PEDIATRIC UROLOGY
VESICOURETERAL REFLUX IN CHILDREN WITH AND WITHOUT A HISTORY OF URINARY TRACT INFECTION: A COMPARATIVE ANALYSIS SAUL P GREENFIELD, M.D. EHSAN AFSHANI, M.D.
Departments of Urology and Radiology, Children’s Hospital of Buffalo, State University of New York at Buffalo Medical School, Buffalo, New York
ABSTRACT-Eighty-eight children who were discovered to have vesicoureteral reflux were prospectively studied over a two-year period. Two groups were compared: 49 who presented with a urinary tract infection and 39 who were identified through prospective screening. Based on the distribution of grade and the presence of parenchymal scarring, the severity of vesicoureteral reflux was comparable in the two groups. Of note, more males with reflux were identified in the noninfected group, whereas sex distribution was almost equal in the infected group. Ultrasound alone was found to be highly inaccurate in identifying reflux or parenchymal changes. In conclusion, screening of at-risk groups of children without a history of urinary tract infection may identify patients with clinically significant vesicoureteral reflux.
Vesicoureteral reflux (VUR) is most commonly identified in children who first present with a urinary tract infection (UTI). ls2 Recently, the evaluation of groups without a history of urinary tract infection has been proposed. These groups are mainly the siblings of children with reflux and children with voiding dysfunction.3*4 To a lesser extent, children with hypospadias, imperforate anus, or other congenital syndromes may occasionally be found to have VUR.5,e The purpose of this study was to compare the severity of the VUR in two populations who were newly diagnosed in the same time period at one institution: those with and without a history of UTI. Severity was determined by grade and the presence of parenchyma1 scarring. Material and Methods Eighty-eight children with newly diagnosed VUR who presented between 1984 and 1986 were included in this study. Excluded were children with spina bifida, posterior urethral
UROLOGY
I OCTOBER1992
/ VOLUME40,NUMBER4
valves, ureterocele, and ectopic ureter, since either the renal parenchymal changes or the reflux in these children are secondary to congenital dysplasia or obvious neurologic dysfunction. Forty-nine children with a history of UT1 and 39 with no history of UT1 who were identified through evaluating the following groups-siblings of refluxers, children with voiding dysfunction, hypospadias, imperforate anus, and other less common syndromes of congenital anomalies, and healthy newborns.’ All children underwent contrast-enhanced voiding cystourethrograms (VCUG), intravenous pyelograms (IVP), and technetium dimercaptosuccinic acid (DMSA) renal scans. Thirty-six children were also evaluated with renal ultrasound. Reflux was graded on the international scale (grades l-5). The DMSA renal scan was used to delineate renal scarring. All radiographs were re-reviewed by one radiologist (EA) for this study. Catheterized urine specimens were also sent for culture at the time of VCUG. A positive culture placed that individual in the
339
II.
Clinical characteristics of 39 patients (57 ureters) without a history of UTI and with reflux*
TABLE
Clinical characteristics of 49 patients (74 ureters) with a history of UTI and reflux*
TABLE I.
Grade I II III IV V TOTALS
No. of Ureters 12 28 23 7 4
No. of Renal Units with Scarring
(16) (38) (31) (9.5) (5.5)
74 (100)
4 4 5 2 15 (20)
No. of Pts. Undergoing Surgery 1 2 8 6 2 19 (39)
*Figures in parenthesesindicate percent.
UT1 group, even if no prior history of infection had been elicited. Forty-nine patients with a history of UT1 and 39 without a history of UT1 were entered into the study. The 39 patients in the sterile group were initially evaluated for the following reasons: (1) voiding dysfunction, 13 patients; (2) siblings with refluxing probands, 10 patients; (3) imperforate anus, 3 patients; (4) miscellaneous, 13 patients (failure to thrive, hypospadias, para auricular-vertebral syndrome, hemamultiple congenital anomalies, turia, unexpected hydronephrosis seen on an abnormal ultrasound). Results Seventy-four refluxing ureters were identified in the 49 UT1 patients. The distribution of grade among the ureters is shown in Table I. The majority of ureters (69%) had reflux of grades 2 and 3. Fifty-seven refluxing ureters were identified in the sterile group; the grade distribution is shown in Table II. Once again, the majority of ureters (60 % ) demonstrated reflux of grades 2 and 3. Renal scarring was found on the DMSA scan in 17.5 percent of the refluxing ureters in the sterile group and 20% of the refluxing ureters in the UT1 group. Fourteen children with 15 scarred kidneys were identified in the UT1 group, and 8 children with 10 scarred kidneys were identified in the sterile group* Age and sex distribution is shown in Table III. There were 22 (56%) males and 17 (44%) females in the sterile group. Age distribution in this group was from one day to eleven years, with an average age of 4.6 years. The 8 children with scarring and no history of urinary tract infection had an average age of 5.8 years (range: 3 months to 11 years). There were 6 (12 % )
340
No. of Ureters
Grade I II III IV V
13 (23) 17 (30) 17 (30)
TOTALS
57 (100)
No. of Renal Units with Scarring
No. of Pts. Undergoing Surgery
2 1 2 4 1
7 (12) 3 (5)
3 4 1
10 (17.5)
S (21)
‘Figures in parenthesesindicate percent.
Distribution of age and sex in both infected and non-infected groups *
TABLE III.
Age Average age (yrs.) Male Female Average age of children with scarring (yrs.)
Non-infected 4.26 22 (56) 17 (44)
(s”thildr
Infected 4.27 6 (12) 43 (88)
en)
(t46children)
‘Figures in parenthesesindicate percent.
males and 43(88%) females in the UT1 group with an average age of 4.27 years (range: 2 days to 11 years), The average age of the 14 children with scarring in this group was 4.6 years (range: newborn to 11 years). Nineteen of 49 patients (39 % ) from the UT1 group and 8 of the 39 (21%) of the sterile group ultimately underwent reimplantation surgery. The remainder are being followed on antibiotic prophylaxis. Of the 8 children (10 ureters) who had renal scarring, but no history of infection, 7 were male. Two of these children were siblings of refluxers, 4 had a history of voiding dysfunction, 1 was screened because he had multiple congenital anomalies, and 1 was evaluated as a newborn as part of a broad nonselective ultrasound screening program. Of all 88 children, 36 were subject to renal ultrasound as part of their initial evaluation-16 with a history of UT1 and 20 without a history of UTI. Only 10 (28 % ), or 5 in each group, had sonograms which suggested any renal pathology, either hydronephrosis or a scarred kidney. Comment Of those children with a history of UT1 30 to 50 percent will have vesicoureteral reflux.l.2 Sibling studies have shown that up to 46
UROLOGY
/ OCTOBER 1992 /
VOLUME 40, NUMBER 4
percent of asymptomatic siblings of refluxers will also have reflux.3 To a lesser extent, children with voiding dysfunction, hypospadias, imperforate anus, and other syndromes of multiple congenital anomalies may also have vesicoureteral reflux.5y0 Up to 15 percent of children with voiding dysfunction and no history of UT1 will have vesicoureteral reflux, and up to 16 percent of these children will have demonstrable scarring on a renal scan at the time of diagnosis.4 Broad nonselective screening studies of asymptomatic populations using ultrasound alone have shown that hydronephrosis is found in 1-2 percent of children.’ One newborn male in our non-UT1 group with extensive renal scarring was identified in this manner. Over a two-year period, in a single institution, almost as many children (39) with reflux and no history of UT1 were identified as those who were newly diagnosed with a history of UT1 (49). The data from this study also indicate that the distribution of grade and incidence of scarring are comparable in these two groups. The majority of both groups had ureters with grade II or III reflux. Based on the DMSA renal scan, an almost identical percentage have parenchymal scarring at the time of presentation, approximately 20 percent. The main difference between these two groups in our study population was in sex distribution. There were more males than females in the sterile group. A male with reflux is less likely, therefore, to present with a symptomatic urinary tract infection first. In addition, of the 8 children with scarring in this group, 7 were male. The exact mechanism of renal injury in children with vesicoureteral reflux remains a controversial subject. Undoubtedly, urinary tract infection plays a major role as has been shown in both the experimental model and clinically.8,9 Antibiotic prophylaxis with the prevention of infection is the cornerstone of management in these children.lOJ1 These data suggest, however, that urinary tract infections are not the only way that children with significant disease present. It is possible that some of these non-UT1 children had asymptomatic urinary tract infections prior to discovery. The incidence of this phenomenon, however, remains purely speculative. Furthermore, retrospective studies of renal transplant populations reveal that many adolescents and young adults who have scarred kidneys and renal failure secondary to vesicoureteral reflux have no history of urinary tract infection. 12,13
UROLOGY
I OCTOBER
1992
/
VOLUME 40, NUMBER 4
Once children without a history of infection were identified, they were managed in a standard fashion. All patients were placed on antibiotic prophylaxis and a strict surveillance regimen. In general, patients only underwent immediate surgery for high grade reflux (grade 4 or 5) or failure to comply with a prophylaxis schedule, or breakthrough infection. The greatest deterent to screening is the relative invasiveness of the VCUG, which requires catheterization in an awake child and radiation exposure. One can decrease exposure with a radionuclide VCUG,14 but unfortunately, there is no satisfactory noninvasive means of detecting vesicoureteral reflux. The renal ultrasound failed to detect VUR in over 70 percent of those in whom it was employed as a screen in our population. It is unreasonable, therefore, to rely solely on this modality when evaluating children in whom reflux is a possibility. The highest grades of reflux may present with hydronephrosis seen on a renal ultrasound and some of our patients were identified in this manner, 15x18Ultrasound screening will, therefore, identify some patients with unsuspected high-grade reflux, but will miss others with lower grades. This study does not answer the question: Who among those without a history of infection should or should not be screened for reflux? Only long-term prospective follow-up of these children will provide the answer. On the other hand, by evaluating certain populations without a history of infection, a group of children with VUR will be identified with reflux, the severity of which at initial diagnosis equals that found in an infected population. At a single institution, almost an equivalent number of children with reflux were discovered among these uninfected populations. Finally it appears that more males will be identified if non-infected groups are screened. Children’s Hospital of Buffalo 219 Bryant Street Buffalo, New York 14222 (DR. GREENFIELD) References 1. Smellie J, and Normand C: Reflux nephropathy in childhood. in Ho&n RC (Ed\: Reflux Nenhrooathv. New York., 1979. Kin&d-Smith, pp 14-26. 2. Baker R, and Barbaris HT: Comparative results of urological evaluation of children with initial and recurrent urinary tract infections, J Urol 116: 500 (1976). 3. Van den Abbeele AD, Treves ST, and Lebowtiz RL: Vesicoureteral reflux in asymptomatic siblings of patients with known I
&
,,
341
reflux: radionuclide cystography, Pediatrics 79: 147 (1987). 4. Sujka S, Piedmonte M, and Greenfield S: Enuresis and the voiding cysto-urethrogram: a reevaluation. Presented at Urologic Section, American Academy of Pediatrics, New Orleans, Louisiana, November, 1987. 5. Shafir R, et al: Vesicoureteral reflux in boys with hypospadias, Urology 20: 29 (1982). 6. Parrott TS, and Woodard JR: Importance of cysto-urethrography in neonates with imperforate anus, Urology 13: 607 (1979). 7. Steinhart JM, Kuhn JR and Eisenberg MD: Ultrasound screening of healthy infants for urinary tract abnormalities, Pediatrics 82: 609 (1988). 8. Risdon RA: Reflux nephropathy, Diagn Histopathol 4: 61 (1981). 9. Winberg J, Bollgren I, and Kallenius G: Clinical pyelonephritis and focal renal scarring, Pediat Clin North Am 29: 801 (1982). 10. Smellie JM, Edwards D, and Normand ICS: Effects of ves-
342
icoureteric reflux on renal growth in children with urinary tract infection, Arch Dis Child 56: 593 (1981). 11. Skoog SJ, Belman AB, and Majd M: Non-surgical approach to management of primary vesico-ureteral reflux, J Urol 138: 941 (1987). 12. Bailey RR: End-stage reflux nephropathy, Nephron 27: 302 (1981). 13.. Bakshandeh K, Lynne C, and Carrion H: Vesicoureteral reflux and end staee renal disease. 1 Urol 116: 557 (1976). 14. Conway JJ,king LR, and BArnan AB: Detection of vesicoureteral reflux with radionucleotide cystography, Am J Roentgen01 115: 720 (1972). 15. Schneider K, et al: Screening for vesicoureteral reflux in children using real-time sonography, Pediatr Radio1 14: 400 (1984). 16. Kangarloo H, Gold RH, and Fine RN: Urinary tract infection in infants and children evaluated by ultrasound, Radiology 154: 367 (1985).
UROLOGY
I
OCTOBER 1992
I
VOLUME 40, NUMBER 4
VESICOURETERAL REFLUX IN CHILDREN WITH AND WITHOUT A HISTORY OF URINARY TRACT INFECTION: A COMPARATIVE ANALYSIS SAUL P GREENFIELD, M.D. EHSAN AFSHANI, M.D.
Departments of Urology and Radiology, Children’s Hospital of Buffalo, State University of New York at Buffalo Medical School, Buffalo, New York
ABSTRACT-Eighty-eight children who were discovered to have vesicoureteral reflux were prospectively studied over a two-year period. Two groups were compared: 49 who presented with a urinary tract infection and 39 who were identified through prospective screening. Based on the distribution of grade and the presence of parenchymal scarring, the severity of vesicoureteral reflux was comparable in the two groups. Of note, more males with reflux were identified in the noninfected group, whereas sex distribution was almost equal in the infected group. Ultrasound alone was found to be highly inaccurate in identifying reflux or parenchymal changes. In conclusion, screening of at-risk groups of children without a history of urinary tract infection may identify patients with clinically significant vesicoureteral reflux.
Vesicoureteral reflux (VUR) is most commonly identified in children who first present with a urinary tract infection (UTI). ls2 Recently, the evaluation of groups without a history of urinary tract infection has been proposed. These groups are mainly the siblings of children with reflux and children with voiding dysfunction.3*4 To a lesser extent, children with hypospadias, imperforate anus, or other congenital syndromes may occasionally be found to have VUR.5,e The purpose of this study was to compare the severity of the VUR in two populations who were newly diagnosed in the same time period at one institution: those with and without a history of UTI. Severity was determined by grade and the presence of parenchyma1 scarring. Material and Methods Eighty-eight children with newly diagnosed VUR who presented between 1984 and 1986 were included in this study. Excluded were children with spina bifida, posterior urethral
UROLOGY
I OCTOBER1992
/ VOLUME40,NUMBER4
valves, ureterocele, and ectopic ureter, since either the renal parenchymal changes or the reflux in these children are secondary to congenital dysplasia or obvious neurologic dysfunction. Forty-nine children with a history of UT1 and 39 with no history of UT1 who were identified through evaluating the following groups-siblings of refluxers, children with voiding dysfunction, hypospadias, imperforate anus, and other less common syndromes of congenital anomalies, and healthy newborns.’ All children underwent contrast-enhanced voiding cystourethrograms (VCUG), intravenous pyelograms (IVP), and technetium dimercaptosuccinic acid (DMSA) renal scans. Thirty-six children were also evaluated with renal ultrasound. Reflux was graded on the international scale (grades l-5). The DMSA renal scan was used to delineate renal scarring. All radiographs were re-reviewed by one radiologist (EA) for this study. Catheterized urine specimens were also sent for culture at the time of VCUG. A positive culture placed that individual in the
339
II.
Clinical characteristics of 39 patients (57 ureters) without a history of UTI and with reflux*
TABLE
Clinical characteristics of 49 patients (74 ureters) with a history of UTI and reflux*
TABLE I.
Grade I II III IV V TOTALS
No. of Ureters 12 28 23 7 4
No. of Renal Units with Scarring
(16) (38) (31) (9.5) (5.5)
74 (100)
4 4 5 2 15 (20)
No. of Pts. Undergoing Surgery 1 2 8 6 2 19 (39)
*Figures in parenthesesindicate percent.
UT1 group, even if no prior history of infection had been elicited. Forty-nine patients with a history of UT1 and 39 without a history of UT1 were entered into the study. The 39 patients in the sterile group were initially evaluated for the following reasons: (1) voiding dysfunction, 13 patients; (2) siblings with refluxing probands, 10 patients; (3) imperforate anus, 3 patients; (4) miscellaneous, 13 patients (failure to thrive, hypospadias, para auricular-vertebral syndrome, hemamultiple congenital anomalies, turia, unexpected hydronephrosis seen on an abnormal ultrasound). Results Seventy-four refluxing ureters were identified in the 49 UT1 patients. The distribution of grade among the ureters is shown in Table I. The majority of ureters (69%) had reflux of grades 2 and 3. Fifty-seven refluxing ureters were identified in the sterile group; the grade distribution is shown in Table II. Once again, the majority of ureters (60 % ) demonstrated reflux of grades 2 and 3. Renal scarring was found on the DMSA scan in 17.5 percent of the refluxing ureters in the sterile group and 20% of the refluxing ureters in the UT1 group. Fourteen children with 15 scarred kidneys were identified in the UT1 group, and 8 children with 10 scarred kidneys were identified in the sterile group* Age and sex distribution is shown in Table III. There were 22 (56%) males and 17 (44%) females in the sterile group. Age distribution in this group was from one day to eleven years, with an average age of 4.6 years. The 8 children with scarring and no history of urinary tract infection had an average age of 5.8 years (range: 3 months to 11 years). There were 6 (12 % )
340
No. of Ureters
Grade I II III IV V
13 (23) 17 (30) 17 (30)
TOTALS
57 (100)
No. of Renal Units with Scarring
No. of Pts. Undergoing Surgery
2 1 2 4 1
7 (12) 3 (5)
3 4 1
10 (17.5)
S (21)
‘Figures in parenthesesindicate percent.
Distribution of age and sex in both infected and non-infected groups *
TABLE III.
Age Average age (yrs.) Male Female Average age of children with scarring (yrs.)
Non-infected 4.26 22 (56) 17 (44)
(s”thildr
Infected 4.27 6 (12) 43 (88)
en)
(t46children)
‘Figures in parenthesesindicate percent.
males and 43(88%) females in the UT1 group with an average age of 4.27 years (range: 2 days to 11 years), The average age of the 14 children with scarring in this group was 4.6 years (range: newborn to 11 years). Nineteen of 49 patients (39 % ) from the UT1 group and 8 of the 39 (21%) of the sterile group ultimately underwent reimplantation surgery. The remainder are being followed on antibiotic prophylaxis. Of the 8 children (10 ureters) who had renal scarring, but no history of infection, 7 were male. Two of these children were siblings of refluxers, 4 had a history of voiding dysfunction, 1 was screened because he had multiple congenital anomalies, and 1 was evaluated as a newborn as part of a broad nonselective ultrasound screening program. Of all 88 children, 36 were subject to renal ultrasound as part of their initial evaluation-16 with a history of UT1 and 20 without a history of UTI. Only 10 (28 % ), or 5 in each group, had sonograms which suggested any renal pathology, either hydronephrosis or a scarred kidney. Comment Of those children with a history of UT1 30 to 50 percent will have vesicoureteral reflux.l.2 Sibling studies have shown that up to 46
UROLOGY
/ OCTOBER 1992 /
VOLUME 40, NUMBER 4
percent of asymptomatic siblings of refluxers will also have reflux.3 To a lesser extent, children with voiding dysfunction, hypospadias, imperforate anus, and other syndromes of multiple congenital anomalies may also have vesicoureteral reflux.5y0 Up to 15 percent of children with voiding dysfunction and no history of UT1 will have vesicoureteral reflux, and up to 16 percent of these children will have demonstrable scarring on a renal scan at the time of diagnosis.4 Broad nonselective screening studies of asymptomatic populations using ultrasound alone have shown that hydronephrosis is found in 1-2 percent of children.’ One newborn male in our non-UT1 group with extensive renal scarring was identified in this manner. Over a two-year period, in a single institution, almost as many children (39) with reflux and no history of UT1 were identified as those who were newly diagnosed with a history of UT1 (49). The data from this study also indicate that the distribution of grade and incidence of scarring are comparable in these two groups. The majority of both groups had ureters with grade II or III reflux. Based on the DMSA renal scan, an almost identical percentage have parenchymal scarring at the time of presentation, approximately 20 percent. The main difference between these two groups in our study population was in sex distribution. There were more males than females in the sterile group. A male with reflux is less likely, therefore, to present with a symptomatic urinary tract infection first. In addition, of the 8 children with scarring in this group, 7 were male. The exact mechanism of renal injury in children with vesicoureteral reflux remains a controversial subject. Undoubtedly, urinary tract infection plays a major role as has been shown in both the experimental model and clinically.8,9 Antibiotic prophylaxis with the prevention of infection is the cornerstone of management in these children.lOJ1 These data suggest, however, that urinary tract infections are not the only way that children with significant disease present. It is possible that some of these non-UT1 children had asymptomatic urinary tract infections prior to discovery. The incidence of this phenomenon, however, remains purely speculative. Furthermore, retrospective studies of renal transplant populations reveal that many adolescents and young adults who have scarred kidneys and renal failure secondary to vesicoureteral reflux have no history of urinary tract infection. 12,13
UROLOGY
I OCTOBER
1992
/
VOLUME 40, NUMBER 4
Once children without a history of infection were identified, they were managed in a standard fashion. All patients were placed on antibiotic prophylaxis and a strict surveillance regimen. In general, patients only underwent immediate surgery for high grade reflux (grade 4 or 5) or failure to comply with a prophylaxis schedule, or breakthrough infection. The greatest deterent to screening is the relative invasiveness of the VCUG, which requires catheterization in an awake child and radiation exposure. One can decrease exposure with a radionuclide VCUG,14 but unfortunately, there is no satisfactory noninvasive means of detecting vesicoureteral reflux. The renal ultrasound failed to detect VUR in over 70 percent of those in whom it was employed as a screen in our population. It is unreasonable, therefore, to rely solely on this modality when evaluating children in whom reflux is a possibility. The highest grades of reflux may present with hydronephrosis seen on a renal ultrasound and some of our patients were identified in this manner, 15x18Ultrasound screening will, therefore, identify some patients with unsuspected high-grade reflux, but will miss others with lower grades. This study does not answer the question: Who among those without a history of infection should or should not be screened for reflux? Only long-term prospective follow-up of these children will provide the answer. On the other hand, by evaluating certain populations without a history of infection, a group of children with VUR will be identified with reflux, the severity of which at initial diagnosis equals that found in an infected population. At a single institution, almost an equivalent number of children with reflux were discovered among these uninfected populations. Finally it appears that more males will be identified if non-infected groups are screened. Children’s Hospital of Buffalo 219 Bryant Street Buffalo, New York 14222 (DR. GREENFIELD) References 1. Smellie J, and Normand C: Reflux nephropathy in childhood. in Ho&n RC (Ed\: Reflux Nenhrooathv. New York., 1979. Kin&d-Smith, pp 14-26. 2. Baker R, and Barbaris HT: Comparative results of urological evaluation of children with initial and recurrent urinary tract infections, J Urol 116: 500 (1976). 3. Van den Abbeele AD, Treves ST, and Lebowtiz RL: Vesicoureteral reflux in asymptomatic siblings of patients with known I
&
,,
341
reflux: radionuclide cystography, Pediatrics 79: 147 (1987). 4. Sujka S, Piedmonte M, and Greenfield S: Enuresis and the voiding cysto-urethrogram: a reevaluation. Presented at Urologic Section, American Academy of Pediatrics, New Orleans, Louisiana, November, 1987. 5. Shafir R, et al: Vesicoureteral reflux in boys with hypospadias, Urology 20: 29 (1982). 6. Parrott TS, and Woodard JR: Importance of cysto-urethrography in neonates with imperforate anus, Urology 13: 607 (1979). 7. Steinhart JM, Kuhn JR and Eisenberg MD: Ultrasound screening of healthy infants for urinary tract abnormalities, Pediatrics 82: 609 (1988). 8. Risdon RA: Reflux nephropathy, Diagn Histopathol 4: 61 (1981). 9. Winberg J, Bollgren I, and Kallenius G: Clinical pyelonephritis and focal renal scarring, Pediat Clin North Am 29: 801 (1982). 10. Smellie JM, Edwards D, and Normand ICS: Effects of ves-
342
icoureteric reflux on renal growth in children with urinary tract infection, Arch Dis Child 56: 593 (1981). 11. Skoog SJ, Belman AB, and Majd M: Non-surgical approach to management of primary vesico-ureteral reflux, J Urol 138: 941 (1987). 12. Bailey RR: End-stage reflux nephropathy, Nephron 27: 302 (1981). 13.. Bakshandeh K, Lynne C, and Carrion H: Vesicoureteral reflux and end staee renal disease. 1 Urol 116: 557 (1976). 14. Conway JJ,king LR, and BArnan AB: Detection of vesicoureteral reflux with radionucleotide cystography, Am J Roentgen01 115: 720 (1972). 15. Schneider K, et al: Screening for vesicoureteral reflux in children using real-time sonography, Pediatr Radio1 14: 400 (1984). 16. Kangarloo H, Gold RH, and Fine RN: Urinary tract infection in infants and children evaluated by ultrasound, Radiology 154: 367 (1985).
UROLOGY
I
OCTOBER 1992
I
VOLUME 40, NUMBER 4
