- Email: [email protected]
Evaluation of Split Renal Function for Children with Kidney Diseases by Renal and Vascular Color Ultrasonography
ARTICLE IN PRESS Ultrasound in Med. & Biol., Vol. 00, No. 00, pp. 17, 2018 Copyright © 2018 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Printed in the USA. All rights reserved. 0301-5629/$ - see front matter
https://doi.org/10.1016/j.ultrasmedbio.2018.07.018
Original Contribution TAGEDH1EVALUATION OF SPLIT RENAL FUNCTION FOR CHILDREN WITH KIDNEY DISEASES BY RENAL AND VASCULAR COLOR ULTRASONOGRAPHYTAGEDN TAGEDPD1X XHUI ZHANG,D2X X*,y D3X XXUEXUE XING,D4XzX D5X XZHENG WANG,D6X X* and D7X XMIN HED8xX X TAGEDEN
* Department of Pediatrics, West China Second University Hospital of Sichuan University, Chengdu, China; y Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, China; z Jinan Central Hospital Affiliated to Shandong University, Jinan, China; and x Ultrasonic Department, West China Second University Hospital of Sichuan University, Chengdu, China (Received 8 September 2017; revised 17 July 2018; in final from 23 July 2018)
Abstract—Renal dynamic imaging and radionuclide renography use radioactivity to evaluate split renal function. We aimed to investigate the use of renal vascular color Doppler ultrasonography for evaluation of split renal function in children. Thirty-five children with unilateral kidney diseases were enrolled. For patients with unilateral renal tumor, peak systolic velocity (Vmax = 113.04 § 13.59 cm/s) and resistance index (RI = 0.73 § 0.02) were higher on abnormal compared with normal sides (Vmax = 86.03 § 6.49 cm/s, RI = 0.62 § 0.01), and blood perfusion was good, indicating compensatory enhancement in split renal function. For unilateral renal cyst, Vmax (58.20 § 7.38 cm/s) was lower on the abnormal compared with the normal (87.71 § 14.83 cm/s) size, and perfusion was poor. For unilateral hydronephrosis and renal atrophy, the parameters were similar to those of renal cyst, suggesting a weakening of renal function. For unilateral renal agenesis, Vmax (106.07 § 13.07 cm/s) and RI (0.71 § 0.05) were higher, and perfusion was good. Renal vascular color Doppler ultrasonography was superior in the evaluation of split renal function in children, without being invasive or radioactive. (E-mail: [email protected]) © 2018 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Key Words: Split renal function, Vascular color Doppler ultrasonography, Children, Kidney disease.
TAGEDH1INTRODUCTIONTAGEDN
medications (Agarwal et al. 2005; Perez Calvo et al. 2017). Although renal biopsy is the standard method for early diagnosis and assessment of the degree of kidney injury, this invasive operation still cannot evaluate split renal function. Moreover, renal biopsy has several adverse effects, including hematuria, perirenal hematoma, arteriovenous fistula and infection (Ellis et al. 2017; Joseph et al. 2007). Radionuclide renography is commonly used to detect split renal function by means of renal plasma volume, secretion function of renal tubules, void volume and urinary excretion. However, this method has many disadvantages in clinical practice (Biassoni and Easty 2017). For example, the imaging findings of radionuclide renography are non-specific for etiologic diagnosis and lesion character in many circumstances. In addition, many factors influence this technology, such as the quality of the radioactive nuclide, the velocity of the urinary stream, the use of diuretics, mental stress and pain (Biassoni and Easty 2017; Fommei and Volterrani 1995; Niemczyk et al. 1999).
The traditional laboratory parameters of serum creatinine (Cr), blood urea nitrogen (BUN) and glomerular filtration rate (GFR) have been used to evaluate renal function (Joseph et al. 2007; Perez Calvo et al. 2017). When one kidney has been damaged, the other can maintain normal function through compensation, and Cr, BUN and GFR can be sustained within normal ranges for a period. However, Cr and BUN reflect only the total function of kidneys. Eventually, decompensation occurs, characterized by a marked decline in GFR and increased Cr and BUN. These traditional laboratory findings do not truly reflect the degree of kidney injury in the early period and lack the ability to assess split renal function. In addition, they are easily affected by various factors— for example, watersodium balance, nutrition status and Address correspondence to: Hui Zhang, No 20, Section 3, Renmin Nanlu, West China Second University Hospital of Sichuan University, Chengdu 610041, China. E-mail: [email protected] Conflict of interest disclosure: We declare no competing interests.
1
ARTICLE IN PRESS 2
Ultrasound in Medicine & Biology
Currently, the most common method of evaluating split renal function is renal dynamic imaging, which is superior to radionuclide renography in some aspects (Biassoni and Easty 2017; Koff et al. 1980; O’Reilly 2003). However, all of the above methods rely on radioactivity and are invasive; even contrast substances can have side effects on the kidneys, perhaps leading to exacerbation of the disease, especially for patients with renal failure. These challenges have compelled pediatric nephrologists to pay close attention to determining the most optimal method to evaluate split renal function with minimum adverse effects and maximum detectability, especially for children. Routine renal ultrasonography (US) can clearly display the anatomic structure of the kidney in 2-D imaging mode, but it is of no help for the evaluation of renal function (Gudinchet et al. 1994; Niesen et al. 2017). However, renal vascular color Doppler US allows real-time spatial visualization of blood flow patterns in the kidney, which includes color Doppler image formation (CDFI), color Doppler energy (CDE) images and pulse Doppler, which have high sensitivity and tolerability in the evaluation of kidney injury by observation of renal blood flow, blood perfusion and spectral shape (Platt et al. 1999; Splendiani et al. 2002; Yang and Room 2017). If combined with routine renal US, renal vascular color Doppler US is likely to be a good choice for evaluation of split renal function as a non-invasive and non-radioactive method, making it an ideal tool for use in pediatric screening programs. Unfortunately, few data are available on the use of this method for the assessment of split renal function in children with kidney diseases (Yang and Room 2017). Thus we aimed to evaluate the values of renal vascular color Doppler US combined with routine US for evaluation of split renal function in children. TAGEDH1METHODSTAGEDN Thirty-five children with unilateral kidney diseases (including tumor, cyst, hydronephrosis, agenesis and atrophy) were enrolled in this study between 2012 and 2017. Initial diagnosis was made by routine renal ultrasound and confirmed by renal computed tomography scans. All parents or guardians of patients provided written informed consent. This study was approved by our university’s ethics committee. Biochemical tests including Cr and BUN were performed at the beginning of the study. In addition, renal vascular color Doppler US combined with routine US was performed for each patient by the same doctor and with the same device (Siemens Sequoia 512 ultrasound system and a 2- to 5-MHz transducer; Siemens, Mountain View, CA, USA). The
Volume 00, Number 00, 2018
examining doctor did not know whether the left or right kidney was previously abnormal. During the ultrasound, patients were asked to hold their breath to keep the probe from moving. Detection began with observation of the renal structure. Next, renal blood perfusion was assessed with CDE, which can evaluate the distribution of renal blood flow, characteristics of spectral shape and vessel filling. It can also display blood flow information of the small vessels (Crutchley et al. 2009; Mostbeck et al. 1991; Nosadini et al. 2006). The results of this detection can be classified into four grades with respect to renal blood perfusion (Fig. 1): In grade I, the main renal arteries, segmental arteries and interlobar arteries appear clearly, with continuous arcuate arteries, and interlobular arteries have abundant blood flow distributed through the renal cortex to the subrenal capsule. In grade II, all renal arteries are clear, except for the interlobular arteries, which have little color signal distributed through onethird to two-thirds of the renal cortex. In grade III, the main renal arteries and segmental arteries are clear, but interlobar arteries are not, with discontinuous arcuate arteries. And in grade IV, the main renal arteries and segmental arteries are also clear, with no color signal from other small arteries. Lastly, the hemodynamic conditions of the main renal arteries, segmental arteries and interlobar arteries were assessed using parameters such as peak systolic velocity (Vmax), diastolic minimum velocity (Vmin) and resistance index (RI), which are regarded as potential indicators for monitoring the progression of renal damage and renal function (Chen et al. 2014; Splendiani et al. 2002). Vmax, as well as RI, is a well-documented index for the evaluation of renal hemodynamics and renal function (Crutchley et al. 2009; Nosadini et al. 2006). Statistical analysis Results are expressed as the mean § standard deviation and percentage. Statistical analyses were done with SPSS software (Version 19.0, IBM, Armonk, NY, USA). The measured parameters of the two groups were compared with the x2 test for categorical data, and continuous measurements were compared by variance analysis. All reported p values < 0.05 were considered to indicate statistical significance. TAGEDH1RESULTSTAGEDN In this study, all patients had normal GFRs. The clinical information of the patients is outlined in Table 1. For patients with unilateral renal tumor (n = 6), both Vmax (113.04 § 13.59 cm/s) and RI (0.73 § 0.02) of the main renal arteries were significantly higher on the abnormal side compared with the normal side (Vmax = 86.03 § 6.49 cm/s, RI = 0.62 § 0.01), indicating
ARTICLE IN PRESS
Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al.
Fig. 1. Color Doppler energy imaging findings with respect to grade. (a) Grade I: The main renal arteries, segmental arteries and interlobar arteries appear clearly, with continuous arcuate arteries, and the interlobular arteries have abundant blood flow distributed through the renal cortex to the subrenal capsule. (b) Grade II: All renal arteries are clear, except for the interlobular arteries, which have a rare color signal distributed through one-third to two-thirds of the renal cortex. (c) Grade III: The main renal arteries and segmental arteries are clear, but the interlobar arteries are not, with discontinuous arcuate arteries. (d) Grade IV: The main renal arteries and segmental arteries are also clear, with no color signal of other small arteries.
3
ARTICLE IN PRESS 4
Ultrasound in Medicine & Biology
Volume 00, Number 00, 2018
Table 1. Clinical characteristics of 35 patients with unilateral renal malformations Case
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35
Gender
M M M F M F M F M F F M M F F M M F F F M F M M M F F F F M M M M M F
Age (y)
7.14 8.53 6.25 6.78 9.17 7.84 6.42 7.40 6.05 7.47 5.04 6.12 6.92 6.31 8.45 8.35 7.35 6.94 7.48 6.90 8.03 7.84 7.15 7.07 6.73 7.33 5.98 6.56 5.95 7.18 5.88 8.19 5.85 6.07 8.99
Diagnosis
Tumor of left kidney Tumor of left kidney Tumor of right kidney Tumor of right kidney Tumor of right kidney Tumor of right kidney Cyst of left kidney Cyst of right kidney Cyst of left kidney Cyst of right kidney Cyst of left kidney Cyst of left kidney Cyst of right kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Agenesis of right kidney Agenesis of right kidney Agenesis of right kidney Agenesis of left kidney Agenesis of left kidney Agenesis of left kidney Agenesis of left kidney Atrophy of right kidney Atrophy of right kidney Atrophy of right kidney Atrophy of left kidney Atrophy of left kidney
BUN (mmol/L)
4.01 3.88 5.02 6.12 6.13 5.32 7.33 4.23 5.28 5.02 4.96 4.37 5.32 4.09 6.68 5.43 3.38 4.78 4.93 3.96 5.68 4.75 5.09 6.12 6.61 5.28 5.08 3.72 6.17 5.13 4.72 6.77 6.06 3.60 5.90
Cr (mmol/L)
31.1 39.8 48.0 51.2 54.2 49.4 42.4 36.3 48.4 46.8 45.2 38.6 50.3 39.5 48.9 33.5 46.2 37.5 42.5 41.0 49.2 39.1 46.7 53.8 68.5 48.3 58.0 36.3 53.7 43.8 52.8 51.6 50.7 51.0 62.0
Normal kidney
Abnormal kidney
Vmax (cm/s)
RI
CDE
Vmax (cm/s)
RI
CDE
78.90 80.12 86.02 97.04 87.90 86.20 57.92 102.08 99.66 91.54 82.06 93.65 87.03 96.24 97.33 89.99 54.00 89.36 83.05 64.12 75.88 95.43 90.61 110.56 104.00 91.60 103.00 89.69 124.70 118.94 146.00 119.00 81.53 87.17 81.40
0.62 0.61 0.62 0.62 0.61 0.63 0.64 0.60 0.61 0.62 0.63 0.62 0.61 0.61 0.61 0.79 0.66 0.63 0.65 0.69 0.69 0.65 0.66 0.69 0.71 0.70 0.72 0.62 0.78 0.73 0.74 0.61 0.82 0.68 0.59
I I I I I I I I I I I I I I I I II I I II I I I I I I I I I II I I I I I
96.54 95.86 114.68 126.05 121.30 123.80 47.51 52.35 67.09 61.08 56.14 55.98 67.23 68.15 66.43 69.03 32.00 54.82 64.92 45.14 58.97 67.05 59.55 — — — — — — — 45.00 73.00 54.97 56.55 19.38
0.74 0.75 0.71 0.74 0.72 0.74 0.59 0.62 0.61 0.69 0.67 0.66 0.63 0.68 0.65 0.68 0.69 0.61 0.67 0.69 0.68 0.66 0.67 — — — — — — — 0.71 0.59 0.88 0.67 0.63
II II I I I I II III II II II II II III III II III II II III II II II — — — — — — — II III II II III
Cr = serum creatinine; BUN, blood urea nitrogen; Vmax = peak systolic velocity; RI = resistance index; CDE = color Doppler energy; GFR = glomerular filtration rate.
the compensatory enhancement of residual renal function. The reason might be that the tumor was rich in vascular tissue, leading to rich blood flow, and overload of renal capillary volume could induce increased vascular resistance. Interestingly, blood perfusion of the abnormal side was as good as that of the normal side, generally with a CDE of grade I or II. For unilateral renal cysts (n = 7), Vmax (58.20 § 7.38 cm/s) values were much lower on the abnormal side than on the normal side (87.71 § 14.83 cm/s), with low blood flow and normal vascular resistance. There was no difference between RIs (abnormal side: 0.63 § 0.03, normal side: 0.61 § 0.01). In addition, blood perfusion was poor compared with the normal side, with CDE generally grade II or III. The reason might be that the cyst lacked vascular tissue and there was local compression to normal tissue, suggesting a weakening of residual renal function. With reference to unilateral hydronephrosis (n = 10), the hemodynamic parameters (abnormal side:
Vmax = 58.61 § 11.91 cm/s, RI = 0.67 § 0.02; normal side: Vmax = 83.60 § 14.63 cm/s, RI = 0.66 § 0.05) were similar to those of renal cysts. Most patients had CDE grade II or III because of the local compression to normal tissue. As for unilateral renal agenesis (n = 7), both Vmax (106.07 § 13.07 cm/s) and RI (0.71 § 0.05) of the residual kidneys were higher, implicating the compensatory enhancement of renal function. Blood perfusion was good, with CDE grade I or II. In addition, the defective kidney had no color signal on display, indicating neither blood perfusion nor renal function. With respect to unilateral renal atrophy (n = 5), Vmax (49.78 § 19.74 cm/s) of the abnormal side was much lower compared with that of the normal side (Vmax = 103.02 § 28.65 cm/s). However, RI appeared not to differ between the normal (0.69 § 0.09) and abnormal (0.70 § 0.11) sides. In addition, blood perfusion of the abnormal side was poorer than that of the normal side, generally with CDE grade II or III. The reason
ARTICLE IN PRESS Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al.
might be congenital anomalies of renal structure resulting in a weakening of renal function. TAGEDH1DISCUSSIONTAGEDN Renal vascular color Doppler US combined with routine US is a non-invasive and non-radioactive method for evaluating kidney structure and hemodynamics. This method has been reported to be very useful in screening for various kinds of kidney diseases (Kim et al. 1992; Mostbeck et al. 1991; Ozbek 1992; Yang and Room 2017). However, few authors have used this method to study the function of a single kidney (Gudinchet et al. 1994). US has been reported to be a reliable method for evaluation of renal function, and different measurements have been proposed, such as hemodynamic parameters (Niesen et al. 2017; Yang and Room 2017). First, routine renal US can be used to observe the structure of the urinary tract, identifying whether the urinary tract has an obstruction or other structural abnormalities, which is similar to the excretory curve of radionuclide renography. Second, renal vascular color Doppler US allows determination of semi-quantitative parameters, such as RI, which provides details on vascular resistance, and this is inversely related to renal blood flow (He et al. 2017; Norris and Barnes 1984). Certain studies have indicated that higher RI is related to
5
thickening of the renal small vessel wall, glomerular sclerosis or degenerative change (He et al. 2017; Kasiske and Umen 1986), implicating aggravation of kidney damage and poor prognosis. Vmax directly reflects the degree of renal vascular filling and blood supply, which is negatively correlated with the degree of kidney damage. Lastly, renal vascular color Doppler US can be also beneficial in evaluating renal perfusion. For example, CDFI can display the direction of blood flow and the number, shape and size of blood vessels and blood flow distribution in different organs. However, CDFI results are easily affected by the angle of insonation, with poor sensitivity and continuity. In our study, CDE imaging proved to be a useful technology based on the total integral of the energy frequency spectrum. It detects blood flow using the energy of moving reflectors and has the advantages of high sensitivity to slow blood flow, while providing a less cluttered image and being less dependent on angles (Hamper et al. 1993; He et al. 2017). The results of our study indicated that there were obvious changes in hemodynamic tests and CDE grades between the left and right kidneys of patients with unilateral kidney diseases. Based on these differences, we can preliminarily assess split renal function. Compared with radionuclide renography, renal vascular color Doppler US lacks the ability to evaluate renal tubule function. However, radionuclide renography
Table 2. Comparison of common methods used for evaluation of split renal function RVCDUS + RUS
Radionuclide renography
Universality of method
New proposed method
Old and traditional method Yes Yes Reserve, decay and waste disposal of radionuclide No Yes
Radioactivity Radionuclide
No No
Contrast agent Side effects for kidney and/ or other organs Convenience
No No Yes
No Radionuclide injection needed Observation time limited
Cost Requirement for devices Characteristics of renal lesion, such as tumor, cyst Range of application GFR of single kidney
Cheap Moderate Clear
Cheap Specific device Unclear
Wide No Hemodynamic indexes (Vmax, RI, PI), CDE grades; further need to make split GFR
Wide No Three curves (vascular, secretary, excretory)
Renal dynamic imaging
Enhanced CT
Recognized method
Poor universality
Yes Yes Reserve, decay and waste disposal of radionuclide No Yes
Yes No
Yes Yes
No Radionuclide injection needed Observation time limited Time consuming Expensive High Unclear
Expensive High Clear
Wide Yes
Narrow Yes
No Contrast agent injection needed Complicated calculation method for GFR
RVCDUS = renal vascular color Doppler ultrasonography; RUS = routine ultrasonography; CT = computed tomography; GFR = glomerular filtration rate; Vmax = peak systolic velocity; RI = resistance index; PI = pulsatility index; CDE = Color Doppler energy image.
ARTICLE IN PRESS 6
Ultrasound in Medicine & Biology
cannot reflect renal damage in the early day (Biassoni and Easty 2017). Currently, the most common method used to evaluate split renal function is renal dynamic imaging, and other imaging techniques have been used to assess renal function, such as enhanced CT (Alexander et al. 2010; Prassopoulos et al. 1992, 1993). Comparison of these methods used for the evaluation of split renal function is documented in Table 2. Renal vascular color Doppler US is more likely to analyze the development of kidney disease in a timely and objective way via monitoring for renal hemodynamic changes, providing quantitative indicators for the disease in clinical practice. When dysfunction occurs in a single kidney, traditional laboratory indexes are likely to be in the normal range, while Vmax, RI and CDE have changed, easily reflecting the degree of renal damage. In the compensatory period of renal function, because the damage to renal units and the small artery is slight, the injured kidney is rich in blood flow, and the complete renal vascular tree can be clearly displayed. In the azotemia period, the endogenous creatinine clearance rate of patients with decompensation of renal function decreases, and serum Cr and BUN increase markedly, aggravating the damage to the renal arteriole, which leads to discontinuation of blood flow signals. At this time, the main renal arteries and segmental arteries can be displayed on a scan, but the signals of the interlobular arteries and arcuate artery are distributed in a stellate fashion. In uremia, the blood perfusion of patients is reduced significantly, accompanied by aggravation of renal damage. The signals of the interlobular arteries and arcuate arteries disappear, and the blood flow signal of the segmental artery is discontinuous. This study had some limitations. The most noteworthy is that the sample size was small in each group. An increase in cases would make the results of the study more persuasive.
TAGEDH1CONCLUSIONSTAGEDN As a non-invasive and non-radioactive examination method, renal vascular color Doppler US combined with routine US is an appropriate method for evaluation of single-kidney function and may be useful in detecting early damage caused by kidney disease. This method is likely superior to radionuclide renography and may even replace it in the evaluation of split renal function in children. However, larger studies should be performed to increase our knowledge about these patients.
Acknowledgments—H.Z. has received a grant from the foundation of the Medical Association of Sichuan Province (Grant S16052).
Volume 00, Number 00, 2018
TAGEDH1REFERENCESTAGEDN Agarwal SK, Dash SC, Irshad M, Raju S, Singh P, Pandey RM. Prevalence of chronic renal failure in adults in Delhi, India. Nephrol Dial Transplant 2005;20:1638–1642. Alexander K, Dunn M, Carmel EN, Lavoie JP, Del Castillo JR. Clinical application of Patlak plot CT-GFR in animals with upper urinary tract disease. Vet Radiol Ultrasound 2010;51:421–427. Biassoni L, Easty M. Paediatric nuclear medicine imaging. Br Medical Bulletin 2017;123:127. Chen Q, He F, Feng X, Luo Z, Zhang J, Zhang L, Wang Y, Tong J. Correlation of Doppler parameters with renal pathology: A study of 992 patients. Exp Ther Med 2014;7:439–442. Crutchley TA, Pearce JD, Craven TE, Stafford JM, Edwards MS, Hansen KJ. Clinical utility of the resistive index in atherosclerotic renovascular disease. J Vasc Surg 2009;49:148–155. Ellis RJ, Joshi A, Ng KL, Francis RS, Gobe GC, Wood ST. Optimising assessment of kidney function when managing localised renal masses. Med J Aust 2017;207:127. Fommei E, Volterrani D. Renal nuclear medicine. Semin Nucl Med 1995;25:183–194. Gudinchet F, Meuli R, Regazzoni B. Compensatory renal growth in children and adults studied by Doppler sonography. J Clin Ultrasound 1994;22:11–15. Hamper UM, Sheth S, Abbas FM, Rosenshein NB, Aronson D, Kurman RJ. Transvaginal color Doppler sonography of adnexal mases: Differences in blood flow independence in benign and malignant lesions. AJR Am J Roentgenol 1993;160:225. He X, Guan B, Zhu L. Hemodynamics as measured with color doppler sonography in early-stage obesity-related nephropathy in children. J Ultrasound Med 2017;36:1671–1677. Joseph A, Vassalotti LesleyA, Stevens AndrewS, Levey. Testing for chronic kidney disease: A Position Statement from the National Kidney Foundation. Am J Kidney Dis 2007;50:169–180. Kasiske BL, Umen AJ. The influence of age, sex, race, and body habitus on kidney weight in humans. Arch Pathol Lab Med 1986;110:55–60. Kim SH, Kim H, Choi BI, Kim CW. Duplex Doppler US in patients with medical renal disease: resistive index vs serum creatinine level. Clin Radiol 1992;45:85–87. Koff SA, Thrall JH, Keyes JW. Assessment of hydroureteronephrosis in children using diuretic radionuclide urography. J Urol 1980;123:531–534. Mostbeck GH, Kain R, Mallek R, Derfler K, Walter R, Havelec L, Tscholakoff D. Duplex Doppler sonography in renal parenchymal disease. J Ultrasound Med 1991;10:189–194. Norris CS, Barnes RW. Renal artery flow velocity analysis: A sensitive measure of experimental and clinical renovascular resistance. J Surg Res 1984;36:230–236. Niemczyk P, Krisch EB, Zeiger L, Marmar JL. Use of diuretic renogram in evaluation of patients before and after endopyelotomy. Urology 1999;53:271–275. Nosadini R, Velussi M, Brocco E, Abaterusso C, Carraro A, Piarulli F, Morgia G, Satta A, Faedda R, Abhyankar A, Luthman H, Tonolo G. Increased renal arterial resistance predicts the course of renal function in type 2 diabetes with microalbuminuria. Diabetes 2006;55: 234–239. Niesen TJ, Finch N, Gakhal M, Dressler RM, Levy HM. Value of prior imaging review before ordering renal sonography in the evaluation of abnormal renal function. J Clin Ultrasound 2017;45:537–541. O’Reilly PH. for the Consensus Committee of the Society of Radionuclides in Nephrourology. Standardisation of the renogram technique for investigating the dilated upper urinary tract and assessing the results of surgery. BJU Int 2003;91:239–243. Ozbek SS. Duplex Doppler US in medical renal disease. Clin Radiol 1992;46:219–220. Perez Calvo JI, Josa LC, Gimenez LI. Renal function assessment in heart failure. Rev Clin Esp 2017;217:267. Platt JF, Rubin JM, Ellis JH. Diabetic nephropathy: Evaluation with renal duplex Doppler. Radiology 1999;190:343–346.
ARTICLE IN PRESS Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al. Prassopoulos P, Gourtsoyiannis N, Cavouras D, Pantelidis N. CT evaluation of compensatory renal growth in relation to postnephrectomy time. Acta Radiol 1992;33:566–568. Prassopoulos P, Cavouras D, Gourtsoyiannis N. Pre- and post-nephrectomy kidney enlargement in patients with contralateral renal cancer. Eur Urol 1993;24:58–61.
7
Splendiani G, Parolini C, Fortunato L, Sturniolo A, Costanzi S. Resistive index in chronic nephropathies: Predictive value of renal outcome. Clin Nephrol 2002;57:45–50. Yang X, Room BU. Clinical effect of color Doppler ultrasound on patients with chronic renal failure. China Continuing Med Educ 2017;9:75–76.
https://doi.org/10.1016/j.ultrasmedbio.2018.07.018
Original Contribution TAGEDH1EVALUATION OF SPLIT RENAL FUNCTION FOR CHILDREN WITH KIDNEY DISEASES BY RENAL AND VASCULAR COLOR ULTRASONOGRAPHYTAGEDN TAGEDPD1X XHUI ZHANG,D2X X*,y D3X XXUEXUE XING,D4XzX D5X XZHENG WANG,D6X X* and D7X XMIN HED8xX X TAGEDEN
* Department of Pediatrics, West China Second University Hospital of Sichuan University, Chengdu, China; y Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, China; z Jinan Central Hospital Affiliated to Shandong University, Jinan, China; and x Ultrasonic Department, West China Second University Hospital of Sichuan University, Chengdu, China (Received 8 September 2017; revised 17 July 2018; in final from 23 July 2018)
Abstract—Renal dynamic imaging and radionuclide renography use radioactivity to evaluate split renal function. We aimed to investigate the use of renal vascular color Doppler ultrasonography for evaluation of split renal function in children. Thirty-five children with unilateral kidney diseases were enrolled. For patients with unilateral renal tumor, peak systolic velocity (Vmax = 113.04 § 13.59 cm/s) and resistance index (RI = 0.73 § 0.02) were higher on abnormal compared with normal sides (Vmax = 86.03 § 6.49 cm/s, RI = 0.62 § 0.01), and blood perfusion was good, indicating compensatory enhancement in split renal function. For unilateral renal cyst, Vmax (58.20 § 7.38 cm/s) was lower on the abnormal compared with the normal (87.71 § 14.83 cm/s) size, and perfusion was poor. For unilateral hydronephrosis and renal atrophy, the parameters were similar to those of renal cyst, suggesting a weakening of renal function. For unilateral renal agenesis, Vmax (106.07 § 13.07 cm/s) and RI (0.71 § 0.05) were higher, and perfusion was good. Renal vascular color Doppler ultrasonography was superior in the evaluation of split renal function in children, without being invasive or radioactive. (E-mail: [email protected]) © 2018 World Federation for Ultrasound in Medicine & Biology. All rights reserved. Key Words: Split renal function, Vascular color Doppler ultrasonography, Children, Kidney disease.
TAGEDH1INTRODUCTIONTAGEDN
medications (Agarwal et al. 2005; Perez Calvo et al. 2017). Although renal biopsy is the standard method for early diagnosis and assessment of the degree of kidney injury, this invasive operation still cannot evaluate split renal function. Moreover, renal biopsy has several adverse effects, including hematuria, perirenal hematoma, arteriovenous fistula and infection (Ellis et al. 2017; Joseph et al. 2007). Radionuclide renography is commonly used to detect split renal function by means of renal plasma volume, secretion function of renal tubules, void volume and urinary excretion. However, this method has many disadvantages in clinical practice (Biassoni and Easty 2017). For example, the imaging findings of radionuclide renography are non-specific for etiologic diagnosis and lesion character in many circumstances. In addition, many factors influence this technology, such as the quality of the radioactive nuclide, the velocity of the urinary stream, the use of diuretics, mental stress and pain (Biassoni and Easty 2017; Fommei and Volterrani 1995; Niemczyk et al. 1999).
The traditional laboratory parameters of serum creatinine (Cr), blood urea nitrogen (BUN) and glomerular filtration rate (GFR) have been used to evaluate renal function (Joseph et al. 2007; Perez Calvo et al. 2017). When one kidney has been damaged, the other can maintain normal function through compensation, and Cr, BUN and GFR can be sustained within normal ranges for a period. However, Cr and BUN reflect only the total function of kidneys. Eventually, decompensation occurs, characterized by a marked decline in GFR and increased Cr and BUN. These traditional laboratory findings do not truly reflect the degree of kidney injury in the early period and lack the ability to assess split renal function. In addition, they are easily affected by various factors— for example, watersodium balance, nutrition status and Address correspondence to: Hui Zhang, No 20, Section 3, Renmin Nanlu, West China Second University Hospital of Sichuan University, Chengdu 610041, China. E-mail: [email protected] Conflict of interest disclosure: We declare no competing interests.
1
ARTICLE IN PRESS 2
Ultrasound in Medicine & Biology
Currently, the most common method of evaluating split renal function is renal dynamic imaging, which is superior to radionuclide renography in some aspects (Biassoni and Easty 2017; Koff et al. 1980; O’Reilly 2003). However, all of the above methods rely on radioactivity and are invasive; even contrast substances can have side effects on the kidneys, perhaps leading to exacerbation of the disease, especially for patients with renal failure. These challenges have compelled pediatric nephrologists to pay close attention to determining the most optimal method to evaluate split renal function with minimum adverse effects and maximum detectability, especially for children. Routine renal ultrasonography (US) can clearly display the anatomic structure of the kidney in 2-D imaging mode, but it is of no help for the evaluation of renal function (Gudinchet et al. 1994; Niesen et al. 2017). However, renal vascular color Doppler US allows real-time spatial visualization of blood flow patterns in the kidney, which includes color Doppler image formation (CDFI), color Doppler energy (CDE) images and pulse Doppler, which have high sensitivity and tolerability in the evaluation of kidney injury by observation of renal blood flow, blood perfusion and spectral shape (Platt et al. 1999; Splendiani et al. 2002; Yang and Room 2017). If combined with routine renal US, renal vascular color Doppler US is likely to be a good choice for evaluation of split renal function as a non-invasive and non-radioactive method, making it an ideal tool for use in pediatric screening programs. Unfortunately, few data are available on the use of this method for the assessment of split renal function in children with kidney diseases (Yang and Room 2017). Thus we aimed to evaluate the values of renal vascular color Doppler US combined with routine US for evaluation of split renal function in children. TAGEDH1METHODSTAGEDN Thirty-five children with unilateral kidney diseases (including tumor, cyst, hydronephrosis, agenesis and atrophy) were enrolled in this study between 2012 and 2017. Initial diagnosis was made by routine renal ultrasound and confirmed by renal computed tomography scans. All parents or guardians of patients provided written informed consent. This study was approved by our university’s ethics committee. Biochemical tests including Cr and BUN were performed at the beginning of the study. In addition, renal vascular color Doppler US combined with routine US was performed for each patient by the same doctor and with the same device (Siemens Sequoia 512 ultrasound system and a 2- to 5-MHz transducer; Siemens, Mountain View, CA, USA). The
Volume 00, Number 00, 2018
examining doctor did not know whether the left or right kidney was previously abnormal. During the ultrasound, patients were asked to hold their breath to keep the probe from moving. Detection began with observation of the renal structure. Next, renal blood perfusion was assessed with CDE, which can evaluate the distribution of renal blood flow, characteristics of spectral shape and vessel filling. It can also display blood flow information of the small vessels (Crutchley et al. 2009; Mostbeck et al. 1991; Nosadini et al. 2006). The results of this detection can be classified into four grades with respect to renal blood perfusion (Fig. 1): In grade I, the main renal arteries, segmental arteries and interlobar arteries appear clearly, with continuous arcuate arteries, and interlobular arteries have abundant blood flow distributed through the renal cortex to the subrenal capsule. In grade II, all renal arteries are clear, except for the interlobular arteries, which have little color signal distributed through onethird to two-thirds of the renal cortex. In grade III, the main renal arteries and segmental arteries are clear, but interlobar arteries are not, with discontinuous arcuate arteries. And in grade IV, the main renal arteries and segmental arteries are also clear, with no color signal from other small arteries. Lastly, the hemodynamic conditions of the main renal arteries, segmental arteries and interlobar arteries were assessed using parameters such as peak systolic velocity (Vmax), diastolic minimum velocity (Vmin) and resistance index (RI), which are regarded as potential indicators for monitoring the progression of renal damage and renal function (Chen et al. 2014; Splendiani et al. 2002). Vmax, as well as RI, is a well-documented index for the evaluation of renal hemodynamics and renal function (Crutchley et al. 2009; Nosadini et al. 2006). Statistical analysis Results are expressed as the mean § standard deviation and percentage. Statistical analyses were done with SPSS software (Version 19.0, IBM, Armonk, NY, USA). The measured parameters of the two groups were compared with the x2 test for categorical data, and continuous measurements were compared by variance analysis. All reported p values < 0.05 were considered to indicate statistical significance. TAGEDH1RESULTSTAGEDN In this study, all patients had normal GFRs. The clinical information of the patients is outlined in Table 1. For patients with unilateral renal tumor (n = 6), both Vmax (113.04 § 13.59 cm/s) and RI (0.73 § 0.02) of the main renal arteries were significantly higher on the abnormal side compared with the normal side (Vmax = 86.03 § 6.49 cm/s, RI = 0.62 § 0.01), indicating
ARTICLE IN PRESS
Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al.
Fig. 1. Color Doppler energy imaging findings with respect to grade. (a) Grade I: The main renal arteries, segmental arteries and interlobar arteries appear clearly, with continuous arcuate arteries, and the interlobular arteries have abundant blood flow distributed through the renal cortex to the subrenal capsule. (b) Grade II: All renal arteries are clear, except for the interlobular arteries, which have a rare color signal distributed through one-third to two-thirds of the renal cortex. (c) Grade III: The main renal arteries and segmental arteries are clear, but the interlobar arteries are not, with discontinuous arcuate arteries. (d) Grade IV: The main renal arteries and segmental arteries are also clear, with no color signal of other small arteries.
3
ARTICLE IN PRESS 4
Ultrasound in Medicine & Biology
Volume 00, Number 00, 2018
Table 1. Clinical characteristics of 35 patients with unilateral renal malformations Case
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35
Gender
M M M F M F M F M F F M M F F M M F F F M F M M M F F F F M M M M M F
Age (y)
7.14 8.53 6.25 6.78 9.17 7.84 6.42 7.40 6.05 7.47 5.04 6.12 6.92 6.31 8.45 8.35 7.35 6.94 7.48 6.90 8.03 7.84 7.15 7.07 6.73 7.33 5.98 6.56 5.95 7.18 5.88 8.19 5.85 6.07 8.99
Diagnosis
Tumor of left kidney Tumor of left kidney Tumor of right kidney Tumor of right kidney Tumor of right kidney Tumor of right kidney Cyst of left kidney Cyst of right kidney Cyst of left kidney Cyst of right kidney Cyst of left kidney Cyst of left kidney Cyst of right kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of right kidney Hydronephrosis of left kidney Hydronephrosis of left kidney Agenesis of right kidney Agenesis of right kidney Agenesis of right kidney Agenesis of left kidney Agenesis of left kidney Agenesis of left kidney Agenesis of left kidney Atrophy of right kidney Atrophy of right kidney Atrophy of right kidney Atrophy of left kidney Atrophy of left kidney
BUN (mmol/L)
4.01 3.88 5.02 6.12 6.13 5.32 7.33 4.23 5.28 5.02 4.96 4.37 5.32 4.09 6.68 5.43 3.38 4.78 4.93 3.96 5.68 4.75 5.09 6.12 6.61 5.28 5.08 3.72 6.17 5.13 4.72 6.77 6.06 3.60 5.90
Cr (mmol/L)
31.1 39.8 48.0 51.2 54.2 49.4 42.4 36.3 48.4 46.8 45.2 38.6 50.3 39.5 48.9 33.5 46.2 37.5 42.5 41.0 49.2 39.1 46.7 53.8 68.5 48.3 58.0 36.3 53.7 43.8 52.8 51.6 50.7 51.0 62.0
Normal kidney
Abnormal kidney
Vmax (cm/s)
RI
CDE
Vmax (cm/s)
RI
CDE
78.90 80.12 86.02 97.04 87.90 86.20 57.92 102.08 99.66 91.54 82.06 93.65 87.03 96.24 97.33 89.99 54.00 89.36 83.05 64.12 75.88 95.43 90.61 110.56 104.00 91.60 103.00 89.69 124.70 118.94 146.00 119.00 81.53 87.17 81.40
0.62 0.61 0.62 0.62 0.61 0.63 0.64 0.60 0.61 0.62 0.63 0.62 0.61 0.61 0.61 0.79 0.66 0.63 0.65 0.69 0.69 0.65 0.66 0.69 0.71 0.70 0.72 0.62 0.78 0.73 0.74 0.61 0.82 0.68 0.59
I I I I I I I I I I I I I I I I II I I II I I I I I I I I I II I I I I I
96.54 95.86 114.68 126.05 121.30 123.80 47.51 52.35 67.09 61.08 56.14 55.98 67.23 68.15 66.43 69.03 32.00 54.82 64.92 45.14 58.97 67.05 59.55 — — — — — — — 45.00 73.00 54.97 56.55 19.38
0.74 0.75 0.71 0.74 0.72 0.74 0.59 0.62 0.61 0.69 0.67 0.66 0.63 0.68 0.65 0.68 0.69 0.61 0.67 0.69 0.68 0.66 0.67 — — — — — — — 0.71 0.59 0.88 0.67 0.63
II II I I I I II III II II II II II III III II III II II III II II II — — — — — — — II III II II III
Cr = serum creatinine; BUN, blood urea nitrogen; Vmax = peak systolic velocity; RI = resistance index; CDE = color Doppler energy; GFR = glomerular filtration rate.
the compensatory enhancement of residual renal function. The reason might be that the tumor was rich in vascular tissue, leading to rich blood flow, and overload of renal capillary volume could induce increased vascular resistance. Interestingly, blood perfusion of the abnormal side was as good as that of the normal side, generally with a CDE of grade I or II. For unilateral renal cysts (n = 7), Vmax (58.20 § 7.38 cm/s) values were much lower on the abnormal side than on the normal side (87.71 § 14.83 cm/s), with low blood flow and normal vascular resistance. There was no difference between RIs (abnormal side: 0.63 § 0.03, normal side: 0.61 § 0.01). In addition, blood perfusion was poor compared with the normal side, with CDE generally grade II or III. The reason might be that the cyst lacked vascular tissue and there was local compression to normal tissue, suggesting a weakening of residual renal function. With reference to unilateral hydronephrosis (n = 10), the hemodynamic parameters (abnormal side:
Vmax = 58.61 § 11.91 cm/s, RI = 0.67 § 0.02; normal side: Vmax = 83.60 § 14.63 cm/s, RI = 0.66 § 0.05) were similar to those of renal cysts. Most patients had CDE grade II or III because of the local compression to normal tissue. As for unilateral renal agenesis (n = 7), both Vmax (106.07 § 13.07 cm/s) and RI (0.71 § 0.05) of the residual kidneys were higher, implicating the compensatory enhancement of renal function. Blood perfusion was good, with CDE grade I or II. In addition, the defective kidney had no color signal on display, indicating neither blood perfusion nor renal function. With respect to unilateral renal atrophy (n = 5), Vmax (49.78 § 19.74 cm/s) of the abnormal side was much lower compared with that of the normal side (Vmax = 103.02 § 28.65 cm/s). However, RI appeared not to differ between the normal (0.69 § 0.09) and abnormal (0.70 § 0.11) sides. In addition, blood perfusion of the abnormal side was poorer than that of the normal side, generally with CDE grade II or III. The reason
ARTICLE IN PRESS Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al.
might be congenital anomalies of renal structure resulting in a weakening of renal function. TAGEDH1DISCUSSIONTAGEDN Renal vascular color Doppler US combined with routine US is a non-invasive and non-radioactive method for evaluating kidney structure and hemodynamics. This method has been reported to be very useful in screening for various kinds of kidney diseases (Kim et al. 1992; Mostbeck et al. 1991; Ozbek 1992; Yang and Room 2017). However, few authors have used this method to study the function of a single kidney (Gudinchet et al. 1994). US has been reported to be a reliable method for evaluation of renal function, and different measurements have been proposed, such as hemodynamic parameters (Niesen et al. 2017; Yang and Room 2017). First, routine renal US can be used to observe the structure of the urinary tract, identifying whether the urinary tract has an obstruction or other structural abnormalities, which is similar to the excretory curve of radionuclide renography. Second, renal vascular color Doppler US allows determination of semi-quantitative parameters, such as RI, which provides details on vascular resistance, and this is inversely related to renal blood flow (He et al. 2017; Norris and Barnes 1984). Certain studies have indicated that higher RI is related to
5
thickening of the renal small vessel wall, glomerular sclerosis or degenerative change (He et al. 2017; Kasiske and Umen 1986), implicating aggravation of kidney damage and poor prognosis. Vmax directly reflects the degree of renal vascular filling and blood supply, which is negatively correlated with the degree of kidney damage. Lastly, renal vascular color Doppler US can be also beneficial in evaluating renal perfusion. For example, CDFI can display the direction of blood flow and the number, shape and size of blood vessels and blood flow distribution in different organs. However, CDFI results are easily affected by the angle of insonation, with poor sensitivity and continuity. In our study, CDE imaging proved to be a useful technology based on the total integral of the energy frequency spectrum. It detects blood flow using the energy of moving reflectors and has the advantages of high sensitivity to slow blood flow, while providing a less cluttered image and being less dependent on angles (Hamper et al. 1993; He et al. 2017). The results of our study indicated that there were obvious changes in hemodynamic tests and CDE grades between the left and right kidneys of patients with unilateral kidney diseases. Based on these differences, we can preliminarily assess split renal function. Compared with radionuclide renography, renal vascular color Doppler US lacks the ability to evaluate renal tubule function. However, radionuclide renography
Table 2. Comparison of common methods used for evaluation of split renal function RVCDUS + RUS
Radionuclide renography
Universality of method
New proposed method
Old and traditional method Yes Yes Reserve, decay and waste disposal of radionuclide No Yes
Radioactivity Radionuclide
No No
Contrast agent Side effects for kidney and/ or other organs Convenience
No No Yes
No Radionuclide injection needed Observation time limited
Cost Requirement for devices Characteristics of renal lesion, such as tumor, cyst Range of application GFR of single kidney
Cheap Moderate Clear
Cheap Specific device Unclear
Wide No Hemodynamic indexes (Vmax, RI, PI), CDE grades; further need to make split GFR
Wide No Three curves (vascular, secretary, excretory)
Renal dynamic imaging
Enhanced CT
Recognized method
Poor universality
Yes Yes Reserve, decay and waste disposal of radionuclide No Yes
Yes No
Yes Yes
No Radionuclide injection needed Observation time limited Time consuming Expensive High Unclear
Expensive High Clear
Wide Yes
Narrow Yes
No Contrast agent injection needed Complicated calculation method for GFR
RVCDUS = renal vascular color Doppler ultrasonography; RUS = routine ultrasonography; CT = computed tomography; GFR = glomerular filtration rate; Vmax = peak systolic velocity; RI = resistance index; PI = pulsatility index; CDE = Color Doppler energy image.
ARTICLE IN PRESS 6
Ultrasound in Medicine & Biology
cannot reflect renal damage in the early day (Biassoni and Easty 2017). Currently, the most common method used to evaluate split renal function is renal dynamic imaging, and other imaging techniques have been used to assess renal function, such as enhanced CT (Alexander et al. 2010; Prassopoulos et al. 1992, 1993). Comparison of these methods used for the evaluation of split renal function is documented in Table 2. Renal vascular color Doppler US is more likely to analyze the development of kidney disease in a timely and objective way via monitoring for renal hemodynamic changes, providing quantitative indicators for the disease in clinical practice. When dysfunction occurs in a single kidney, traditional laboratory indexes are likely to be in the normal range, while Vmax, RI and CDE have changed, easily reflecting the degree of renal damage. In the compensatory period of renal function, because the damage to renal units and the small artery is slight, the injured kidney is rich in blood flow, and the complete renal vascular tree can be clearly displayed. In the azotemia period, the endogenous creatinine clearance rate of patients with decompensation of renal function decreases, and serum Cr and BUN increase markedly, aggravating the damage to the renal arteriole, which leads to discontinuation of blood flow signals. At this time, the main renal arteries and segmental arteries can be displayed on a scan, but the signals of the interlobular arteries and arcuate artery are distributed in a stellate fashion. In uremia, the blood perfusion of patients is reduced significantly, accompanied by aggravation of renal damage. The signals of the interlobular arteries and arcuate arteries disappear, and the blood flow signal of the segmental artery is discontinuous. This study had some limitations. The most noteworthy is that the sample size was small in each group. An increase in cases would make the results of the study more persuasive.
TAGEDH1CONCLUSIONSTAGEDN As a non-invasive and non-radioactive examination method, renal vascular color Doppler US combined with routine US is an appropriate method for evaluation of single-kidney function and may be useful in detecting early damage caused by kidney disease. This method is likely superior to radionuclide renography and may even replace it in the evaluation of split renal function in children. However, larger studies should be performed to increase our knowledge about these patients.
Acknowledgments—H.Z. has received a grant from the foundation of the Medical Association of Sichuan Province (Grant S16052).
Volume 00, Number 00, 2018
TAGEDH1REFERENCESTAGEDN Agarwal SK, Dash SC, Irshad M, Raju S, Singh P, Pandey RM. Prevalence of chronic renal failure in adults in Delhi, India. Nephrol Dial Transplant 2005;20:1638–1642. Alexander K, Dunn M, Carmel EN, Lavoie JP, Del Castillo JR. Clinical application of Patlak plot CT-GFR in animals with upper urinary tract disease. Vet Radiol Ultrasound 2010;51:421–427. Biassoni L, Easty M. Paediatric nuclear medicine imaging. Br Medical Bulletin 2017;123:127. Chen Q, He F, Feng X, Luo Z, Zhang J, Zhang L, Wang Y, Tong J. Correlation of Doppler parameters with renal pathology: A study of 992 patients. Exp Ther Med 2014;7:439–442. Crutchley TA, Pearce JD, Craven TE, Stafford JM, Edwards MS, Hansen KJ. Clinical utility of the resistive index in atherosclerotic renovascular disease. J Vasc Surg 2009;49:148–155. Ellis RJ, Joshi A, Ng KL, Francis RS, Gobe GC, Wood ST. Optimising assessment of kidney function when managing localised renal masses. Med J Aust 2017;207:127. Fommei E, Volterrani D. Renal nuclear medicine. Semin Nucl Med 1995;25:183–194. Gudinchet F, Meuli R, Regazzoni B. Compensatory renal growth in children and adults studied by Doppler sonography. J Clin Ultrasound 1994;22:11–15. Hamper UM, Sheth S, Abbas FM, Rosenshein NB, Aronson D, Kurman RJ. Transvaginal color Doppler sonography of adnexal mases: Differences in blood flow independence in benign and malignant lesions. AJR Am J Roentgenol 1993;160:225. He X, Guan B, Zhu L. Hemodynamics as measured with color doppler sonography in early-stage obesity-related nephropathy in children. J Ultrasound Med 2017;36:1671–1677. Joseph A, Vassalotti LesleyA, Stevens AndrewS, Levey. Testing for chronic kidney disease: A Position Statement from the National Kidney Foundation. Am J Kidney Dis 2007;50:169–180. Kasiske BL, Umen AJ. The influence of age, sex, race, and body habitus on kidney weight in humans. Arch Pathol Lab Med 1986;110:55–60. Kim SH, Kim H, Choi BI, Kim CW. Duplex Doppler US in patients with medical renal disease: resistive index vs serum creatinine level. Clin Radiol 1992;45:85–87. Koff SA, Thrall JH, Keyes JW. Assessment of hydroureteronephrosis in children using diuretic radionuclide urography. J Urol 1980;123:531–534. Mostbeck GH, Kain R, Mallek R, Derfler K, Walter R, Havelec L, Tscholakoff D. Duplex Doppler sonography in renal parenchymal disease. J Ultrasound Med 1991;10:189–194. Norris CS, Barnes RW. Renal artery flow velocity analysis: A sensitive measure of experimental and clinical renovascular resistance. J Surg Res 1984;36:230–236. Niemczyk P, Krisch EB, Zeiger L, Marmar JL. Use of diuretic renogram in evaluation of patients before and after endopyelotomy. Urology 1999;53:271–275. Nosadini R, Velussi M, Brocco E, Abaterusso C, Carraro A, Piarulli F, Morgia G, Satta A, Faedda R, Abhyankar A, Luthman H, Tonolo G. Increased renal arterial resistance predicts the course of renal function in type 2 diabetes with microalbuminuria. Diabetes 2006;55: 234–239. Niesen TJ, Finch N, Gakhal M, Dressler RM, Levy HM. Value of prior imaging review before ordering renal sonography in the evaluation of abnormal renal function. J Clin Ultrasound 2017;45:537–541. O’Reilly PH. for the Consensus Committee of the Society of Radionuclides in Nephrourology. Standardisation of the renogram technique for investigating the dilated upper urinary tract and assessing the results of surgery. BJU Int 2003;91:239–243. Ozbek SS. Duplex Doppler US in medical renal disease. Clin Radiol 1992;46:219–220. Perez Calvo JI, Josa LC, Gimenez LI. Renal function assessment in heart failure. Rev Clin Esp 2017;217:267. Platt JF, Rubin JM, Ellis JH. Diabetic nephropathy: Evaluation with renal duplex Doppler. Radiology 1999;190:343–346.
ARTICLE IN PRESS Evaluation of Split Renal Function for Children with Kidney Diseases by Renal H. ZHANG et al. Prassopoulos P, Gourtsoyiannis N, Cavouras D, Pantelidis N. CT evaluation of compensatory renal growth in relation to postnephrectomy time. Acta Radiol 1992;33:566–568. Prassopoulos P, Cavouras D, Gourtsoyiannis N. Pre- and post-nephrectomy kidney enlargement in patients with contralateral renal cancer. Eur Urol 1993;24:58–61.
7
Splendiani G, Parolini C, Fortunato L, Sturniolo A, Costanzi S. Resistive index in chronic nephropathies: Predictive value of renal outcome. Clin Nephrol 2002;57:45–50. Yang X, Room BU. Clinical effect of color Doppler ultrasound on patients with chronic renal failure. China Continuing Med Educ 2017;9:75–76.