Changes in renal Doppler ultrasonographic parameters in patients
managed with rigid ureteroscopy
O
¨ zlem Tokgo¨z
1, Hu¨snu¨ Tokgo¨z
2, I˙lker U
¨ nal
3, Nuray Voyvoda
4and I˙smail S¸erifog˘lu
11
Department of Radiology, Karaelmas University, School of Medicine, Zonguldak;2Department of Urology, Karaelmas University, School of Medicine, Zonguldak;3Izmir University, School of Medicine, Department of Biostatistics, Izmir;4Acıbadem Kocaeli Hospital, Department of Radiology, Kocaeli, Turkey
Correspondence to: Ozlem Tokgoz. Email: h_tokgoz@hotmail.com
Abstract
Background: There has been no study evaluating the intrarenal hemodynamic changes after ureteroscopy in the published literature.
Purpose: To determine preoperative and postoperative intrarenal vascular parameters such as resistive index (RI), pulsatility index (PI), peak systolic velocity (PSV), end-diastolic velocity (EDV), measure changes on these values (DRI, DPI, DPSV, DEDV) after ureteroscopy (URS) and compare the outcomes with the results of normal contralateral kidneys, and finally investigate possible parameters that would affect renal vascular resistance changes.
Material and Methods: We prospectively studied 47 patients who underwent rigid URS. Preoperative gray-scale and Doppler ultrasonography (CDUS) measurements were obtained 24 h before URS. Similarly, postoperative CDUS measurements were done 24 h after the operation. The degree of hydronephrosis and location of stones in the obstructed kidneys, diameters of both kidneys, and thickness of renal parenchyma were evaluated with gray-scale US followed by CDUS with calculation of the intrarenal RI, PI, PSV, and EDV values for each kidney.
Results: For the operated kidneys, statistically significant P values were noticed when RI and PI values were considered (P , 0.001). DRI and DPI of the operated kidneys were also significantly greater than the values for non-operated kidneys (P , 0.001). However, it was not the case for DPSV and DEDV values. In Spearman correlation coefficient analysis, DRI was found to be correlated with the parameters: “operative time” and “irrigation fluid volume”. No significant relation was documented between DRI and the other parameters: age, gender, side of ureteroscopy, stone location, and degree of hydronephrosis.
Conclusion: Significant changes in RI and PI values in patients treated with URS reveal that URS can cause a significant increase in renal vascular resistance. With the increase in operative time and irrigation fluid volume used during the operation, RI seems to be significantly increased.
Keywords:Doppler, renal resistance index, rigid ureteroscopy, ultrasonography Submitted August 20, 2012; accepted for publication October 20, 2012
Today, ultrasonography (US) is regarded as a non-invasive, quick, inexpensive, and reproducible diagnos-tic method for the evaluation of obstructive uropathy. It also has additional advantages such as the absence of contrast material injection and exposure to ionizing radiation. Although conventional gray-scale US should provide ana-tomical assessment of kidneys, it cannot be used for func-tional evaluation. Major disadvantages appear especially when dilation in the collecting system is limited or absent. Therefore, dynamic US evaluation of kidneys with color duplex sonography (CDUS) may provide information
about functional hemodynamic changes earlier than ana-tomical changes ( pyelocaliectasis or hydronephrosis in col-lecting system). Pepe et al. investigated this issue in patients with renal colic and proposed that renal vascular resistance measurement with CDUS might improve the diagnostic accuracy of conventional gray-scale US for the differentiation between obstructive and non-obstructive dilations (1). Even after 2 h of renal obstruction, those hemo-dynamic changes might be demonstrated with CDUS (2 – 5). Ureter is a frequent location where stones may be found and the management differs according to the size, location,
and number of stones. A treatment option for this group of patients is ureteroscopy (URS). URS is the preferred approach for the surgical treatment of ureteral stones with low complication and high success rates (6 –8). The reported overall stone-free rate of URS for ureteral stones is remark-ably high at 85 – 100% depending on stone location and size (7, 9, 10). Our study population was composed of patients with ureteral stones 10 mm and none of our patients had significant (4 mm) residual stones during US evaluation done on the first postoperative day, so we finally achieved a 100% stone-free rate. Routinely, during an URS operation, irrigation fluid was infused through the ureteroscope in order to visualize the ureter. Therefore, an increased intraureteral and intrapelvic pressure could be expected during this operation. Our hypothesis was that URS operation would increase renal vascular resistance and cause functional hemodynamic changes detected by CDUS in the operated kidney side. To the best of our knowl-edge, there is no study evaluating these intrarenal hemody-namic changes after URS in the published literature.
Hence, our primary aim in this prospective clinical study was to determine preoperative and postoperative intrarenal vascular parameters such as resistive index (RI), pulsatility index (PI), peak systolic velocity (PSV), end-diastolic vel-ocity (EDV); measure changes on those values (DRI, DPI, DPSV, and DEDV) in patients treated with URS; and compare the outcomes with the results of normal contralat-eral kidneys which served as controls. In addition, we aimed to determine possible parameters that could affect renal vascular resistance changes.
Material and Methods
After the approval of the hospital ethic committee was obtained, we prospectively studied 47 patients who under-went rigid URS because of obstructive ureteric stones with a diameter of 10 mm. All of the patients were managed at the urology department of our University hospital. No patient in our study group was known to have suffered prior renal vascular disease, renal failure, diabetes mellitus, or liver disease. In addition, no patient had prior open or percutaneous renal surgery on either operated side or con-tralateral kidneys. Otherwise, the patients were excluded from the study.
All examinations were performed by the same experi-enced radiologist (OT) and all ultrasound measurements were done by LOGIQw
9 system (GE Healthcare, Milwaukee, WI, USA) equipped with a 3.5-Mhz convex-array transducer. Preoperative gray-scale and CDUS measurements were obtained 24 h before the operations. Similarly, postoperative CDUS measurements were done 24 h after URS.
The degree of hydronephrosis and location of the stone (if visible) in the obstructed kidney, diameters of both kidneys, and thickness of renal parenchyma were evaluated with conventional gray-scale US followed by CDUS with calcu-lation of the intrarenal RI, PI, PSV, and EDV values for each kidneys. In total, 94 kidneys were evaluated.
When the central echo complex was separated minimally by distended anechoic calyceal structures, then the kidneys were classified as hydronephrotic (grade 1) (11,12). Non-dilated systems were categorized as grade 0 (absence of hydronephrosis). Patients with hydro-nephrotic kidneys greater than grade 1 were excluded from the study.
Doppler signals were obtained from interlobar arteries along the edge of the medullary pyramids. Doppler spectral waveforms were optimized by using the lowest pulse rep-etition frequency possible without aliasing, the greatest gain possible without background noise, a low-wall filter (50 Hz), and a 2 –4 mm Doppler gate. Evaluation included obtaining waveforms in the upper, mid aspect, and lower pole of the kidneys. Multiple Doppler waveforms were obtained from at least 3 – 5 vessels, and the values for each kidney were averaged. The angle correction cursor was adjusted parallel to the direction of flow and always ,608. This correction was performed in all spectral Doppler measurements. PSV, EDV, and mean flow velocity were measured directly (Fig. 1). Then, measurement of the RI and PI were performed with the use of online calculation software. RI was calculated as “(PSV2minimum diastolic velocity)/PSV” from the Doppler spectral waveforms using the built-in software of the sonographic equipment. An average RI was calculated from all the RI values from each kidney. DRI was calculated as the mean difference between the postoperative and preoperative RI values ( post-operative 2 prepost-operative RI). PI was calculated as “(PSV 2 EDV)/mean velocity”. An average PI was calculated from all the PI values from each kidney. DPI, DPSV, and DEDV were similarly calculated as the mean difference between the mean postoperative and preoperative values. In each patient, the mean RI, PI, PSV, and EDV for the contralateral normal kidney was also obtained and compared with the symptomatic side. The normal contralateral kidneys, which served as controls, were assessed according to same protocol.
Interventions were made under general anesthesia. The patients were positioned on the operating table in a lithot-omy position with the leg stretched on the affected side and raised on the opposite side (Perez-Castro position).
Fig. 1 Color duplex sonogram of a patient showing spectral Doppler findings (angle correction was performed in all measurements)
Video monitoring and fluoroscopy were used in each case. Routine application of an endocamera is preferred to secure sterility and because of much easier manipulation. Warmed physiological saline solution was used as an irriga-tion fluid. After visualizing the ureteral orifice with cysto-urethroscopy, a guidewire was inserted through the orifice followed by rigid ureteroscopic evaluation with a 9.5 French ureteroscope. Operative time and volume of the irrigation fluid were recorded for each patient. Operative time was taken from the first entry of the ureteroscope into the ureter to the exit of the ureteroscope through the ureteral orifice. The amount of the irrigation fluid consumed
during this time period was also recorded and regarded as “irrigation fluid volume”.
For statistical analyses, a commercially available software package (Statistical Package for Social Sciences, version 18.0, SPSS Inc., Chicago, IL, USA) was used. Categorical vari-ables were summarized as numbers and percentages; con-tinuous variables were given as the means and standard deviations (median, minimum, and maximum, if required). Variables were compared using Student’s T and Mann-Whitney U tests depending on the data type. For the comparison of postoperative and preoperative CDUS parameters (RI, PI, PSV, EDV, DRI, DPI, DPSV, and DEDV), paired samples T and Wilcoxon Signed Rank tests were used. Spearman correlation coefficient was obtained to investigate the correlation between continuous variables. Two-tailed P value of ,0.05 was accepted as statistically significant.
Results
Clinical, demographic data, and renal morphological par-ameters in the study population are reported in Table 1. Mean renal parenchymal thickness, renal length, and width values for operated kidneys were comparable with the values for normal contralateral kidneys of which served as controls (P . 0.05, student’s t test).
In Table 2, CDUS findings for each kidney and relevant P values for each comparison were given. Although, the Pvalue was ,0.05, the mean RI increase on normal contra-lateral kidneys after ureteroscopies was only 0.01 (2.25% increase after the operation). However, for the operated kidneys, very significant statistical significancies were noticed when RI (8.6% increase after the operation) and PI (21.8% increase after the operation) values were considered (P , 0.001). The changes in mean RI (DRI) and PI (DPI) of the operated kidneys were also significantly greater than the changes of non-operated kidneys (P , 0.001). The differ-ences in the mean DPSV and DEDV between the operated Table 1 Clinical, demographic data, and renal morphological
par-ameters in the study population
Mean age (years) 49.40 + 14.73 (21 – 81) Gender (male/female) 27/20
Side of ureteroscopy (right/left) 25/22 Stone location (n; %)
No stone 7 (15%)
Lower ureter 19 (40%) Middle ureter 16 (34%)
Upper ureter 5 (11%)
Hydronephrosis degree in operated kidney (n; %)
Absent (grade 0) 21 (45%)
Grade 1 26 (55%)
Mean operative time (min) 49.81 + 32.54 (5 – 120) Mean irrigation fluid volume (mL) 2392.31 + 1820.31
(100 – 7000) Mean renal parenchymal thickness (mm)
Normal contralateral kidney 13.12 + 2.65 (10 – 23) Operated kidney 12.03 + 2.68 (9 – 23) Mean renal length (mm)
Normal contralateral kidney 112.81 + 13.48 (72 – 158) Operated kidney 108.87 + 14.68 (70 – 159) Mean renal width (mm)
Normal contralateral kidney 47.62 + 7.3 (31 – 72) Operated kidney 46.15 + 8.48 (24 – 73)
Table 2 Spectral Doppler analysis findings for each kidneys
Normal contralateral kidney Operated kidney
Preoperative Postoperative P Preoperative Postoperative P Mean +++++ SD Mean +++++ SD Mean +++++ SD Mean +++++ SD
Med (range) Med (range) Med (range) Med (range)
RI 0.59 + 0.05 0.6 + 0.05 0.014 0.61 + 0.05 0.66 + 0.06 <0.001 0.59 (0.5 – 0.76) 0.6 (0.53 – 0.74) 0.61 (0.53 – 0.79) 0.65 (0.54 – 0.83) DRI 0.01 + 0.03 0.05 + 0.05 <0.001† PI 1.02 + 0.32 1.01 + 0.18 0.633 1.03 + 0.22 1.23 + 0.28 <0.001 0.97 (0.71 – 2.76) 0.96 (0.63 – 1.6) 1 (0.65 – 1.97) 1.14 (0.79 – 1.9) DPI 20.02 + 0.31 0.2 + 0.25 <0.001† PSV (cm/s) 30.04 + 8.63 29.63 + 9.32 0.794 27.9 + 8.55 31.1 + 12.83 0.080 28.3 (14.4 – 51.4) 28 (10.7 – 50) 26 (14.6 – 52.7) 27.5 (10.5 – 77) DPSV 20.42 + 10.91 3.2 + 12.25 0.106† EDV (cm/s) 12.23 + 3.77 11.54 + 3.79 0.280 10.95 + 3.83 10.14 + 4.03 0.208 11.7 (5 – 23.1) 11 (4.4 – 21) 10.6 (4.5 – 24.7) 9.8 (4.1 – 23.3) DEDV 20.69 + 4.31 20.8 + 4.32 0.664†
Significant P values were written as bold
Paired samples T test or Wilcoxon signed rank tests were used for preoperative and postoperative comparisons †
Student’s T test or Mann-Whitney U tests were used for the comparison of DRI, DPI, DPSV, and DEDV values
cm/s, cantimeters/second, EDV, end-diastolic velocity; PI, pulsatility index; PSV, peak systolic velocity; RI, resistivity index; SD, standard deviation; D, mean difference between the postoperative and preoperative values ( postoperative minus preoperative value for the relevant parameter)
and non-operated kidneys were not statistically significant (Table 2). The mean RI and PI values for the groups categor-ized according to the operation status were illustrated in Figs. 2 and 3, respectively.
The change in mean RI, which was represented in current study as DRI, was only correlated with the parameters; “operative time” and “irrigation fluid volume” (Table 3). No significant relationship was documented between DRI and the other parameters; age, gender, side of ureteroscopy, stone location, and degree of hydronephrosis. On the other hand, none of the above parameters including operative time and irrigation fluid volume were not correlated with DPI, DPSV, and DEDV values.
Discussion
Despite its limitations in determining functional significance of obstructions, gray-scale US provides excellent anatomical information with nearly 100% specificity for the detection of
hydronephrosis (2, 11, 13 – 18). In recent years, the appli-cation of CDUS has gained importance in the assessment of genitourinary disorders. This imaging technique is non-invasive, rapidly performed, painless, and regarded as an inexpensive method (19, 20). However, the technique remains relatively subjective and time-consuming, requires technical expertise and high-quality equipment (21). As early in the course of obstruction, hydronephrosis may be absent or mild (grade 1), so functional evaluation of urinary tract during this period gains importance. For this purpose, scintigraphy has been used, but recently CDUS started to be used to obtain functional information. The reason why we excluded cases with grade 2 hydrone-phrosis was mainly due to our aim to evaluate those patients within the gray zone. In addition, as RI may be increased with marked increases in hydronephrosis, by excluding those cases, false increases in RIs were prevented in the current study (22). In a small series by Platt et al., RIs from 21 hydronephrotic kidneys were obtained before nephrostomy (23). The mean RI in 14 kidneys with con-firmed obstruction (0.77 + 0.04) was significantly higher than the mean RI from seven kidneys with non-obstructive pelvicaliectasis (0.64 + 0.04). Moreover, RI values returned to normal after nephrostomy. Later, the same authors pub-lished a study including 229 kidneys and proposed that the accuracy of the Doppler diagnosis of obstruction increased when the RI of the potentially obstructed kidney was com-pared with that of the unaffected contralateral kidney (16). However, we evaluated the contralateral kidneys, which were accepted as controls. Mean renal volumes between operated and contralateral kidneys were also comparable. Shokeir et al. examined 22 pregnant women with acute unilateral ureteric obstruction and concluded that mea-surements of the difference between the RI of the corre-sponding and contralateral kidney was a sensitive and specific test that could replace intravenous urography (24). More recently, Onur et al. revealed that the mean RI of obstructed kidneys was significantly greater than that of normal contralateral kidneys and concluded that CDUS could detect altered renal perfusion before pelvicalyceal system dilation start and distinguish obstructed cases (25).
Fig. 3 Renal pulsatility index (PI) values Fig. 2 Renal resistive index (RI) values
Table 3 Correlation of variables with mean DRI, DPI, DPSV, and DEDV values measured from the operated kidneys
Variables
Correlation
coefficient P value
Operative time DRI 0.539 0.004 DPI 0.296 0.143 DPSV 20.088 0.670 DEDV 20.367 0.065 Irrigation fluid volume DRI 0.404 0.041 DPI 0.169 0.408 DPSV 20.070 0.734 DEDV 20.263 0.194
Significant P values were written as bold
Spearman correlation coefficient analysis
EDV, end-diastolic velocity; PI, pulsatility index; PSV, peak systolic velocity; RI, resistivity index; D, mean difference between the postoperative and preoperative values ( postoperative minus preoperative value for the relevant parameter)
In the early 1990s, several groups postulated that the pathophysiology of urinary obstruction might be reliably manifested by changes in arterial Doppler spectra (16, 23, 26 –28). This application was based on exhaustive animal research that showed a unique biphasic hemodynamic response to complete ureteral obstruction. A short period (,2 h) of likely prostaglandin-mediated vasodilation occurs immediately after obstruction. After this period, renal blood flow decreases, and renal vascular resistance increases (29, 30). Initial studies suggested that this vaso-constriction response was primarily mechanical, due to increases in collecting system pressures. Recent research, however, suggests that complex interactions between several regulatory pathways (renin –angiotensin, kallik-rein – kinin, and prostaglandin – thromboxane) are respon-sible for intense, postobstructive renal vasoconstriction (3, 5, 31, 32). This vasoconstriction response, however mediated, seemed to be an ideal phenomenon to be detected by changes in the RI. Similarly, the PI was also used as pulsed-wave Doppler measurement of downstream renal artery resistance. Both PI and RI values have been found to correlate with renal vascular resistance, filtration fraction and effective renal plasma flow (33). In our study, besides RI measurement, we also preferred to evaluate PI, PSV and EDV values and investigated the changes on those parameters. However, only the changes in RI and PI values remained statistically significant between “operated kidney” and “contralateral normal kidney” groups (Table 2). When we assessed the correlations with double group combinations, the operative time and irrigation fluid volume were only found to be correlated with DRI (Table 3).
URS is the method of choice in the diagnosis and treat-ment of ureteral obstructions. With advances in endoscopic technology and endourological techniques, URS has become less invasive and less traumatic. Most of the time, a 9.5 F ureteroscope was used for initial diagnosis (visualization of an ureteral lumen) and treatment (ureteral stone disease management via laser system) if necessary. The procedure was carried out with warmed saline solution either without or with ureteric dilation (34). In our study, we used holmium laser for the elimination of stones. In seven (15%) cases, no stone was observed during URS operation. The procedure itself increased the RI and PI values signifi-cantly revealing that URS causes an increase in renal vascu-lar resistance.
During an URS operation, because of the irrigation fluid used, the irrigation pressures generated within the collect-ing system can be significantly elevated, and can even lead to pyelovenous and pyelolymphatic backflow. This backflow may create a pressure on the intrarenal vasculature and may also contribute to the increase in renal vascular resistance. In any way, the amount of the irrigation press-ures transmitted to the renal pelvis, collecting ducts and subsequently to the parenchyma determines the degree of the vasoconstrictive response that would eventually lead to an increase in RI values. Irrigation pressure is mainly affected by the amount of the irrigation fluid used, length of time period that the ureteroscope stayed within the ureter, and irrigation fluid height from the patient. In our
study population, since the height of the irrigation fluid was kept constant in all cases, main parameters involved in the etiology of this significant change were, any pro-longation of operative time and increase in the amount of irrigation fluid used. So, during an URS operation, the urol-ogist must be alert to the operative time and irrigation fluid consumed in order to prevent an increase in intrarenal vas-cular resistance (followed by a decrease in renal blood flow). Endourologists are already experienced in observing these two parameters during an operation, since their importance during a transurethral prostate resection operation are well documented (35). (Increase in these two parameters may cause transurethral resection syndrome which is a kind of dilutional hyponatremia).
Potential limitations to this study should be considered. First of all, one could reasonably offer to form an indepen-dent control group which was composed of non-operated healthy subjects. However, we thought that it would be more homogenous and reliable to evaluate the normal con-tralateral kidneys of the operated patients since we only included cases with unilateral obstructed systems and excluded patients with abnormal-looking dilated contralat-eral kidneys. As mentioned previously, renal vascular par-ameters may be affected by several competing factors like hormones ( prostaglandin) (3, 5, 31, 32, 36). Although, we did not find any study in the literature regarding renal Doppler changes in anesthetized patients, we were not sure that anesthetic agents would not affect RI and PI values. So, as many authors have suggested, we preferred to evaluate the contralateral kidneys as control group (24, 25, 34). Secondly, our sample size does not seem small con-sidering the literature related to our trial, but we hope pro-spective studies with larger series in near future may give more valuable data (2, 25, 34, 37, 38).
In conclusion, significant changes in RI and PI values in patients treated with URS revealed that URS operation itself is a functionally obstructing event and can cause sig-nificant increase in renal vascular resistance that may even-tually lead to a decrease in renal blood flow. With the increase in operative time and irrigation fluid volume used during the operation, renal vascular resistance (RI) seems to be significantly increased. Thus, we think that it would be better for an endourologist to manage URS oper-ations with minimum operative time available and, volume of irrigation fluid infused must be as low as possible. Conflict of interest:None.
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