (P = 0.985) of GPT and HD01 Qa results in predicting events (thrombosis or PTA). AUC = area under the curve (±SE); 95% CI = confidence interval.

 


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Fig. 3. ROC curves show similar accuracies (P = 0.812) of GPT and HD01 {Delta}Qa results in predicting events (thrombosis or PTA). AUC = area under the curve (±SE); 95% CI = confidence interval.

 
The mean Qa values of 112 measurements were 1056±331 ml/min (range 193–2479 ml/min) for GPT and 848±327 ml/min (range 155–2095 ml/min) for HD01. The mean difference between the two methods was statistically significant ({Delta}Qa GPT-HD01 = 208±161 ml/min; P<0.0001) but not correlated to their mean (Bland–Altman analysis, r = 0.03; Figure 4) showing that the discrepancy between GPT and HD01 was systematic, independent of Qa values. This result was further confirmed in 12 patients with severe stenosis comparing the {Delta}Qa GPT-HD01 pre- and post-PTA. Also in this subgroup of patients the differences between GPT and HD01 were stable before and after PTA treatments, that is, with and without stenosis (Pre-PTA {Delta}Qa GPT-HD01 = 143±152; post-PTA {Delta}Qa GPT-HD01 = 147±174 ml/min).



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Fig. 4. Bland–Altman plot between GPT and HD01 Qa results (differences against averages). The solid line is the regression line and the dotted lines are the limits of agreement (mean difference±2 SD).

 
For all patients we recorded the MAP before each Qa measurement and found a significant difference between the pre-dialysis MAP = 103.5±12.9 mmHg and the intra-dialysis MAP = 98.9±14.6 mmHg; P<0.001. Finally, in order to verify if the pre-dialysis situation had a more stable MAP rather than during dialysis, we analysed the pooled MAP variations from intra-patient serial measurements (mean 4.6±2.2 sequential measurements for patient; range 2–9), obtaining similar pooled coefficient of variation of MAP (CV of 8.1 and 8.5% in pre- and intra-dialysis, respectively; P = 0.9). This result showed that pre-dialysis was not a more stable haemodynamic condition in comparison with during dialysis, according to other published data [13].



   Discussion
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 
The GPT is a new application of the old dilution principle [14], which was used for VA blood flow measurements in the 1970s [15] and then abandoned because cumbersome.

The GPT novelty consists of using glucose as a blood flow tracer because it is harmless, easy to measure and economic. We had already used glucose as a dialysis recirculation indicator with very good results [16]. Now, using a continuous glucose infusion into the arterial needle and measuring the glucose increase from the venous needle, we can evaluate the inter-needle blood flow. This test has been validated previously in vitro and compared with the HD01 in a small population [4]. This study is the first wide clinical validation for GPT compared with HD01 in serial Qa measurements. The endpoints were thrombosis or PTA treatment identified by CDU diagnosis (see Subjects and methods). Given the low number of events (four thromboses and 21 PTAs) it was impossible to perform a separate analysis for each of the two end-points. The ROC curve analysis showed similar diagnostic accuracy between GPT and HD01, either for absolute Qa value or Qa trend (Figures 2 and 3). GPT had no false positive cases while HD01 had 12 false positive cases (specificity of 100 and 86%, respectively). Both dilution methods had similar sensitivities with 10 and 11 false negative cases for HD01 and GPT, respectively. These patients had a stable Qa >600 ml/min, but showed haemodynamically significant stenosis at CDU study and underwent PTA. The low sensitivity showed with both methods confirms other data in the literature [17,18]. A large number of false positive results given indication for unnecessary, invasive and expensive angiographies. In our study, GPT did not produce any false indication to treat, without underestimating the thrombosis risk (the two tests showed similar number of false negative cases). Reducing the Qa cut-off, the specificity improved while the false negative cases increased. Considering both the predictors (Qa <600 ml/min and {Delta}Qa >25%, as suggested by K/DOQI) the diagnostic efficiency improved, especially with GPT, which showed a reduction of false negative cases. The low diagnostic accuracy (area under the ROC curves less than 0.8) yielded with both Qa methods questions the actual role of blood flow measurements in a surveillance programme. Two randomized controlled studies [19,20] have shown recently no advantage in graft survival between a clinical control group and a blood flow-monitoring group. New protocols have to be studied in order to improve the diagnostic accuracy of surveillance tests and to improve the VA survival. The mean blood flow difference between GPT and HD01 ({Delta}Qa = 208±161 ml/min; P<0.001; n = 112) was systematic, independent on Qa values confirming our previous data [4]. Krivitski has hypothesized that GPT overestimation could vary with the entity and position of graft stenosis [21]. Ram et al. [22] analysed GPT equation using a theoretical electrical circuit simulating the VA model. Their conclusion was that the aspiration of C2 sample could cause an increase in Qa ranging from 62 to 240 ml/min depending on the presence of stenosis. This hypothesis was not confirmed by their observational data showing a strong one-to-one correlation between GPT and HD01 with a mean difference of 83 ml/min, independent of Qa values. In addition, our results showed that GPT discrepancies did not depend on Qa values, or the presence of stenosis (Figure 4). In fact, the pre-PTA grafts had severe venous stenoses almost completely resolved by PTA treatment. In these particular cases, the {triangleup}Qa GPT-HD01 did not change before and after PTA showing that other factors are probably involved. First, dilution methods require complete blood mixing of the indicator and no interference between measured values and measuring procedure. The isotonic saline mixes with blood easier than hypertonic glucose because it is pre-mixed during the intra-blood line flow and then by the high counter-current flow. On the other hand, it has been shown that reversed blood flow offers resistance to normal Qa reducing it up to 10% [23,24]. C2 sample aspiration could interfere with the real Qa because of variations in intra-access pressures. Summarizing, there are several haemodynamic variables (intra-vascular turbolences, peripheral rouleaux formation of red cells with preferential flows) influencing mixing, while different intra-access resistances and VA compliance could modify the effect of C2 sample and reversed blood flow on real Qa. These interferences could explain the high variability of Qa measurements and the wide overlap between grafts with and without events (Figure 1).

Another crucial issue is the difference in time between GPT (pre-dialysis) and HD01 (intra-dialysis) measurements. In our study we have shown a significant decrease in intra-dialysis MAP in comparison with the pre-dialysis ({Delta}MAP 6.4±14.3 mmHg; P<0.001). The data is in agreement with many other published data. For example, Polkinghorne et al. [13] have shown recently that there is a statistically significant reduction in MAP and Qa during a dialysis session ({Delta}MAP 10.4 mmHg; {Delta}Qa 104 ml/min). Ram et al. [22] compared HD01 and GPT in close succession during dialysis using a particular intra-dialysis GPT protocol. They found a good correlation between the two methods, r = 0.905, with less difference between the averages ({Delta}Qa GPT-HD01 = 83 ml/min; n = 33), supporting the hypothesis that the change in time is an important source of this discrepancy.

The GPT procedure does not require skills beyond the normal activities of dialysis staff and it is very quick and little intrusive to the patient. The HD01 technique, however, needs well-trained personnel to handle the blood lines in reverse fashion without contaminating the dialysis circuit. Reversal of dialysis blood lines is not required by GPT, so it can be used at any time during and also out of dialysis.

In conclusion, GPT has been shown to be an accurate quick method to measure and follow the VA blood flow in a surveillance protocol. GPT is a new effective and low cost alternative to the ultrasound dilution technique.



   Acknowledgments
 
This study was presented in part at the 2003 ASN Congress of Nephrology and it was supported in part by Italian Society of Nephrology grant.

Conflict of interest statement. None declared



   References
 Top
 Abstract
 Introduction
 Subjects and methods
 Results
 Discussion
 References
 

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Received for publication: 22.12.03
Accepted in revised form: 31. 3.04





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