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Published online before print September 24, 2001, 10.1148/radiol.2212010146
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(Radiology. 2001;221:366-370.)
© RSNA, 2001

Pediatric Imaging

Renal Fibrosis: Prediction from Acute Pyelonephritis Focus Volume Measured at 99mTc Dimercaptosuccinic Acid SPECT1

Yuan-Yow Chiou, MD, Shan-Tair Wang, PhD, Ming-Jer Tang, MD, PhD, Bi-Fang Lee, MD and Nan-Tsing Chiu, MD

1 From the Department of Pediatrics and Institute of Clinical Medical Sciences (Y.Y.C.), Public Health (S.T.W.), Physiology (M.J.T.), and Nuclear Medicine (B.F.L., N.T.C.), National Cheng Kung University Medical Center and College of Medicine, 138 Sheng-Li Rd, Tainan, Taiwan 704, Republic of China. Received December 13, 2000; revision requested January 16, 2001; revision received April 2; accepted April 9. Supported in part by grants from the National Science Council, Republic of China (NSC 88-2314-B-006-071 and 87-2314-B-006-001). Address correspondence to N.T.C. (e-mail: ntchiu@mail.ncku.edu.tw).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate whether acute pyelonephritis lesion volume derived from acute technetium 99m (99mTc) dimercaptosuccinic acid (DMSA) renal single photon emission computed tomographic (SPECT) images is predictive of the development of subsequent renal fibrosis.

MATERIALS AND METHODS: Children with acute pyelonephritis underwent 99mTc DMSA renal SPECT during acute infection and 6–10 months later. At quantitative analysis, the volume of photopenic lesions and the ratio of radioactivity in the photopenic lesion to that in normal renal tissue were calculated. Sensitivity, specificity, and positive and negative predictive values were determined.

RESULTS: Sixty-nine acute pyelonephritis foci in 44 children were analyzed. Thirty-seven (54%) of these lesions were normal on follow-up renal scans, while 32 (46%) developed scars. Significant differences in the photopenic lesion volume were found between the two groups (P < .001). When photopenic lesion volume indicated a positive diagnosis (>=4.6-cm3 lesion volume), sensitivity, specificity, positive predictive, and negative predictive values were 96.7%, 92.3%, 90.6%, and 97.3%, respectively.

CONCLUSION: Quantitative analysis of acute DMSA renal SPECT findings is valuable in predicting renal fibrosis. The volume of an acute pyelonephritis lesion is useful in predicting the development of fibrosis.

Index terms: Kidney, infection, 81.2121 • Kidney, SPECT, 81.12162 • Nephritis, 81.2121 • Single photon emission computed tomography (SPECT), in infants and children, 81.12162


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Urinary tract infection (UTI) is one of the most common diseases in children. Severe sequelae such as hypertension, renal failure, and end-stage kidney disease could develop if the infection leads to acute pyelonephritis (APN) and subsequently to renal fibrosis (scarring) (1,2). Hypertension during adolescence or early adulthood has been reported in 10%–18% of the patients with renal scarring, and the risk appears to be greater in those with multifocal scarring (3). Renal scarring associated with vesicoureteral reflux (VUR) accounts for 10%–20% of patients with end-stage renal disease (4,5). Reduction of the incidence of renal scarring requires early diagnosis and aggressive treatment of APN. Unfortunately, it is difficult to establish an accurate early diagnosis of renal parenchymal infection on the basis of the patient’s clinical presentation, especially in small young children (6,7). It is important to establish a tool to evaluate the progress of APN.

The authors of several studies have reported that technetium-99m (99mTc) dimercaptosuccinic acid (DMSA) scintigraphy is a highly sensitive and specific noninvasive imaging modality for detection of renal inflammation, because it can demonstrate radiotracer uptake defects in APN foci (8,9). In one report (10), the authors said it had a specificity of 100% and a sensitivity of 87% for prospective detection of APN, when compared with histopathologic criteria. The application of single photon emission computed tomography (SPECT) together with DMSA scintigraphy further enhanced the sensitivity of DMSA in the detection of APN to 96% (11). DMSA scintigraphy is more effective and has better sensitivity for the detection of permanent renal damage (scarring) than do urography and ultrasonography (US) (12,13). It may become even more valuable if acute DMSA scintigraphy can provide prognostic information that helps determine whether APN lesions are at risk of developing into scars, thereby requiring intensive treatment.

With the assistance of SPECT, we can accurately assess the volume of an APN lesion. The issue of whether volume is associated with the process of scar formation has not, to our knowledge, been determined. Thus, the purpose of our study was to assess the value of the volume of an APN lesion derived from acute DMSA renal SPECT images as a predictor for the development of subsequent renal fibrosis.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Population
Children admitted to our pediatric unit with febrile symptomatic UTI were entered consecutively in this prospective study. The inclusion criteria were (a) age between 1 week and 16 years (inclusive); (b) evidence of UTI (fever, >=38°C; positive urine culture, >=105 colony-forming units of bacteria of a given species per milliliter; leukocyturia, more than five cells per high power field); and (c) presence of focal or multifocal photon defects on a DMSA renal SPECT scintigram obtained during acute infection. The exclusion criteria were (a) history of UTI; (b) concurrent congenital urogenital abnormality or uropathy, except VUR; (c) recurrent UTI infection between the initial and subsequent scintigrams; (d) diffuse hypoactive kidney on DMSA renal SPECT scintigram; and (e) space-occupying lesion at US. The study protocol was approved by our institutional review board. Informed consent was obtained from the patients’ parents after a full explanation.

After bacteriologic samples had been obtained from urine and blood, empiric parenteral treatment with ampicillin (Ancillina; China Chemical & Pharmaceutical, Taipei, Taiwan) and gentamicin (Yung Shin Pharmaceutical Industrial, Taichung, Taiwan) was administered for 3–5 days until the fever had subsided for 48 hours. This was followed by an approximately 10-day course of oral antibiotics according to the sensitivity of each drug to the bacterial infection. All patients received treatment within 7 days of fever occurrence. A low dose of trimethoprim or cephalothin was applied until voiding cystourethrography was performed 2–4 weeks later. Presence of VUR was graded according to the system of the International Reflux Study in Children (14). US of the urinary tract was performed at the time of admission to exclude congenital uropathy and space-occupying lesions.

99mTc DMSA Renal SPECT
Initial 99mTc DMSA renal SPECT was performed within 1 week after admission. The results were used as the reference standard for determination of APN. Those who had APN underwent repeat DMSA renal SPECT more than 6 months later. In general, an APN lesion takes at least 5 months to stabilize (15). If a renal cortical defect persisted, a renal scar was diagnosed. According to these results, we (Y.Y.C., B.F.L., N.T.C.) together classified the children into scar and nonscar groups and the lesions into sequelae and nonsequelae groups. Lesions that were persistently present on follow-up DMSA renal SPECT scans were assigned to the sequelae group. Those that resolved completely were classified into the nonsequelae group. Children with any sequelae-group lesion were assigned to the scar group, and those in whom all lesions resolved completely were assigned to the nonscar group.

For renal SPECT imaging, each subject was injected intravenously with 2.5 MBq per kilogram of body weight (minimal dose, 20 MBq) of 99mTc DMSA. Imaging was initiated approximately 2–3 hours later. We used a triple-headed rotating gamma camera (Multispect3; Siemens Medical Systems, Hoffman Estates, Ill) with high-resolution collimators. The SPECT data were acquired over a circular 360° rotation, 120 steps, and 35 seconds per step in a 128 x 128 x 16 matrix. Reconstruction was performed with filtered back projection by using a Butterworth filter (cut-off frequency, 0.55 of the Nyquist frequency; power factor, 7) with attenuation correction according to the Chang method (16). After reconstruction, each image was sectioned at 1-pixel (0.89-mm) intervals in the transverse, coronal, and sagittal planes. Three-dimensional images were also constructed. Any photopenic area in the renal cortex was considered abnormal. The number and location of photopenic areas, homogeneity of uptake, presence of renal volume loss, changes in renal contour, and differential renal function were recorded. Two experienced nuclear medicine physicians (B.F.L., N.T.C.) who were unaware of the patient’s clinical signs and symptoms visually assessed the SPECT images independently to render their diagnosis. Disagreements were resolved in discussion to reach a consensus interpretation. In a previous analysis, the agreement between these two physicians in the interpretation of DMSA renal SPECT was substantial ({kappa} = 0.78 for normal-abnormal DMSA scan dichotomy for a kidney; unpublished data, 1999).

For quantitative analysis of the acute DMSA renal SPECT images, we adopted the empiric-threshold method for volume determination (17,18). According to our previous phantom study results (unpublished data, 1996), the optimal threshold value for our gamma camera system was 41%. We analyzed the volumes and radioactivity of normal renal tissue and acute inflammatory foci from the acute DMSA renal SPECT images. We then calculated the photopenic lesion volume and radioactivity change (the ratio of radioactivity in the photopenic lesion to that in remaining normal renal tissue of the ipsilateral kidney) of the photopenic lesion to compare the sequelae and nonsequelae groups.

Statistical Analysis
Sex distribution between the scar and nonscar groups was compared with the Fisher exact test; and age distribution, with the Fisher-Freeman-Halton test (19). Mann-Whitney statistics were used to compare photopenic lesion volume and radioactivity change of the photopenic area between the sequelae and nonsequelae groups. Multiple logistic regression was used to determine the significance of age, sex, volume, and radioactivity change in predicting renal fibrosis. Because some patients had multiple foci and because these foci could be positively correlated, we used generalized estimating equations to calculate these effects (20). The radioactivity change of the photopenic area was correlated with the volume of the photopenic lesion by using the Spearman rank-order correlation. The cutoff value with maximum efficiency (ie, maximal sum of sensitivity and specificity) for a diagnostic measure was chosen for its positive predictive value for renal scarring. Unless indicated otherwise, continuous data were expressed as the mean plus or minus standard error. A P value of less than .05 was considered to indicate a significant difference.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Forty-four children, 29 boys and 15 girls (age range, 1–118 months; mean, 20 months ± 3.9), were included in this study. There were 69 APN foci found at acute DMSA renal SPECT. At follow-up DMSA renal SPECT performed 6–10 months later, all foci had resolved completely in 22 children; the other 22 children with permanent scar foci were defined as the scar group (Table 1). Age and sex distributions in the two groups were not significantly different. Furthermore, 32 (46%) of the 69 focal photon defects that subsequently developed into permanent scars were defined as the sequelae group; the remaining 37 (54%) lesions in 28 children (21 [75%] boys, seven [25%] girls) had resolved completely at follow-up and were defined as the nonsequelae group. The numbers of children and lesions and the outcomes are shown in Table 2.


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  		TABLE 1. Sex and Age between Scar and Nonscar Groups

 

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  		TABLE 2. Number of Children, Number of Lesions, and Outcome

 
Retrograde micturating cystourethrography was performed in 36 (82%) children, when parental permission was obtained. The average interval between admission and this examination was 4 weeks. Thirteen abnormal results were seen in 10 (27%) children, eight (44%) children with foci in the sequelae group and five (21%) children with foci in the nonsequelae group. In the patients with foci in the nonsequelae group, only unilateral VUR could be found. However, bilateral VUR was noted in six (32%) children in the sequelae group (P = .01, Fisher-Freeman-Halton test). In the sequelae group with VUR, three had grade I, three had grade II, six had grade III, and two had grade V VUR. In the nonsequelae group with VUR, all had grade I. There was a significant difference in the grades of reflux between the nonsequelae and sequelae groups (P < .001, Fisher-Freeman-Halton test).

In both the sequelae and nonsequelae groups, radioactivity change in the photopenic area was not linearly correlated with volume of the photopenic lesion (Spearman rank-order correlation coefficient = 0.5, P = .1). The means of lesion volume and radioactivity ratio between abnormal and normal renal tissue in the nonsequelae group were 2.5 cm3 ± 0.2 and 45% ± 1.2, respectively; in the sequelae group these values were 15.0 cm3 ± 2.0 and 39% ± 1.4, respectively (Fig 1). There was a significant difference in lesion volume between these two groups (P < .001). Although the nonsequelae group had a larger mean radioactivity ratio, the difference was not statistically significant (P = .33). The significance of lesion volume for prediction of renal fibrosis still held after adjustment for age, sex, and radioactivity change and was the only significant predictor in a multiple logistic regression (P < .001). A lesion volume 4.6 cm3 or larger was chosen as an indicator for subsequent development of scar; the sensitivity, specificity, positive predictive value, and negative predictive value were 96.7%, 92.3%, 90.6%, and 97.3%, respectively. Furthermore, there were six children (three boys, three girls) with 18 foci in whom eight foci developed into permanent renal scarring; the other 10 foci resolved. The lesion volumes of the eight foci that developed into permanent scar were higher than those of the latter 10 foci (12.1 cm3 ± 2.8 vs 2.4 cm3 ± 0.4, P = .001) (Fig 2).



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  		Figure 1. Top: Scattergram shows radioactivity ratio between abnormal and normal renal tissue (L/N ratio) of the sequelae group (39% ± 1.4 ) and the nonsequelae group (45% ± 1.2). There was no significant difference between groups. Bottom: Scattergram shows lesion volume of the sequelae group (15.0 cm3 [ml] ± 2.0) and the nonsequelae group (2.5 cm3 ± 0.2). The sequelae group had significantly larger lesion volume than did the nonsequelae group (P < .001). Solid horizontal lines represent mean values in both scattergrams.

 


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  		Figure 2. Scattergram shows lesion volume in children with multiple foci that progressed to different outcomes: sequelae and nonsequelae groups. The volume of lesions that progressed to sequelae (12.1 cm3 [ml] ± 2.8) was significantly larger (P = .001) than that of lesions that resolved without sequelae (2.4 cm3 ± 0.4). The dotted line represents a lesion volume of 4.6 cm3.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
In children with febrile UTI, routine clinical and laboratory parameters are poor indicators for distinguishing APN from UTI without parenchymal involvement. Until now, 99mTc DMSA scintigraphy has been the most sensitive tool for detection of APN among children (8,9). Because DMSA scintigraphy can demonstrate anatomic and functional changes in renal parenchyma, it was believed that DMSA scintigrams could be used to predict renal scarring (21). The relationship between the area of renal parenchymal involvement and the risk of subsequent renal scarring has been roughly estimated by using acute planar DMSA scintigraphic results in one animal study (22). Planar DMSA scintigraphy can provide only two-dimensional images. With three-dimensional SPECT images, it is possible to accurately determine both volume and radioactivity level. Our results demonstrated that lesion volume determined with SPECT findings was a useful predictor of renal scarring. We also calculated the ratio of lesion volume to that of the ipsilateral whole renal volume (data not shown). The volume of an APN lesion was a superior determinant of the outcome than were volume ratio and radioactivity change.

After intravenous injection, 99mTc DMSA accumulates in the proximal tubular cells. Cortical uptake of this radiotracer depends on renal blood flow and proximal tubular cell membrane transport function (23). In pyelonephritic areas, the low uptake of DMSA will be confined to photopenic areas, due to locally reduced blood flow and/or a disturbed transport mechanism (13). The reduced blood flow is attributed to intravascular granulocyte aggregation leading to arteriolar or capillary occlusion, and the disturbed transport to the intratubular neutrophils that release toxic enzymes and produce superoxide (24). The combination of host immunologic response and bacterial virulence factors could further enhance tissue inflammation. With tissue ischemia and necrosis with edema change, the range of parenchymal injury would be more extensive, ultimately resulting in extended tissue volume and irreversible renal scarring (23). Therefore, an analysis of the lesion region and intensity with acute DMSA SPECT is a plausible method for predicting subsequent renal scarring. We believe that changes in radioactivity levels shown on DMSA scintigrams would be a reversible process in a limited region if these were caused solely by intravascular granulocyte aggregation, capillary occlusion, and/or local inflammation. On the contrary, if this process leads to tubular dysfunction, tubular cell death, and extensions into the interstitium, it would result in an imbalance of the repair process and a more extensive volume, both leading to irreversible renal scarring.

Renal scarring is also closely related to the normal process by which tissue recovers from damage. The failure of beneficial clearance of renal cells by means of apoptosis and/or the removal of apoptotic leukocytes before they lose membrane integrity will inevitably lead to the uncontrolled release of noxious contents. Undesirable disintegration of apoptotic cells prior to phagocytic clearance may not only exacerbate inflammation but also increase the risk of further rounds of immune-mediated tissue injury due to the release of potential intracellular autoantigens (25–28). These hypotheses remain to be verified, but they all describe possible sources of the exacerbation of local tissue injury. We believe that any lesion that undergoes the above-mentioned sequence and becomes a scar will cause a more extensive photopenic focus at DMSA scintigraphy. Therefore, in addition to the severity of regional function changes, we think it is necessary to consider the involved inflammatory photopenic lesion volume when analyzing nephropathy.

Various factors have been implicated as causes of renal scarring in children with UTI. The reported rate of renal scarring in children after APN varies between 37% and 80% (29–31). Duration of symptoms prior to initiation of therapy has been shown to be a factor in the development of renal fibrosis after APN (32,33). However, study results have suggested that there would be no difference in the frequency of renal scarring if treatment were to be started in the 1st week (7,29). Although a higher percentage of VUR was found in the sequelae group, renal damage could occur in the absence of reflux (34). Of 17 patients in the scar group in our study, nine (53%) had VUR and eight (47%) did not. Among the 26 patients who did not have reflux, nine (35%) had fibrosis. The evidence indicates that all children, regardless of age and sex, run a risk of renal scarring after APN. Thus, if one could successfully modulate the inflammatory response, postpyelonephritic renal scarring might be lessened. An immune modulator, oral prednisolone, was used as adjunctive therapy in an experimental piglet model (22) of severe reflux and APN, and it appeared to be effective in diminishing renal scarring. Our results emphasize the importance of inflamed photopenic lesion volume during an acute episode of infection; our findings may also provide evidence for the use of an immune modulator agent with more adequate selective criteria.

We have demonstrated that measurement of the volume of an APN focus with 99mTc DMSA renal SPECT is valuable for prediction of the occurrence of renal scarring and identification of those at high risk for scarring. Furthermore, the volume of the renal injury in the pathogenesis of renal fibrosis may be a more important and more accurate predictor than in situ inflammation.


   ACKNOWLEDGMENTS
 
We thank the National Cheng Kung University Department of Nuclear Medicine technical staff for their kind assistance. We also thank Bill Franke, MA, for proofreading and revising the English in this article.


   FOOTNOTES
 
Abbreviations: APN = acute pyelonephritis, DMSA = dimercaptosuccinic acid, UTI = urinary tract infection, VUR = vesicoureteral reflux

Author contributions: Guarantors of integrity of entire study, Y.Y.C., N.T.C.; study concepts, Y.Y.C., N.T.C.; study design, Y.Y.C., S.T.W., M.J.T., N.T.C.; literature research, Y.Y.C., N.T.C.; clinical studies, Y.Y.C., B.F.L., N.T.C.; data acquisition, Y.Y.C., B.F.L., N.T.C.; data analysis/interpretation, Y.Y.C., S.T.W., B.F.L., N.T.C.; statistical analysis, S.T.W.; manuscript preparation, Y.Y.C., S.T.W., N.T.C.; manuscript definition of intellectual content, all authors; manuscript editing, Y.Y.C., N.T.C.; manuscript revision/review and final version approval, all authors.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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