Eur. Radiol. 8, 765±769 (1998) Ó Springer-Verlag 1998

European Radiology

Urogenital radiology Original article Duplex Doppler analysis of interlobular arteries in transplanted kidneys C. Martinoli1, M. Bertolotto2, G. Crespi1, F. Pretolesi1, M. Valle1, L. E. Derchi1 1 2

Cattedra ªRº di Radiologia, Università di Genova, I-16 132 Genova, Italy Istituto di Radiologia, Università di Trieste, I-34 139 Trieste, Italy

Received 30 December 1996; Revision received 16 May 1997; Accepted 3 September 1997

Abstract. The aim of our study was to analyze changes in spectral Doppler waveforms between interlobar and interlobular arteries in renal transplants and to determine whether sampling location at interlobular level can be suitable for intrarenal resistive index (RI) measurements. Paired series of spectral tracings from interlobar arteries and respective interlobular branches were obtained in 62 consecutive renal transplants at 6.5-MHz Doppler frequency. The values of peak systolic velocity (PSV), end diastolic velocity (EDV) and RI were significantly (P < 0.01) reduced when calculated at interlobular level. In 38 % of cases, an interlobar RI higher than 0.70 corresponded to a normal interlobular RI. The values of PSV, EDV, and RI did not differ significantly at interlobular level between allograft subsets with normal and elevated serum creatinine level. Both intra- and interobserver variation were higher at interlobular than at interlobar level when performing the RI. During a conventional study of renal vasculature, an underestimation of abnormal RI findings can be expected from the incidental evaluation of interlobular tracings. We recommend sonologists to pay attention in accurately locating the sample volume at interlobar±arcuate level when evaluating intrarenal RI. Key words: Kidney, transplantation ± Ultrasonography, Doppler studies ± Kidney, blood flow

Introduction With the increasing quality of US equipment, the capability of Doppler systems to depict flow in the renal cortex has further advanced [1] and flow signals can be easily appreciated up to the renal capsule, including interlobular vessels and perhaps their distal branches [2]. DeCorrespondence to: C. Martinoli

pending on different technologies, machine settings and body habitus, the interlobular vasculature can be depicted either in form of cortical blush or as discrete and well-individualized vessels both in the cortex of native kidneys and renal transplants [2±5]. Therefore, the incidental evaluation of interlobular spectra is becoming increasingly possible during a conventional duplex Doppler study of renoparenchymal vasculature and it must be substantiated what waveform changes, if any, occur at the interlobular level with respect to the other sites of Doppler sampling, and mostly to the interlobar one that is commonly regarded as the preferred site at which the renoparenchymal arterial tracing is sampled for spectral analysis [6, 7]. Accordingly, we performed this study to compare spectral Doppler waveforms between interlobar and interlobular arteries in renal transplants. Materials and methods We prospectively examined 62 consecutive patients (21 women, 41 men) with a mean age of 43.7 years (range 21±68 years) who underwent renal transplantation and were referred to our department for routine follow-up. Three patients had living related donor allografts, and the others received cadaveric kidneys. The mean time after renal transplantation was 54 months (range 1 month to 15 years). Twenty-nine patients had a normal allograft function [defined as stable serum creatinine level of £ 1.4 mg/dL (124 mmol/L)]; thirty-three (53 %) had abnormal function [serum creatinine range of 1.5±3.7 mg/dL (133±327 mmol/L)] and a biopsy diagnosis of acute (n = 7 acute rejection; n = 5 toxic reaction to cyclosporine) and chronic (n = 14 chronic rejection; n = 6 relapse of underlying glomerulonephritis) pathology. One patient had renal artery stenosis and abnormal renal function. Overall, 3 of 62 renal allografts with diagnosis of acute (n = 2) and chronic (n = 1) rejection were excluded from the study group due to inconsistent interlobular visibility or too weak pulsed Doppler signals at interlobular level, so that 59 kidneys were studied.

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a

C. Martinoli et al.: Duplex Doppler analysis of interlobular arteries in transplanted kidneys

b

Fig. 1. Paired series of Doppler tracings are obtained from a interlobar and b respective interlobular arteries under color Doppler US guidance. Due to the high density of interlobular vessels in the normal transplant cortex, the Doppler spectrum in b reports, at the same time, the flow signal from an interlobular artery (above the baseline) and an interlobular vein (below the baseline)

Ultrasound studies were performed with a commercially available scanner (HDI-3000, ATL, Bothell, Wash.) using a linear-array broadband transducer (L 10±5 model, frequency band 10±5 MHz) working at 6 MHz for Doppler imaging. At this frequency, conventional color and amplitude modulated Doppler techniques are able to depict the interlobular arteries in full extension, from their arcuate origin to the proximity of renal capsule. Interlobulars appear as discrete, closely spaced, vessels well separated from one another by a signal-void interval, and can consistently be evaluated by means of spectral analysis. In each kidney, two paired series of Doppler tracings were obtained from interlobar and respective interlobular arteries throughout the near portion of renal circumference. As determined under color or amplitude-modulated Doppler guidance, each interlobular vessel studied arose from the interlobar vessel that was also studied. Signals located at the corticomedullary junction and connected distally with interlobular vessels were assumed to be from arcuate arteries and were excluded from evaluation. In malfunctioning kidneys with avascular patches or diffuse reduction of cortical signals, Doppler tracings were obtained from the cortical areas in which interlobular vessels were more apparent. The following technical parameters were applied: low wall filter (50 Hz), low pulse repetition frequency (1250±3120 Hz), power output of 100 % and sample volume size of 2 mm. These settings were important to obtain the larg-

est and most sharply defined waveforms possible, especially at the interlobular level. Each recording was obtained from one of at least three consecutive, similarly appearing waveforms to ensure that movement of the Doppler sample volume or change in the Doppler interrogation angle had not occurred during waveform acquisition. Placement of Doppler gate was obtained by keeping the vessel in a longitudinal orientation without inducing any probe compression on the allograft cortex. In each measurement, the transducer position was adjusted to maximize the length of vessel displayed and the sample gate was placed at the middle third of the vessel examined. From each recording, PSV, EDV, and RI were calculated using the software of the US unit. Measurement of flow velocity was always achieved with angle correction, by keeping the beam/vessel angle below 30 . In addition, spectral Doppler tracings were qualitatively evaluated for the presence of an early systolic peak (ESP), as described by Stavros et al. [8]. Mean values of PSV, EDV, and RI were used for statistical analysis of differences between the two groups of arteries. Then, 42 series of spectral Doppler measurements at interlobar and interlobular level were obtained in 21 kidneys by two independent observers to assess interobserver variability, and two times by one observer for intraobserver variability. Kappa statistics were used to measure the agreement between observers with a useful range of 1.00 (complete agreement) to 0.0 (chance agreement) [9]. For all tests, significance was considered to be a P-value of less than 0.05. Results Paired spectral Doppler tracings from interlobar and interlobular arteries were readily obtained in 59 renal transplants (Fig. 1). Duplex Doppler results from com-

C. Martinoli et al.: Duplex Doppler analysis of interlobular arteries in transplanted kidneys Table 1. Correlation of Doppler parameters between interlobar and interlobular arteries. RI resistive index; PSV peak systolic velocity; EDV end diastolic velocity Doppler parameter

Interlobara

Interlobulara

P -value

RI PSV (cm/s) EDV (cm/s)

0.70 ± 0.07 25.13 ± 9.99 7.54 ± 3.73

0.66 ± 0.06 10.27 ± 4.35 3.49 ± 1.66

3.64 e- 5 < 10- 6 < 10- 6

a Data are given as mean ± SD of n = 118 values obtained from 59 cases

Table 2. Correlation of Doppler parameters between interlobar and interlobular arteries in subgroups of renal allografts with normal or abnormal renal function Doppler parameter Interlobar arteries RI PSV (cm/s) EDV (cm/s) Interlobular arteries RI PSV (cm/s) EDV (cm/s) a b

Creatinine £ 1.4 mg/dLa

Creatinine > 1.4 mg/dLb

P -value

0.70 ± 0.05 23.69 ± 9.84 7.11 ± 3.14

0.71 ± 0.09 26.99 ± 9.99 8.11 ± 4.34

0.916 0.046 0.293

0.67 ± 0.05 10.64 ± 4.35 3.57 ± 1.47

0.66 ± 0.08 9.79 ± 4.34 3.39 ± 1.88

0.971 0.157 0.179

Data are given as mean ± SD of n = 58 values Data are given as mean ± SD of n = 60 values

parative evaluation of interlobar and interlobular tracings are summarized in Table 1. As the sample gate was moved downstream from interlobars to interlobulars, four main points could be observed: 1. Spectral analysis showed that all values of PSV, EDV, and RI were reduced when calculated at interlobular level. Between corresponding interlobar and interlobular branches (paired data), differences of PSV, EDV, and RI proved to be statistically significant (Table 1). In 38 % of cases with an interlobar RI ³ 0.70, the interlobular RI was less than 0.70. Conversely, an interlobar RI < 0.70 corresponded to an interlobular RI ³ 0.70 in only 5 % of cases. However, all these cases, two with normal and one with impaired allograft function, had borderline (0.69) interlobar RI values. 2. The ESP was recognized at a lesser extent in interlobulars (11 %) than in interlobars (36 %). At both arterial levels, no significant difference in ESP expression was observed between kidneys with normal and abnormal function. The ESP was undetected in the patient with renal artery stenosis. 3. When the interlobar and interlobular tracings were subdivided into two groups on the basis of presence of normal or abnormal renal function tests, no significant difference in RI, PSV, or EDV could be observed at both arterial levels between the groups (Table 2). However, from the group with abnormal function, renal allograft with acute rejection had higher interlobar (range 0.85±0.89, mean 0.87) and interlobular (range 0.76±0.82, mean 0.78) RI than the overall mean RI (see Table 2).

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4. The intraobserver agreement for RI measurements performed better at interlobar (k = 0.90; P < 0.001) than at interlobular (k = 0.79; P < 0.001) level, whereas a weaker interobserver agreement was observed at both arterial levels (k for interlobars = 0.70; P < 0.001; k for interlobulars = 0.56; P < 0.001). Discussion Recent attention has been paid in the literature to whether the site of Doppler measurement influences reliability of flow parameters in the renal vasculature [6, 7, 10]. Some authors indicated the interlobar±arcuate arteries as the preferred site to obtain duplex Doppler measurements in clinical practice, because the RI value is reproduced most consistently at this anatomic level [5, 6]. On the other side, in an experimental study for detecting indirect signs of renal artery stenosis, the RI from segmental arteries correlated better with mean pressure gradient and had a lower standard deviation than RI from interlobar arteries [11]. With the increasing quality of US equipments and the recent development of amplitude-modulated Doppler technology, the capability of Doppler systems to depict flow in the kidney has further advanced and, at present, the interlobular arteries can be added to the list of possible anatomic sites at which sampling can be reliably obtained. The interlobular arteries are quite dissimilar from the interlobar vessels as regards vessel diameter and overall number. In fact, they are 10±20 times smaller and much more numerous (mean vessel diameter: 100±200 mm; number of vessels per kidney: > 50 000) than the interlobar arteries (mean vessel diameter: 2 mm; number of vessels per kidney: < 50) [12]. These considerations could explain some differences in flow velocity and impedance that we have observed between the two groups of arteries. Among these, the decline of PSV and EDV from interlobar to interlobular arteries can be interpreted as a result of tapering of arterial diameter, enlargement of vascular bed, and more distal site of the interlobulars. In the renal vasculature, this finding is in accordance with the progressive decline of flow velocities reported from the hilum of the kidney to the outer parenchyma [6]. Then, as RI is calculated from the ratio: PSV±EDV/PSV, the cause of its decrease at interlobular level follows the more rapid decline of PSV than EDV. This explains why the systodiastolic ratio is lower at the interlobulars: as it reduces the further one proceeds down the vascular tree. Likewise, the decreasing detection rate of the ESP from interlobar to interlobular arteries can be explained, at any given level of compliance, by a progressive absorption of the transmitted pulse as the vessel proceeds more distally [13]. Knapp et al. have already made an attempt to compare, in native kidneys, Doppler waveforms at interlobular level with other intrarenal arteries using a 5-MHz transducer performing color Doppler at 3.5 MHz [7]. These authors also obtained the lowest RI values while sampling at the most distal site, even if their figures did not reach statistical significance. At least in part, this

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discrepancy could be explained with the different methods and technologies used. We have performed Doppler analysis at 6 MHz to obtain tracings at interlobular level possibly in a more distal site than that evaluable by a 3.5-MHz Doppler system. In our series, the interobserver variability exceeded the intraobserver variability at interlobar and interlobular levels. This finding is in agreement with previous studies on reproducibility of Doppler US measurements of RI in renal allografts [14]. In addition, both intra- and interobserver agreement for RI measurements were weaker at the interlobular level. This could be explained by the fact that Doppler tracings from interlobular arteries were less clearly defined, due to a worse signal-to-noise ratio, than those obtained at interlobar level. This could lead to higher subjectivity during manual placement of calipers for spectral measurements. On the contrary, Doppler signals were easier to obtain at interlobar arteries, and thus most likely to result in reproducible measurements. However, we could also speculate that Doppler spectra sampled from proximal arteries reflect the overall changes of multiple interlobular vessels, which leads to a lower variability of blood flow profiles upstream. In native kidneys, Platt considered 0.70 as a reasonable upper limit for a normal mean intrarenal RI assessed at the interlobar±arcuate level [15], and this value has become widely accepted as a threshold between normal and abnormal status of renal vasculature. However, in our groups of paired measurements, an elevated interlobar RI corresponded to an interlobular RI < 0.70 in 38 % of measurements. Although duplex Doppler US has proved to be of questionable value in the evaluation of renal transplant dysfunction and wide discrepancies in sensitivities and specificities of RI thresholds are reported in this field [16, 17], an underestimation of abnormal RI findings can be expected from the incidental evaluation of interlobular tracings. As Doppler technology progresses this can be increasingly true, and also in native kidneys. Therefore, we recommend sonologists to pay attention in accurately locating the sample volume at interlobar±arcuate level when intrarenal RI is evaluated, at least until new upper limits of normal interlobular RI are established. Finally, we have made a preliminary attempt to assess if differences in Doppler flow parameters occur at interlobar and interlobular level in allograft subsets with normal or abnormal renal function. Our data have demonstrated that pulsed Doppler analysis is quite insensitive, at least in renal transplants, to detect functional changes linked to creatininemia. These data support other reports that show normal allograft function cannot be reliably assured using the RI [16, 17]. On the contrary, with respect to flow velocities, lower PSV and EDV values in intrarenal arteries have been reported in malfunctioning kidneys as a consequence of reduced distal compliance [13, 18]. We have not observed this finding at interlobular level. A possible explanation for this discrepancy could be suggested by the occurrence, in many of our allografts with abnormal function, of cortical patches without interlobular flow. In these kidneys Doppler measurements were performed in cortical

areas in which the interlobular signals were more clearly visible. Therefore, it is conceivable that these measurements did not reflect the actual vascularization of the entire transplant, but only of the less pathologic areas. In malfunctioning transplants, qualitative abnormalities of interlobular vasculature, including absence, reduced density, tortuosities and distorsion of interlobular vessels, have been described with amplitude-modulated Doppler systems using high-frequency transducers [4, 19]. These signs could probably provide higher capability to identify pathologic changes of the renal cortex, even when affecting focal areas only. However, such abnomalities are too subjective and dependent on technical factors to be considered, at least at present, as reliable signs for assessing renal transplant dysfunction. In conclusion, intrarenal spectral Doppler measurements obtained from interlobular arteries do not lead to further advantages in assessing renal parenchymal disease and cause underestimation of RI values. The RI at the level of the interlobar arteries must be preferred in clinical applications. References 1. Rubin JM, Bude RO, Carson PL et al. (1994) Power Doppler: a potentially useful alternative to mean-frequency based color Doppler sonography. Radiology 190: 853±856 2. Bude RO, Rubin JM, Adler RS (1994) Power versus conventional color Doppler sonography: comparison in the depiction of normal intrarenal vasculature. Radiology 192: 777±780 3. Preidler KW, Szolar DM, Uggowitzer M et al. (1995) Technical note: comparison of colour Doppler energy sonography with conventional colour Doppler sonography in detection of flow signal in peripheral renal transplant vessels. Br J Radiol 68: 1103±1105 4. Martinoli C, Crespi G, Bertolotto M et al. (1996) Interlobular vasculature in renal transplants: a power Doppler US study with MR correlation. Radiology 200: 111±117 5. Turetschek K, Nasel C, Wunderbaldinger P et al. (1996) Power Doppler versus color Doppler imaging in renal allograft evaluation. J Ultrasound Med 15: 517±522 6. London NJ, Aldoori MI, Lodge VG et al. (1993) Reproducibility of Doppler ultrasound measurement of resistance index in renal allografts. Br J Radiol 66: 510±513 7. Knapp R, Plötzeneder A, Frauscher F et al. (1995) Variability of Doppler parameters in the healthy kidney: an anatomic±physiologic correlation. J Ultrasound Med 14: 427±429 8. Stavros AT, Parker SH, Yakes WF et al. (1992) Segmental stenosis of the renal artery: pattern recognition of tardus and parvus abnormalities with duplex sonography. Radiology 184: 487±492 9. Gottlieb RH, Snizer EL, Hartley DF, Fultz PJ, Rubens DJ (1996) Interobserver and intraobserver variation in determining intrarenal parameters by Doppler sonography. AJR 168: 627±631 10. Bude RO, DiPietro MA, Platt JF et al. (1992) Age dependency of the renal resistive index in healthy children. Radiology 184: 469±473 11. Eibenberger K, Schima H, Trubel W et al. (1995) Intrarenal Doppler ultrasonography: Which vessel should be investigated? J Ultrasound Med 14: 451±455 12. Cuttino JT, Clark RL (1990) The normal vasculature of the genitourinary tract: embryology, anatomy and hemodynamics. In: Pollak HM (ed) Clinical urography, vol 3. Saunders, Philadelphia, pp 2076±2091

C. Martinoli et al.: Duplex Doppler analysis of interlobular arteries in transplanted kidneys 13. Halpern EJ, Deane CR, Needleman L et al. (1995) Normal renal artery spectral Doppler waveform: a closer look. Radiology 196: 667±673 14. London NJ, Aldoori MI, Lodge VG, Bates JA, Irving HC, Giles GR (1993) Reproducibility of Doppler ultrasound measurement of resistance index in renal allografts. Br J Radiol 66: 510±513 15. Platt JF (1992) Duplex Doppler evaluation of native kidney dysfunction: obstructive and nonobstructive disease. AJR 158: 1035±1042 16. Drake DG, Day DL, Letourneau JG et al. (1990) Doppler evaluation of renal transplants in children: a prospective analysis with histopathologic correlation. AJR 154: 785±787

Book reviews Legmann, P.: Scanner Thoracique: Guide Pratique. Paris: Masson 1996. 265 pp., 438 figs., (ISBN 2-225-85403-3), FF 500.00. As stated in the title, this book deals with the CT examination technique and CT findings observed in diseases of the chest, including the lung, pleura and mediastinum. Containing contributions from nine writers, it includes 265 pages and more than 400 figures, and its 19 chapters are divided into four sections. The first section is an overview of normal anatomy of the chest at CT and the different CT technique protocols for chest disease, including high-resolution technique, and helical volumetric acquisition during breath-holding. One chapter is designed to describe the postprocessing reconstruction techniques such as 2D multiplanar reformation, 3D surface display and volumetric rendering techniques. However, this fails to provide clear guidelines concerning the selection of technical parameters. In addition, there is almost nothing on helical CT angiography. The second section deals with focal lung disease, including chapters dedicated to solitary pulmonary nodule, lung collapse and air trapping, cavitation, and lung cancer. The third section deals with diffuse chronic infiltrative lung disease, airway disease, pleural and mediastinal disease. The fourth section is a sort of melting pot made up of disparate chapters dealing with vascular diseases, tuberculosis, mycosis, AIDS, postoperative chest and interventional radiology. Although the structure of the book is rather difficult to understand, it is written in a concise manner and is easy to read. It offers an overview of the current possibilities of CT in many aspects of chest diseases. On the other hand, the book does not attempt a complete, in-depth review. The bibliography remains short and many recent references are missing. From an imaging point of view, it is not a substitute for a chest radiology textbook. The main criticism that can be made concerns the illustrations. Most of the examples are not optimal and many figures are not of high quality. The size of the figures is small and unfortunately the high-resolution CT scan images are not targetted. In summary, despite some shortcomings this book can be considered as good reading for residents and fellows in training. Nevertheless, it could be rather disappointing for the experienced radiologist. Ph. Grenier, Paris

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17. Kelcz F, Pozniak MA, Pirsch JD et al. (1990) Pyramidal appearance and resistive index: insensitive and nonspecific sonographic indicators of renal transplant rejection. AJR 155: 531±535 18. Deane C (1992) Doppler and color Doppler ultrasonography in renal transplants: chronic rejection. J Clin Ultrasound 20: 539±544 19. Grenier N, Claudon M, Trillaud H, Douws C, Levantal O (1997) Noninvasive radiology of vascular complications in renal transplantation. Eur Radiol 7: 385±391

European Radiology Coldwell D. M.: Radiologic Interventions: Embolotherapy. Baltimore: Williams & Wilkins 1997. 185 pp., 185 illustrations, (ISBN 0-683-30268-X), £ 54.00. This book is the first volume in the monograph series Radiologic Interventions. This multi-authored work, consisting of 185 pages, seven chapters and an index, illustrated with numerous figures, covers the whole field of this subspecialty of interventional radiology. The volume starts with a chapter on all the available embolic agents, discussing their individual advantages and limitations. Indications and specific technical details of embolotherapy in different pathologic entities are discussed in the following chapters. Dr. Y. Ben-Menachem, an authority in this field, has written the second chapter on angiographic control of hemorrhage in trauma. He starts with a general introduction and continues with region-specific issues. The quality of the figures of this chapter is rather poor but the text is very structured and informative. In his conclusion he stresses the need for the angiographic approach as the examination of preference in the bleeding trauma patient'. The third chapter, written by the editor, deals with embolotherapy of tumors. General comments are followed by organ-specific treatment modalities. In chapter 4, the same author describes embolotherapy of miscellaneous lesions such as gastrointestinal hemorrhage, bronchial arterial hemorrhage, renal hemorrhage, splenic embolization and embolization of congenital anomalies. Chapter 5 is dedicated entirely to embolotherapy of vascular malformations as therapeutic treatment or as preoperative intervention. Transcatheter embolization techniques as well as direct puncture of the lesion are described. Chapter 6 gives a concise overview of neuro-anatomy and radiological neuro-interventions with the emphasis on neuro-embolization. Although special training is required, this chapter informs the radiologist which intervention is the most feasible in different conditions. In chapter 7, embolotherapy of varicoceles is explained. This book gives a complete overview of embolotherapy. It is well structured, contains interesting and useful information, and is illustrated with several examples. After reading this book, the interventional radiologist will be encouraged to perform embolotherapy safely and aggressively. L. Stockx, Leuven