Volume 20 Number 5; September 2009 Editorials • Systemic Lupus Erythematosus Conundrums………………….……....……....731 E.N. Wardle
• Cancer Screening in End-Stage Renal Disease………………….……......….....737 S. Nayak-Rao
Review Articles • The Protective Effect of Thymoquinone, an Anti-oxidant and Anti-inflammatory Agent, against Renal Injury: A Review……….........741 A. Ragheb, A. Attia, W. Shehab Eldin, et al
• Prevention of Iodinated Contrast Induced Acute Kidney Injury (ICI-AKI) – What Have We Learnt So Far?……………….....….........753 M. Asim
Original Articles • Relation of Magnesium Level to Cyclosporine and Metabolic Complications in Renal Transplant Recipients……………….….........766 F. Ahmadi, R. Naseri, M. Lessan-Pezeshki
• Modifying Cyclosporine Associated Renal Allograft Dysfunction………………………..770 N. Mohapatra, A.V. Vanikar, R.D. Patel, H.L. Trivedi
• Kaposi’s Sarcoma after Renal Transplantation................................…………775 S. Abbaszadeh, S. Taheri
• Efficacy of Folate and Vitamin B12 in Lowering Homocysteine Concentrations in Hemodialysis Patients......................................779 N. Azadibakhsh, R.S. Hosseini, S. Atabak, et al
• C- Reactive Protein, Cardiac Troponin T and Low Albumin are Predictors of Mortality in Hemodialysis Patients.................................789 N. Bagheri, O. Taziki, K. Falaknazi
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• Application of Intravenous Electrocardiography for Insertion of Central Veins Dialysis Catheters....……..………………………….....794 A.A. Beigi, F. Parvizian, H. Masoudpour
• IgG Glomerulonephritis: A Morphologic Study of a Rare Entity…………………….…......…798 Sawsan M. Jalalah
• Outcome of Pregnancy in Pateints with Inactive Systemic Lupus Erythematosus and Minimal Proteinuria........................................802 S. Alshohaib
• Analysis of Causes of Mortality in Patients with Autosomal Dominant Polycystic Kidney Disease: A Single Center Study......................806 E. Rahman, F.A. Niaz, A. Al-Suwaida, et al
• C-Reactive Protein, a Valuable Predictive Marker in Chronic Kidney Disease……........811 G. Abraham, V. Sundaram, V. Sundaram, et al
• Renal Duplex Doppler Ultrasonography in Patients with Recurrent Urinary Tract Infection............................................................816 N.A. Soliman, A. Saif, A. Abdel Hamid, H. Moustafa
Case Reports • Spontaneous Rupture of Tuberculous Spleen in a HIV Seropositive Patient on Maintenance Hemodialysis…………….............….........…...822 S. Rathore, P. George, M. Deodhar, et al
• Mediastinal Parathyroid Adenoma................826 F. Al-Mashat, A. Sibiany, D. Faleh, et al
• Severe Acute Renal Failure in a Patient with Diabetic Ketoacidosis….…...............…….......831 J. Al-Matrafi, J. Vethamuthu, J. Feber
• Adult Wilms’ Tumor............…………..….....835 M.S. Sharma, M.Z. Ahmed
Contents continued in next page ISSN: 1319-2442
• Emphysematous Pyelonephritis – Case Report and Evaluation of Radiological Feature…....838 R. Mongha, B. Punit, D.K. Ranjit, K.K. Anup
• Granulomatous Interstitial Nephritis due to Tuberculosis-a Rare Presentation…...……...842 K. Sampathkumar, Y.S. Sooraj, A.R. Mahaldar, et al
Letters to the Editor • The Impact of Diagnostic Delay on the Course of Septic Shock Caused by ExtendedSpectrum-Beta-Lactamase-Producing Escherichia Coli…………………………....…846 M. Gashi, L. Raka, S. Ahmeti, et al
• Primary Cutaneous Aspergillosis in Renal Transplant Recipient………………………...848 A. Gupta, A. Khaira, S. Lata, et al
• Acute Urate Nephropathy Precipitated by Acute Diarrhea…….……………………....…850 W.L. Jabur
• Achieving the Aims of the SSN……………...852 A. Karkar
Renal Data from the Arab World • Pattern of Steroid Resistant Nephrotic Syndrome in Children Living in the Kingdom of Saudi Arabia: A Single Center Study…....854 J.A. Kari, M. Halawani, G. Mokhtar, et al
• Pathology of Nondiabetic Glomerular Disease among Adult Iraqi Patients from a Single Center………………………………...858 A.J. Al-Saedi • Prevalence of Cigarette Smoking and Khat Chewing among Aden University Medical Students and their Relationship to BP and Body Mass Index……………………………..862 A.N. Laswar, H. Darwish
Renal Data from Asia-Africa • Post-Transplant Urological and Vascular Complications……………………………….867 J. Safa, N. Nezami, M.K. Tarzamni, et al
• Assessment of Frequency of Complications of Arterio Venous Fistula in Patients on Dialysis: A Two-Year Single Center Study from Iran…………..……………….…....…...872 A. Derakhshanfar, M. Gholyaf, A. Niayesh, S. Bahiraii
SCOT Forum • Treatment of a Common Problem in Hemodialysis Patients: Is the Juice Worth the Squeeze? …………..……………….….....876 K. Al-saran, A. Sabry, N. Shaheen, A.Yehia
Doctor’s Diary • British Doctor Lectures in Damascus. “Human Affiliation or Belonging”……….....883 S. Pharaon
SCOT Data • Organ Donation and Transplantation in the Kingdom of Saudi Arabia 2008……………….885
Proceedings • 4th Annual International Conference of Saudi Society of Nephrology…………………...…...890 Forthcoming Conferences.…………..…...…940 Arabic Section…………...…..………..............968
Saudi J Kidney Dis Transpl 2009;20(5):816-821 © 2009 Saudi Center for Organ Transplantation
Saudi Journal of Kidney Diseases and Transplantation
Original Article Renal Duplex Doppler Ultrasonography in Patients with Recurrent Urinary Tract Infection Neveen A. Soliman1, Aasem Saif2, Alaa Abdel Hamid3, Hosna Moustafa4 1
Department of Pediatrics, Center of Pediatric Nephrology and Transplantation, 2Department of Internal Medicine and Endocrinology, 3Vascular Laboratory, 4Department of Nuclear Medicine, Cairo University, Egypt ABSTRACT. Renal hemodynamics were studied using duplex Doppler ultrasonography in forty (33 females and 7 males; mean age: 12.1 ± 5.3 years) normotensive patients with recurrent urinary tract infection and with no evidence of obstructive uropathy and age matched control group of 24 healthy children and adolescents. Resistivity index (RI) and pulsatility index (PI) in both arcuate (AA) and interlobar (IA) arteries were significantly higher in patients as compared to controls (P= 0.001, 0.01 respectively). Diastolic/systolic ratio (D/S) at the same levels of renal vasculature (AA and IA) was significantly lower in study patients as compared to their controls (P= 0.01, 0.001 respectively). Moreover, scarred renal units had higher RI and PI values as well as lower D/S ratio as compared to non scarred units (p= 0.01, 0.001, 0.001 respectively).). In conclusion, intra renal vascular resistivity is significantly increased in recurrent UTI patients particularly in those sustaining renal scarring. Further follow up studies are recommended to determine if duplex assessment of intrarenal vasculature could be useful as an ancillary diagnostic and/or prognostic technique in the evaluation and follow up of recurrent UTI. Introduction Urinary tract infections (UTIs) in children and adolescents can be classified based on the natural history and subsequent evaluation and maCorrespondence to: Dr. Neveen A. Soliman Professor of Pediatrics Center of Pediatric Nephrology and Transplantation Egyptian Group for Orphan Renal Diseases Cairo University, Cairo, 11451, Egypt E-mail:
[email protected]
nagement as first infection or recurrent infection. Recurrent infections can be subcategorized as unresolved bacteriuria, bacterial persistence, and reinfection.1 Clinical classification of UTI, such as complicated versus uncomplicated, upper versus lower, or cystitis versus pyelonephritis, imply severity of infection when, in fact, this cannot be documented clinically nor may “lesser” infections require less rigorous evaluation.2 Duplex ultrasonography is a non-invasive tool that has been increasingly used in clinical nephrology. Intrarenal blood flow can be observed by color-coded duplex and flow velocity can be measured by real time pulsed Doppler ultrasound.3
Renal ultrasonography in patients with UTI
This prospective study was carried out to detect changes in renal blood flow velocity and vascular indices by duplex ultrasonography and to correlate these changes with clinical parameters as well as with renal imaging results in children and adolescents with recurrent UTI. Methodology This study was approved by the Institutional Review Board at Cairo University Children’s Hospital. Forty patients (33 females and 7 males; age range 5-18 years, with a mean of 12.1 ± 5.3 years) suffering from recurrent UTI as well as 24 age and sex matched healthy children and adolescents (18 females and 6 males, age range 4-17 years, with a mean of 11.7 ± 4.8 years) were examined by color-coded renal duplex ultrasound scan. Informed consent was obtained from the parents. Patients’ case notes were reviewed particularly for: 1) the duration of ill-ness from the first documented UTI, 2) presence or absence of vesico-ureteric reflux (VUR) and 3) the latest calculated glomerular filtration rate (c-GFR) as calculated by Schwartz formula.4 All patients were normotensive at the time of the study; none of them had persistent hypertension (HTN) or obstructive uropathy. They all had c-GFR > 80 mL/min/1.73 m² and had been infection free for at lest 6 months prior to the study. Imaging modalities employed in this work included: 1) Pre-study real time renal ultrasound scan to assess renal size, Patients with small kidneys for age and those with structural urinary tract anomalies were excluded from the study. 2) Static renal scintigraphy (DMSA) scan was performed for all patients for the detection of renal scarring.5 3) Color coded duplex ultrasound scan using 3.5 or 5 MHz transducer (HP Sonos 1500 machine, Hewlett Packard, Santa Clara, CA, USA). Patients were scanned in the supine
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position. The transducer was placed in the midline with slight inclination to the left to get a coronal section of the aorta. Each renal artery was identified as lying between the superior mesentric artery and the corresponding renal vein. Flow velocities were measured by real time pulsed Doppler ultrasonography. The ulltrasonographer was blinded to the results of DMSA scan in the study patients. Recordings were obtained from the main renal artery as well as its main intrarenal branches (segmental, interlobar, and arcuate). For each artery, the resistivity index (RI), the pulsatility index (PI), and distolic systolic ratio (D/S) were measured according to the following formulae:6 Peak systolic velocity – End diastolic velocity RI = Peak systolic velocity Peak systolic velocity − End diastolic velocity PI = Mean velocity End diastolic velocity D/S = Peak systolic velocity Mean renal RIs, PIs, and D/S ratios were used for statistical analysis of differences between patients and controls using student t-test (P value); P< 0.05 was considered significant. The correlation between the duplex indices in patients and the clinical or imaging parameters were studied using the Pearson’s correlation coefficient (r value); r > 0.38 was accepted as statistically significant. Results In the study patients, the recurrence rate of episodes of UTI varied from 3 to as much as 11 times during the entire period of illness which ranged from 2-5 years (Mean ± SD 3.3 ± 0.85 years). Ultrasonographic evaluation of our patients revealed no evidence of underlying obstructive
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Soliman NA, Saif A, Abdel Hamid A, Moustafa H
Figure 1A. Study patient No. 35, six years old girl with recurrent episodes of febrile UTI for almost two years. Indirect radionuclide cystography demonstrated bilateral VUR grade III. (a) DMSA scintigraphy posterior view showing bilateral multiple photopenic areas of renal scarring
congenital anomalies, only mild dilatation of the renal pelvis and/or ureters in 10/40 patients. Previous DTPA scanning of these patients showed no evidence of organic obstruction, moreover indirect radionuclide cystography VCUG confirmed the diagnosis of VUR in 8/40 patients (20%) graded II-III. VUR was bilateral in 1/8 and unilateral in 7/8 of the refluxer patients. One patient 1/40 had an isolated pelvic renal stone which was infective in nature that was surgically removed. DMSA scintigraphy of the study patients re-
vealed that 10/40 (25%) patients had evidence of renal scarring which was bilateral in only 2. Among the children with reflux, only 3/8 (37.5%) patients had renal scarring, Figure 1. Table 1 demonstrates that of all the vascular indices including RI, PI in both AA and IA arteries were significantly higher and D/S lower in patients as compared to controls. Furthermore, high recurrence rate of UTI showed significant positive correlation to RI, PI, and negative correlation to D/S at both AA and IA levels. Patients with renal scarring had significantly higher
Figure 1B. Color-coded duplex scan of the same patient demonstrated abnormal right renal artery waveform, peak systolic velocity with shouldering obliteration of the window and normal diastolic velocity
Renal ultrasonography in patients with UTI
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Table 1. Comparison of Duplex indices in patients and control groups Variable Patients Controls (Mean ± SD) (Mean ± SD) Main renal artery PI 1.0 ± 0.27 0.81 ± 0.29 RI 0.62 ± 0.08 0.54 ± 0.09 D/S 0.36 ± 0.07 0.39 ± 0.11 Segmental artery PI 0.91 ± 0.17 0.81 ± 0.14 RI 0.71 ± 0.09 0.54 ± 0.05 D/S 0.38 ± 0.11 0.41 ± 0.14 Arcuate artery PI 0.85 ± 0.20 0.51 ± 0.08 RI 0.73 ± 0.11 0.53 ± 0.06 D/S 0.41 ± 0.10 0.50 ± 0.07 Interlobar artery PI 0.83 ± 0.35 0.53 ± 0.15 RI 0.71 ± 0.08 0.43 ± 0.10 D/S 0.58 ± 0.15 0.48 ± 0.07
RI and PI values as well as lower D/S ratios (at the AA and IA levels) as compared to patients with no evidence of scarring. Nevertheless, no significant correlation was observed between any of the vascular indices and duration of infection and vesicoureteric reflux (VUR) Table 2. Discussion Urinary tract infection (UTI) is common and results in significant morbidity in children and adolescents. In the past few decades, a better understanding of the pathogenesis and the natural history of UTI in this age group has evolved. This, together with the identification of risk factors that predispose to subsequent renal parenchymal damage, have led to the prompt, appropriate, and thorough evaluation to minimize the acute morbidity and the long term sequelae of UTIs, such as: renal scarring, hypertension, and renal failure.7
P value
NS NS NS NS NS NS 0.01 0.001 0.01 0.01 0.001 0.001
The natural history of recurrent UTIs has been well documented by Winberg et al, moreover they demonstrated that the relative risk for recurrent infection depends on the number of prior infections.8 For example, one prior infection increased the risk for recurrence by 25%; this figure increased proportionately with the number of infections (50% and 75% with two and three infections, respectively). Intrarenal blood flow can be observed by color-coded duplex and the flow velocity can be measured by real time pulsed Doppler ultrasound in patients with diabetes mellitus, renal artery stenosis, chronic kidney disease and renal transplant recipients with some limitations.6,9-12 Radionuclide renal imaging studies are widely used to detect renal scarring, rule out obstructive uropathies, diagnosis and follow up of VUR as well as for the assessment of relative renal function.13,14 Nevertheless, these scans are costly, invasive, and incur a radiation load. A non-
Table 2. Correlation between vascular indices (at the Arcuate artery andInterlobar artery levels) of the study patients with clinical and imaging parameters Variable PI RI D/S ratio r value P value r value P value r value P value Duration of UTI 0.28 NS 0.30 NS -0.31 NS Recurrence rate 0.44 0.01 0.42 0.02 -0.43 0.01 VUR 0.29 NS 0.33 NS -0.35 NS Renal Scarring 0.52 0.001 0.46 0.01 -0.51 0.001
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invasive test is therefore more desirable. Of all the vascular indices studied in this workup, RI and PI in both AA and IA arteries were significantly higher in patients as compared to controls (P= 0.001, 0.01 respectively). Moreover, D/S at the same levels of renal vasculature (AA and IA) were significantly lower in study patients as compared to their controls (P= 0.01, 0.001 respectively). This demonstrates the higher focal intra-renal vascular resistivity in patients compared to controls. Nevertheless, RI and PI were higher and D/S ratio was lower in patients compared to controls at both the main renal and segmental arteries, yet the difference did not reach statistical significance. Platt and his co-workers demonstrated that active renal disease within the tubulointerstitial compartment (acute tubular necrosis, interstitial nephritis) or vasculitis/vasculopathy generally resulted in an elevated RI, whereas disease limited to the glomeruli, no matter how severe, did not significantly elevate the RI.15 Moreover, Izumi and his associates reported the diagnostic value of Doppler ultrasound in differentiating acute tubular necrosis from prerenal azotemia by comparing RI and PI results with the fractional excretion of sodium, renal failure index, and urinary/serum creatinine ratio.6 The correlation between the studied vascular indices and clinical parameters revealed that the high recurrence rate of UTI was significantly positively correlated to RI (P= 0.02) and PI (P= 0.01), and negatively to D/S ratio (P= 0.01) at both AA and IA levels. This was again shown in kidneys with scarring on radionuclide scans. Riccabona and co-workers demonstrated that amplitude coded-color Doppler sonography accurately depicted altered renal perfusion, when compared to scintigraphy or CT scan, in pediatric renal diseases including renal scars, UTI, reflux nephropathy among other renal diseases.16 In another study, RI values were increased significantly in children with febrile UTI when renal parenchymal involvement (assessed by DMSA scintigraphy) was present. Refluxing kidneys and scarred kidneys also had higher RI values.17 Many of the previous studies utilizing Doppler
Soliman NA, Saif A, Abdel Hamid A, Moustafa H
ultrasonography in the evaluation of UTI were mainly addressed to febrile UTI in an attempt to differentiate acute pyelonephritis from lower urinary tract infection.17-20 Only few workers, however, did study its potential use to depict altered renal perfusion in pediatric renal diseases other than acute UTI including reflux nephropathy and renal scarring.16 In conclusion, our study in patients without active UTI demonstrated significant intra-renal vascular changes that predicted the possibility of recurrence of UTI. Further studies are recommended to evaluate the role of duplex Doppler ultrasound in detecting altered renal hemodynamics and whether it helps in identifying those at high risk of recurrence and therfore permanent renal damage. Acknowledgement The authors thank the patients and their families for participating in this study. References 1.
2.
3.
4.
5.
6.
7.
Smellie JM, Prescod NP, Shaw PJ, et al. Childhood reflux and urinary infection: a follow up of 10-41 years in 226 adults. Pediatr Nephrol 1998;12(9):727-36. Stamey TA. Pathogenesis and treatment of urinary tract infections. Ed Baltimore, Williams & Wilkins 1980 pp 934-45. Scholbach I. Doppler studies in normal kidneys of healthy children. Pediatr Nephrol 1996;10(2): 156-9. Schwartz GJ, Haycock GB, Edelmann CM, Spitzer A. A simple method estimate of glomerular filtration rate in children derived from Body lengh and plasma creatinine. Pediatrics 1976;58: 259-63. Taylor CM, Chapman S. Imaging: Nuclear medicine. In Handbook of Renal Investigations in Children. Wright, Kent 1989;pp148-149. Izumi M, Sugiura T, Nakamura H, Nagatoya K, Imai E, Hori M. Differential diagnosis of prerenal azotemia from acute tubular necrosis and prediction of recovery by Doppler ultrasound. Am J Kidney Dis 2000;35(4):713-9. Chon CH. Pediatric urinary tract infections. Pediatr Clin Nephrol Am 2001;48(6):1441-59.
Renal ultrasonography in patients with UTI 8.
9.
10.
11.
12.
13.
14.
Winberg J, Andersen HJ, Bergstrom T, Jacobsson B, Larson H, Lincoln K. Epidemiology of symptomatic urinary tract infection in childhood. Acta Paediatr Scand 1974; 252 Suppl:1-20. Perrella R, Duerinckx A, Tessler F, et al. Evaluation of renal transplant dysfunction by duplex Doppler sonography: A prospective study and review of the literature. Am J Kidney Dis 1990; 15:544-50. Distler A, Spies K. Diagnostic procedure in renovascular hypertension. Clin Nephrol 1991; 36:174-80. Ishimura E, Nishizawa Y, Kawagishi T, et al. Intra-renal hemodynamic abnormalities in diabetic nephropathy measured by duplex Doppler sonography. Kidney Int 1997;51:1920-7. Mostbeck G, Kain R, Mallek R, et al. Duplex Doppler sonography in renal parenchymal disease. J Ultrasound Med 1991;10:189-94. Gordon I. Imaging the kidneys and the urinary tract. In: Holliday MA; Barratt TM; Avner (Eds) Pediatric Nephrology, 4th edn. Kogan BA, London, 2000.pp 421-37. Heyman S. Radionuclide studies of the genitourinary tract. In: Miller JH; Gelfand MJ (Eds). Pediatric Nuclear Imaging 1st edn. Saunders, Philadelphia, London, 1994.pp 195-251.
821 15. Platt JF, Ellis JH, Rubin JM, DiPietro MA, Sedman AB. Intrarenal arterial doppler sonography in patients with nonobstructive renal disease: Correlation of resistive index with biopsy findings. AJR Am J Roentgenol 1990; 154:1223-7. 16. Riccabona M, Ring E, Schwinger W, Aigner R. Amplitude coded color Doppler sonography in paediatric renal disease. Eur Radiol 2001;11(5): 861-6. 17. Ozcelik G, Polat TB, Aktas S, Cetinkaya F. Resistive index in febrile urinary tract infections: predictive value of renal outcome. Pediatr Nephrol 2004;19(2):148-52. 18. Berro Y, Baratte B, Seryer D, et al. Comparison between scintigraphy, B mode, and power Doppler sonography in acute pyelonephritis in children. J Radiol 2000;81(5):523-7. 19. Akdilli A, Karaman CZ, Basak O, Aydogdu A. The diagnostic value of intrarenal colour duplex Doppler ultrasonography in children with lower urinary tract infection. Pediatr Radiol 1999;29 (12):897-900. 20. Basiratnia M, Noohi AH, Lotfi M, Alavi MS. Power Doppler sonographic evaluation of acute childhood pyelonephritis. Pediatr Nephrol 2006; 21(12):1854-7.
