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European Heart Journal Advance Access originally published online on July 5, 2006
European Heart Journal 2006 27(15):1811-1817; doi:10.1093/eurheartj/ehl134
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© The European Society of Cardiology 2006. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

Evaluation of the haemodynamic characteristics of drug-eluting stents at implantation and at follow-up

Marcel van't Veer1,2, Nico H.J. Pijls1,2,*, Wilbert Aarnoudse1,2, Jacques J. Koolen1 and Frans N. van de Vosse2

1 Department of Cardiology, Catharina Hospital, PO Box 1350, 5602 ZA Eindhoven, The Netherlands
2 Department of Biomedical Engineering, Eindhoven University of Technology, Eindhoven, The Netherlands

Received 28 September 2005; revised 15 May 2006; accepted 15 June 2006; online publish-ahead-of-print 5 July 2006.

* Corresponding author. Tel: +31 40 239 7004; fax: +31 40 244 7885. E-mail address: nico.pijls{at}inter.nl.net

See page 1764 for the editorial comment on this article (doi:10.1093/eurheartj/ehi863)


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
Aims The aim of this study was to investigate the physiologic parameters: fractional flow reserve (FFR), hyperaemic trans-stent gradient (HTG), and wall shear stress (WSS) at implantation and at 6-month follow-up in the drug-eluting sirolimus stent and in its bare metal counterpart implanted in pairs within the same patient.

Methods and results Twenty patients, accepted for percutaneous coronary intervention of at least two coronary arteries with comparable vessel and stenosis characteristics, received at random one sirolimus-eluting stent and one bare metal stent (BMS). Coronary pressure, FFR, HTG, and WSS were measured just after stent implantation and at 6-month follow-up. At 6-month follow-up, FFR was significantly higher in the sirolimus group compared with the bare metal group (0.91±0.05 vs. 0.83±0.10, P=0.027) and HTG was significantly lower (1.2±1.2 vs. 7.5±8.1 mmHg, P<0.001). In-stent WSS at 6 months remained normal in the sirolimus group but was elevated in the bare metal group (1.6±0.7 vs 3.9±3.1 Pa, respectively, P=0.003).

Conclusion The physiologic characteristics of the drug-eluting sirolimus stents were superior to those of the equivalent BMS. Six months after implantation, FFR was significantly higher, HTG was significantly lower in arteries treated by a sirolimus stent, and normal WSS was maintained within the drug-eluting stent.

Key Words: Fractional flow reserve • Blood flow • Angioplasty • Coronary disease


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
Drug-eluting stents have been introduced with the prospect of reducing restenosis rate after percutaneous coronary intervention (PCI). However, only anatomical data related to follow-up of these stents are available so far, mostly obtained from intravascular ultrasound (IVUS) and quantitative coronary angiography (QCA).1,2 It has been shown repeatedly that the physiologic parameters: fractional flow reserve (FFR) and hyperaemic trans-stent gradient (HTG) better reflect the physiologic status of a coronary segment or stenosis both in native coronary arteries and after stenting.3–5 Moreover, it has been shown that there exists a relation between the wall shear stress (WSS) and the neointimal thickness.6,7 Therefore, the aim of this study was to investigate FFR, HTG, and WSS at implantation and at 6-month follow-up in the sirolimus stent (CypherTM, Cordis, Johnson & Johnson, Miami, FL, USA) and in its bare metal counterpart (Bx VELOCITYTM), randomly implanted in pairs in two comparable arteries with comparable stenoses within the same patient.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusion
 Acknowledgements
 References
 
Study population
Twenty consecutive patients with stable angina pectoris were selected who were accepted for elective PCI of at least two coronary arteries with a comparable reference diameter and comparable stenosis characteristics. In none of the patients, previous myocardial infarction had occurred in the myocardial regions supplied by the respective arteries.

The reference diameter of both arteries should vary <0.5 mm and the length of the stenosis should not differ more than 50%. Patients with very tortuous vessels, severe obstructive pulmonary disease, as well as patients with a contraindication for aspirin or clopidogrel were excluded. There were no further exclusion criteria.

All patients were selected from the total population referred to our hospital for PCI of 2-vessel disease (Figure 1). Among a total of 228 patients referred for elective 2-vessel PCI, 20 patients fulfilled the criteria of having comparable stenoses with comparable length, severity, and reference diameter.


Figure 1341
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  		Figure 1 Patient flow chart. Twenty consecutive patients fulfilling the study inclusion criteria were selected from the total population of patients referred to our hospital undergoing PCI in the period 1 June 2003 till 3 December 2003.

 
Immediately before the procedure, the placement of the sirolimus stent and the bare metal stent (BMS) in the two stenoses was determined by computer-coded randomization. The study was approved by the institutional review board of the Catharina Hospital and written informed consent was obtained from all patients prior to the study. It should be noted that at the time the study was performed, drug-eluting stents in our country were not available for routine patients, except in studies.

Interventional protocol
All procedures were performed by the femoral approach with 6F guiding catheters. Patients were pretreated with aspirin and clopidogrel. Prior to the procedure 5000 U of heparin was administered. After intra-coronary administration of 300 µg nitroglycerine, coronary angiography was performed. Next, a sensor-tipped pressure guide-wire (PressureWire 4, Radi Medical Systems, Uppsala, Sweden) was used as routine guide wire in all of the procedures and pressure measurements were performed by this wire as described below. After successful stent implantation and repeated measurement of coronary pressures, this pressure wire was replaced by a Doppler flow wire (FloWire, Jomed, Ulestraten, The Netherlands) for velocity measurements and WSS calculations as described below. Post-interventional pharmacologic treatment included aspirin and clopidogrel as routine in our center. All invasive measurements were repeated after 6 months with the same sequence and methodology of all physiologic measurements.

Haemodynamic analysis
After adequate calibrating and positioning the pressure sensor in the distal part of the coronary artery, hyperaemia was induced by intravenous infusion of adenosine through the femoral vein (140 µg/kg.min) as described before.3,8 After steady state maximum hyperaemia had been achieved, FFR was determined as the ratio of distal coronary pressure (Pd) and aortic pressure (Pa). FFR expresses maximal achievable blood flow in the presence of a stenosis as a ratio of normal maximal blood flow in the hypothetical case that the coronary artery would be completely normal.3,8 Adenosine was stopped and the stent was placed. Thereafter, adenosine was started again and post-stent FFR was measured. Subsequently, during sustained hyperaemia, the wire was slowly pulled back under fluoroscopic guidance and a pull-back recording was made.4,8 HTG was calculated as the pressure just proximal to the stent (Pprox) minus the pressure just distal to the stent (Pdist), both determined at maximum coronary hyperaemia. Also, the trans-stent pressure ratio (TPR) was calculated as the ratio of Pdist and Pprox during maximum coronary hyperaemia. Next, adenosine was stopped and the pressure wire was exchanged for a Doppler flow wire and average peak velocity (APV) was measured at the entrance and the exit of the stent and within the body of the stent at rest. An approximation of WSS at different positions was calculated assuming a Poiseuille flow yielding:

Formula 1(1)
where {eta} is the dynamic viscosity of whole blood, Formula 1 represents the average cross-sectional velocity at the particular location, and d the corresponding diameter obtained from the QCA analysis. A venous blood sample was taken before the administration of heparin prior to the initial intervention and prior to the follow-up procedure for the determination of blood viscosity as described by Matrai et al.9 Because of the assumption of a parabolic Poiseuille flow in a circular straight tube, the average velocity Formula 1 was taken half of the measured APV.10 The definitions of the several haemodynamic indices are clarified in Figure 2. Our method is fundamentally the same as used by Wentzel et al.6 and Gijsen et al.7 However, we do not use a finite element model to calculate local WSSs. Our formula is the analytic solution of the Navier–Stokes equations, under the assumptions of an incompressible steady laminar Newtonian flow through a straight tube.


Figure 1342
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  		Figure 2 Definition of the haemodynamic parameters measured in a coronary artery in this study. Pa, Pd, Pprox, and Pdist represent aortic pressure, distal pressure, and pressure just proximal and just distal to the stent, respectively, all measured during maximal hyperaemia. WSS indicates the approximate WSS in the stent, {eta} is the viscosity of whole blood, d is the diameter of the stented vessel, and Formula 1 the average cross-sectional velocity of the blood at a particular location.

 
Angiographic analysis
Angiograms were made after nitroglycerine administration in at least two orthogonal projections and QCA was performed and analysed as described before.11 Reference diameter, percentage diameter stenosis, and minimal luminal diameter (MLD) were calculated offline (QCA-CMS 4.0, MEDIS medical imaging systems, Leiden, The Netherlands) both before and immediately after the procedure, and at the 6-month follow-up period. Late lumen loss was defined as the difference between the post-procedural MLD and the follow-up MLD at 6 months as described earlier.1,2 The diameters of the artery at the entrance of the stent, within the stent, and at the exit of the stent were measured in the two projections, averaged, and then used for the WSS calculations at those positions.

Statistical analysis
The number of 20 patients was arbitrary but based upon the consideration that if a relevant difference between the stents would be present with respect to the haemodynamic indices, this should be demonstrable in this group. Because of the extensive invasive study protocol, it was considered inappropriate to include a larger group of patients.

The design introduces two sources of repeated measures that we considered in the statistical analysis. First, measurements were performed immediately after placing the stents and repeated at follow-up. We calculated the difference between parameters for these time points and compared them across the stent groups. Second, two different stent types were compared within each patient. Therefore, we used the Wilcoxon signed-rank test for paired observations. All tests were performed two-sided. A P-value of <0.05 was considered significant.

In performing statistical tests, no corrections were made with regard to Type I error as the primary outcome of this study was the difference between FFR from immediately after stenting to follow-up. Further tests may be considered as indicative for the difference in the results between the stents. Statistical software package SAS (Version 8.2, SAS Institute, Cary, NC, USA) was used for the statistical analysis.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusion
 Acknowledgements
 References
 
Baseline characteristics and procedural results
All 20 patients eligible for the study consented to participate. Twenty sirolimus stents and 20 BMSs were implanted in pairs in 20 patients. Four patients received an additional stent due to a residual significant pressure gradient elsewhere in the vessel (n=3) or a dissection (n=1). These additional four stents were also drug-eluting stents. No procedural complications occurred.

Patient characteristics are presented in Table 1. Baseline angiographic and haemodynamic characteristics as well as stent characteristics are presented in Table 2. No significant differences were present at baseline between the two groups.


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  		Table 1 Patient characteristics

 

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  		Table 2 Baseline angiographic and pressure data before stent implantation and stent characteristics

 
Clinical follow-up at 6 months
There where no deaths among these 20 patients after 6-month follow-up. Two cases of sub-acute stent-thrombosis occurred: one in sirolimus and one in BMS. These events occurred within the same patient and were possibly provoked by removal of the sheath several hours after the intervention, accompanied by bradycardia and a vasovagal reaction. Both stents were successfully re-opened by re-intervention. The CK-MB level rose to 677 U/L in this patient.

At 6 months, four re-interventions were necessary based upon an ischaemic FFR: two cases of in-stent restenosis and the other two cases because of restenosis just proximal to the stent. All re-interventions were related to the BMS and were all treated by placing a drug-eluting stent within or overlapping the former stent.

Angiographic follow-up at 6 months
Immediately after intervention, the angiographic characteristics of both groups were similar. However, after 6 months, they differed significantly with respect to the MLD, the percentage diameter stenosis, and the late lumen loss in favor of the sirolimus stent (Table 3). The MLD of the sirolimus stent vs. the BMS was 2.3±0.4 vs 1.7±0.4 mm (P=0.023), the percentage diameter stenosis was 14±9 vs. 36±15 % (P<0.001), and the late luminal loss was 0.1±0.3 vs. 0.6±0.5 mm (P=0.047), respectively.


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  		Table 3 QCA data and physiologic parameters immediately after stent implantation and at 6-month follow-up

 
Haemodynamic follow-up and WSS at 6 months
No significant differences were seen immediately after intervention between the two groups with respect to the haemodynamic data and WSS (Table 3). However, at 6-month follow-up, both FFR and HTG of the sirolimus group differed significantly from the bare metal group. FFR was 0.91±0.05 vs. 0.83±0.10 mmHg (P=0.027) and HTG was 1.2±1.2 vs. 7.5±8.1 mmHg (P<0.001) in favor of the sirolimus stent. Also, the TPR differed significantly: 0.99±0.01 in the sirolimus group vs. 0.91±0.09 in the bare metal group (P=0.002) (Table 3).

The normal reference value of WSS in a coronary artery at rest is 1.5–2 Pa.12 There was no significant difference in WSS for any of the positions at baseline between the groups. WSS within the stent at 6 months differed significantly between the two groups (P=0.003). The values of WSS at the entrance and exit of the stent did not differ significantly at six months (Table 3). In Table 3, also the changes at six months from baseline are mentioned for both stent types. For the parameters FFR and TPR, the change at follow-up in the BMS was significantly lower than in the sirolimus stent (P=0.028 and 0.029, respectively). For the parameters HTG and WSS in the stent, the changes at follow-up were significantly higher in the BMS compared with the sirolimus stent (P=0.026 and 0.009, respectively). Values for the WSS at different positions are presented in Figure 3.


Figure 1343
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  		Figure 3 Approximate WSS at three positions immediately after implantation and at 6-month follow-up for the sirolimus stent (top) and the BMS (bottom). The locations marked with ‘prox’ and ‘dist’ indicate the position just proximal and just distal to the stent, respectively.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusion
 Acknowledgements
 References
 
This study shows that drug-eluting sirolimus stents have a better and a more physiologic haemodynamic performance at 6-month follow-up than the corresponding BMSs. Moreover, at follow-up the sirolimus stent maintained normal values of WSS in contrast to the BMS, where high values of WSS were found within the stent.

It has been shown previously that calculating local WSS in stents is useful in identifying specific locations at risk for restenosis.6,7 In those studies, WSS was calculated with a higher spatial resolution compared with our study where only global approximate values of WSS were obtained. Nevertheless, our values are in the physiologic range of 1.5–2 Pa along the stented segment in both vessels just after stenting, the normal resting value for coronary arteries in a wide range of species.12 In contrast to the BMS, the sirolimus stent maintained this normal WSS after 6 months. The high values of WSS found in the BMS after 6 months reflect the decreased MLD and consequently the higher percentage diameter-stenosis. These findings are in concordance with previous angiographic studies.1,2 As WSS also accounts for the average cross-sectional velocity and viscosity, it is a better indicator for the local haemodynamics within the stent than the anatomy-derived parameters alone.

Despite extensive studies on FFR and pressure gradients across BMSs immediately after implantation and at follow-up,4,13 little was known so far about those physiologic and haemodynamic characteristics of drug-eluting stents over time. The FFR and HTG we found in both groups show that after 6 months, approximately half of the total pressure gradient present in the vessel stented by the BMS was due to gradient across the stent, in contrast to the vessel stented by the sirolimus stent where this gradient across the stent itself was very small (7.5±8.1 mmHg in the BMS vs. 1.2±1.2 mmHg in the sirolimus stent, P<0.001).

A recurring hyperaemic gradient of 5–10 mmHg after 6 months in BMS, due to intimal hyperplasia, has been described earlier.4,13 The present study shows that for sirolimus stents, this phenomenon is much less severe. For both groups, the pressure loss along the remaining non-stented part of the coronary artery was identical, indicating that the arteries in both groups were diseased to a similar degree with a diffuse hyperaemic pressure decline of ~10 mmHg.

In patients with multiple but distant abnormalities within one coronary artery and a significantly decreased FFR (i.e. <0.75–0.80), in the past, it was recommended not to stent spots or segments with a hyperaemic gradient of <10 mmHg because, as mentioned above, despite optimal deployment, a hyperaemic gradient of 5–10 mmHg was present again after 6 months in the majority of the BMSs.13 For sirolimus stents, our study shows that the average HTG after 6 months is significantly smaller, i.e. 1–2 mmHg. Therefore, a practical implication of this study for interventional cardiology is that in such diseased arteries with multiple non-adjacent lesions, whether or not superimposed on diffuse disease or separated by side branches and each in itself not haemodynamically significant but in series responsible for inducible ischaemia, the possibility for successful interventional treatment by several stents is significantly improved. The beneficial effect of BMSs in those stenoses with gradient <10 mmHg was often disappointing in the past due to the recurring gradient of ~5–10 mmHg after 6 months. Having established now that across DES only minor gradients are present at follow-up, interventional treatment in such patients has become more rationale. It should be emphasized that stenting on a purely anatomic basis in these patients makes little sense if FFR of all lesions together is >0.80.14

Finally, because both the sirolimus stent and the BMS were implanted in pairs in stenoses with comparable characteristics within the same patient, the biological environment and risk factors were identical as much as possible and the possibilities that the differences observed were due to other factors than the stent itself was minimized as much as possible.

Limitations
Calculation of WSS in this study was based upon QCA, APV, and viscosity, limited to the entrance, exit, and body of the stent. These calculations are influenced by the inaccuracy in APV that has been described before.10 To have obtained accurate geometrical information and consequently accurate numerical shear stress data, IVUS would have been necessary. However, because this would have further prolonged the time of these extensive procedures, we chose for WSS calculations by Eq. (1) at the entrance, body, and exit of the stent only, as explicated in the Methods section.

Although we did not specifically investigated inter and intra observer variability, we assumed that this would be limited, because WSS is calculated directly from viscosity, flow velocity, and QCA, all of which have a small inter and intra observer variability.9–11

With respect to the limited number of stenoses (2x20), it should be noted that it was not the intention of this study to demonstrate any difference in restenosis or adverse event rate, but to acquire better understanding of the physiological behavior of sirolimus stents compared with the BMS, which was clearly achieved in this study (Table 3).


   Conclusion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
Acknowledgements
 References
 
At 6-month follow-up, the sirolimus stent was superior compared with its bare metal counterpart not only with respect to angiographic but also to physiologic characteristics. FFR was significantly higher and the HTG significantly lower for the sirolimus stent. Furthermore, in contrast to the BMS, the sirolimus stent maintained a normal WSS within the stented segment.


   Acknowledgements
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
References
 
This study was supported by a grant of Cordis, a Johnson & Johnson Company and by grant 04–03 of the foundation ‘Stichting Vrienden van het Hart’, Eindhoven, The Netherlands.

The authors are indebted to the nursing staff of the catheterization laboratory of the Catharina Hospital in Eindhoven for their dedicated assistance in the invasive procedures.

Conflict of interest: none declared.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Acknowledgements
 References
 

  1. Morice MC, Serruys PW, Sousa JE, Fajadet J, Ban Hayashi E, Perin M, Colombo A, Schuler G, Barragan P, Guagliumi G, Molnàr F, Falotico R. (2002) A randomized comparison of a sirolimus-eluting stent with a standard stent for coronary revascularization. N Engl J Med 346:1773–1780.[Abstract/Free Full Text]
  2. Moses JW, Leon MB, Popma JJ, Fitzgerald PJ, Holmes DR, O’Shaughnessy C, Caputo RP, Kereiakes DJ, Williams DO, Teirstein PS, Jaeger JL, Kuntz RE. (2003) Sirolimus-eluting vs. standard stents in patients with stenosis in a native coronary artery. N Engl J Med 349:1315–1323.[Abstract/Free Full Text]
  3. Pijls NHJ, De Bruyne B, Peels K, Van der Voort PH, Bonnier HJRM, Bartunek J, Koolen JJ. (1996) Measurement of fractional flow reserve to assess the functional severity of coronary-artery stenosis. N Engl J Med 334:1703–1708.[Abstract/Free Full Text]
  4. Pijls NHJ, Klauss V, Siebert U, Powers E, Takazawa K, Fearon WF, Escaned J, Tsurumi Y, Akasaka T, Samady H, De Bruyne B. (2002) Coronary pressure measurement after stenting predicts adverse events at follow-up. A multicenter registry. Circulation 105:2950–2954.[Abstract/Free Full Text]
  5. Lopez-Palop R, Pinar E, Lozano Í, Saura D, Picó F, Valdés M. (2004) Utility of the fractional flow reserve in the evaluation of angiographically moderate in-stent restenosis. Euro Heart J 25:2040–2047.[Abstract/Free Full Text]
  6. Wentzel JJ, Krams R, Schuurbiers JC, Oomen JA, Kloet J, Van der Giessen WJ, Serruys PW, Slager CJ. (2001) Relationship between neointimal thickness and shear stress after wallstent implantation in human coronary arteries. Circulation 103:1740–1745.[Abstract/Free Full Text]
  7. Gijsen FJ, Oortman RM, Wentzel JJ, Schuurbiers JCH, Tanabe K, Degertekin M, Ligthart JM, Thury A, De Feyter PJ, Serruys PW, Slager CJ. (2003) Usefulness of shear stress pattern in predicting neointimal distribution in sirolimus-eluting stents in coronary arteries. Am J Cardiol 92:1325–1328.[CrossRef][ISI][Medline]
  8. Pijls NHJ. (2004) Optimum guidance of complex PCI by coronary pressure measurement. Heart 90:1085–1093.[Free Full Text]
  9. Matrai A, Whittington RB, Ernst E. (1987) A simple method of estimating whole blood viscosity at standardized hematocrit. Clin Hemorheol 7:261–265.
  10. Büchi M and Jenni R. (1998) Measurement of flow velocity in the coronary circulation: requirements and pitfalls. Semin Intervent Cardiol 3:45–50.[Medline]
  11. Reiber JH, Serruys PW, Kooijman CJ, Wijns W, Slager CJ, Gerbrands JJ, Schuurbiers JCH, Den Boer A, Hugenholtz PG. (1985) Assessment of short-, medium-, and long-term variations in arterial dimensions from computer-assisted quantitation of coronary cineangiograms. Circulation 71:280–288.[Abstract/Free Full Text]
  12. Ku DN. (1997) Blood flow in arteries. Annu Rev Fluid Mech 29:399–434.[CrossRef][ISI]
  13. Hanekamp CEE, Koolen JJ, Pijls NHJ, Michels HR, Bonnier HJRM. (1999) Comparison of quantitative coronary angiography, intravascular ultrasound, and coronary pressure measurement to assess optimum stent deployment. Circulation 99:1015–1021.[Abstract/Free Full Text]
  14. Bech GJW, De Bruyne B, Pijls NHJ, De Muinck ED, Hoorntje JCA, Escaned J, Stella PR, Boersma E, Bartunek J, Koolen JJ, Wijns W. (2001) Fractional flow reserve to determine the appropriateness of angioplasty in moderate coronary stenosis. A randomized trial. Circulation 103:2928–2934.[Abstract/Free Full Text]

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