Acute Focal Bacterial Nephritis (Acute Lobar Nephronia) 1

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1 Diagnostic Radiology Acute Focal Bacterial Nephritis (Acute Lobar Nephronia) 1 Arthur T. Rosenfield, M.D., Morton G. Glickman, M.D., Kenneth J. W. Taylor, M.D., Ph.D., Michael Crade, M.D., and John Hodson, F.R.C.P. (London) Acute lobar nephronia (ALN) refers to a renal mass caused by acute focal infection without liquefaction. The radiological findings in 12 patients with 13 episodes of ALNare described. A characteristic combination of uroradiological findings is (a) a relatively sonolucent mass which disrupts corticomedullary definition on ultrasonography; (b) a solid-appearing mass on other uroradiological studies; and (c) a positive gallium image in the region of the mass, which may be associated with increased activity elsewhere in the same or opposite kidney. The angiographic finding of significant venous narrowing within the mass associated with only minor arteriographic abnormalities is characteristic of ALN as well. INDEX TERMS: Computed tomography, kidneys, a[ 1].1211 Kidney neoplasms, diagnosis, a[ 1].324 Kidneys, infection Kidneys, radionuclide studies. Kidneys, ultrasound studies Pyelonephritis, a[ 1].212 Radiology 132: , September 1979 ACUTE LOBAR nephronia (ALN), a term analogous to '" acute lobar pneumonia, refers to a renal mass caused by acute focal infection without liquefaction (1). It has been experimentally produced in pigs by surgery designed to create vesicoureteral reflux with subsequent deliberate infection of the urine (2, 3) (Figs. 1 and 2, a). ALN may mimic a tumor (Fig. 2, b) or abscess clinically and radiologically, and a combination of imaging techniques correlated with the clinical history is frequently required to make a diagnosis. This paper describes the uroradiological findings in 12 patients with 13 episodes of ALN. METHODS AND MATERIALS Twelve patients with 13 episodes of fever and flank pain presented during an 18-month period. In each instance, a renal mass was subsequently demonstrated. There were 2 children and 10 adults (range, 14 weeks to 66 years); 6 were male and 6 were female. The clinical features are summarized in TABLE I. Excretory urography was performed during 12 episodes, nephrotomography during 7, gray-scale ultrasonography during 13, gallium imaging during e, arteriography during 5, epinephrine venography during 3, and computed tomography (CT) during 1. The diagnosis was confirmed histologically in 3 patients treated by nephrectomy. Gray-scale ultrasound examinations were performed using standard analog, digital, and real-time equipment. Longitudinal and transverse sections of the right kidney were obtained through the liver with the patient supine; coronal (longitudinal) and transverse scans of the left kidney were obtained through the spleen with the patient lying on his right side. These techniques permitted detailed definition of renal parenchymal anatomy (4, 5) (Fig. 3). Urography, nephrotomography, gallium scanning, arteri- TABLE I: CLINICAL FEATURES IN LOBAR NEPHROMA (13EPISODES) Fever 13 Flank pain 13 Pyuria 13 E. coli bacteriuria 12 E. coli septicemia 4 Klebsiella bacteriuria and septicemia 1t History of recurrent urinary tractinfections 4 Diabetes mellitus 3 Medullary sponge kidney 1 History of nephrolithiasis 1 Crohn disease of thecolon 1 One patient with E. coli septicemia had pyuria, buturine cultures were negative. t E. coli and Klebsiella were found inboth blood and urine cultures. ography, and epinephrine venography were performed using standard techniques. ALN was diagnosed if (a) histological examination demonstrated renal parenchymal infection within a mass without central liquefaction or (b) imaging unequivocally demonstrated a solid mass in a patient with a characteristic history and physical signs and both the mass and the symptoms resolved during therapy. RESULTS Documentation ofinfection: All patients presented with fever and flank pain. E. coli was found in urine cultures during 12 of the 13 episodes and in blood cultures during 3 of these 12. In one episode Klebsiellasp. was also found in both blood and urine cultures. The only patient with a negative urine culture had pyuria and a blood culture that grew E. coli; therefore, the negative urine culture may have been spurious. Mass: Excretory urography and/or gallium imaging 1 From thedepartment of Diagnostic Radiology, Yale University School of Medicine, New Haven, Conn. Presented at the Sixty-fourth Scientific Assembly and Annual Meeting of theradiological Society of North America, Chicago, 111., Nov. 26-Dec. 1, Received Feb. 22, 1979 and accepted May 31. sjh 553

2 554 ARTHUR T. ROSENFIELD AND OTHERS September a,b 1c,d Fig. 1. Experimental acute lobar nephronia. a. Normal excretory urogram in a pig. b. Cystogram obtained alter surgical creation of vesicoureteral reflux demonstrates reflux into the pyramids in the upper pole of the right kidney. c. Following infection of the urine within the bladder. fever developed. The urogram demonstrates swelling of the upper pole with decreased nephrogram density (ALN). d. The infection was successfullytreated with antibiotics. Three weeks alter resolution, the pig died unexpectedly. The right kidney contains a scar at the site of the previous ALN. A smaller scar is present in the medial aspect of the lower pole. showed a focal abnormality in an otherwise normal kidney in 9 patients (Figs. 4 and 5) and demonstrated a diffuse abnormality in addition to a mass in 4 others (Fig. 6). Nine masses occurred in the left kidney and 3 in the right kidney; bilateral masses (one in the right kidney and two on the left) were present in one patient. The masses ranged from 2

3 Vol. 132 ACUTE FOCAL BACTERIAL NEPHRITIS Diagnostic 555 Radiology 2a,b Fig. 2. Acute lobar nephronia. a. Acute phase of ALN in a pig. A focal mass is present (arrows). b. Mass involving the upper %of the left kidney in a young woman. Nephrectomy was performed because malignancy was suspected. The specimen shows acute infection without abscess formation, (ALN). to 5 em in maximum length. Three of the 4 patients with both diffuse and focal abnormalities had nephrectomy after antibiotic therapy failed to control the infection. In each case, infection without liquefaction was found. Those episodes in which only focal lobar disease was present resolved rapidly and completely on appropriate antibiotics. Excretory urography and/or nephrotomography demonstrated a mass with a density slightly less than that of the uninvolved portions of the kidney in 10 patients. In 2 others (including one with bilateral masses), a nephrogram was absent in the affected region on nephrotomography, but angiography demonstratedvessels within the mass(es). In 6 patients, repeat urography one month later showed that the mass had resolved and no residual abnormality was present (Fig. 5, c). In 2 others, repeat urography several months later demonstrated focal scarring without calyceal clubbing at the site of the previous ALN (Fig. 4, f). In all of our patients, ultrasound examination on admission revealed a focal mass disrupting normal corticomedullary differentiation and containing scattered low-level echoes. Seven patients had follow-up ultrasound examinations one month later; in each case the mass had resolved, with return of normal corticomedullary differentiation in the involved region (Fig. 5, e). Both patients who had urography several months after the acute episode also had renal sonography at this time; in both, focal loss of parenchyma was observed on sonography as well as urography in the region of the previous ALN (Fig. 6, e). Gallium images were obtained during the acute phase of ALN in 8 patients. Four showed a focus of activity within the kidney at the site of the mass, and in each case the abnormality was larger on the gallium image than on the ultrasound scan (Fig. 5, a); in 2 cases gallium images were normal a month later. Two patients had focal abnormalities in both kidneys; one had bilateral masses on urography, ultrasound, and arteriography as well. Two patients had diffuse abnormal activity throughout the involved kidney (Fig. 6, b). Five patients had arteriographyduringthe acute episode, and four of them also had epinephrine venography. The arteries within the inflamed renal lobe were much less affected by the process than the veins. Although one or more masses were demonstrated at arteriography in each instance, they were not well demarcated from the adjacent renal parenchyma. Arteries were stretched and displaced but were not attenuated, narrowed, or obstructed (Figs. 4, d and 6, d). Oblique projections verified that even the arteries within the mass largely retained their normal caliber and smooth margins. No neovascularity or hypervascularity was present within or about the mass. Epinephrine venography showed mass effects, but it also demonstrated irregularity, narrowing, and obstruction of large and small veins within the mass (Figs. 4, e and 6, e). The venous abnormalities extended over a wider area and

4 556 ARTHUR T. ROSENFIELD AND OTHERS September a Fig. 3. Transverse sonogram of a normal right kidney (patient supine). The renal sinus (S) contains intense echoes. The cortex, including the septa of Bertin, produces low-level echoes and the medulla (arrows) is sonolucent. L = liver; g =gallbladder; V= inferior vena cava; A = aorta; sp = spine. presumably reflected the volume of renal tissue involved more accurately than the arterial abnormalities did. In 2 patients who did not have angiography at the time of the acute episode, it was performed several weeks after ALN had resolved clinically and urographically. In one patient, arteriography demonstrated no residual mass effect or scar, and the only abnormality was stenosis of one interlobar artery supplying the previously abnormal lobes; epinephrine venography was normal. The second patient was normal on both studies. Only one patient had CT (Fig. 6, f). The enlarged lower pole of the affected kidney consisted of solid tissue which was similar in density to the remainder of the renal parenchyma before and after injection of contrast medium. One child had voiding cystourethrography following resolution of the infection, and bilateral vesicoureteral reflux was demonstrated. Cystography was not performed in any other patient; therefore, the possibility that renal infection resulted from vesicoureteral reflux was not in- Fig year-old man with a history of left renal stones, presenting with fever and left renal colic. E. coli grew in urine cultures. a. Excretory urogram several years prior to the present admission is normal. vestigated in these cases. No alternate mechanism of introduction of infection was apparent, and the cause of ALN in these cases remains speculative. DISCUSSION When the urine in the bladders of pigs with surgically created vesicoureteral reflux was deliberately infected with E. coli, intrarenal reflux resulted in focal infection of the renal parenchyma (2,3) (Fig. 1, b). During these episodes of infection, excretory urography demonstrated a focal mass containing diminished nephrogram density (Fig. 1, c). Because the extent of infection was determined by the lobe(s) into which intrarenal reflux flowed, the phrase "acute lobar nephronia" was used to describe this condition (1). We have extended the use of this term to describe bacterial involvement of the renal parenchyma without abscess formation regardless of etiology. Our series consisted of patients whose radiographic b. Excretory urogram on admission demonstratesa mass in the lateral aspect of the left kidney (arrowheads) with a slightly decreased nephrogram density. One middle calyx and infundibulum are not opacified. c. Coronal scan of the left kidney through the spleen (patient lying on right side) demonstrates a relatively lucent ovoid mass (M) in the lateral aspect of the left kidney. Renal parenchymal definition adjacent to the mass is preserved (the arrow points to a pyramid). S = spleen; Si = renal sinus. d. Selective renal arteriogram shows large arteries displaced by the mass but not stretched or attenuated. A few small arteries are narrowed. No neovascularity is present to suggest abscess. e. Epinephrine venography shows narrowed, irregular veins within the mass. The veins are more severely affected than the arteries. Both the symptoms and the mass responded rapidly to antibiotics. f. Urogram taken six months after the acute episode demonstrates focal loss of parenchyma (arrowheads) at the site of previous ALN. g. Longitudinal scan of the upper portion of the left kidney seven months after the acute episode. The mass has completely regressed, leaving a scar (arrowheads). Renal scars are characterized at ultrasonography by parenchymal atrophy surrounding a narrow zone of dense echoes (arrow) (28).

5 Vol. 132 ACUTE FOCAL BACTERIAL NEPHRITIS Diagnostic 557 Radiology

6 558 ARTHUR T. ROSENFIELD AND OTHERS September 1979 Sc-e Fig year-old woman with a history of several urinary tract infections presenting with fever and right flank pain. E. coli grew in urine and blood cultures. a. Urogram demonstrates a mass on the lateral surface of the right kidney, extending toward the lower pole. b. Gallium image demonstrates multiple zones of increased activity (arrow) in the right kidney. c. Follow-up urogram three weeks later demonstrates resolution of the mass. d. Transverse scan taken at the level of the mass during the acute episode shows that corticomedullary differentiation is normal anteriorly but disrupted posteriorly by a mass (m) containing low-level echoes. L :::: liver; 5 =renal sinus; sp = spine. e. Three weeks later, follow-up ultrasound examination of the right kidney (arrowheads) demonstrates normal corticomedullary differentiation throughout and return of the involved renal lobe to normal size. Arteriography and epinephrine venography were normal at this time. findings and clinical course were identical to those in the pigs with ALN and distinct in several respects from those in human patients with acute pyelonephritis. While the mechanism of infection in the pigs was proved, in our patients it was only investigated by cystography in one case. Since this study demonstrated vesicoureteral reflux, the mechanism may be the same as that in the pigs. This idea is further supported by the identification of E. coli as the infecting organism in all cases. However, we are using the term "acute lobar nephronia" as a description of clinical and uroradiological features rather than a statement of etiology. The identical features of the disease in the experimental model and in the human patients may indicate a relationship, if further investigation documents an identical mechanism. While the findings in ALN seem new, few patients with

7 Vol. 132 ACUTE FOCAL BACTERIAL NEPHRITIS 559 Diagnostic Radiology 6a-c 6d-f Fig year-old diabetic woman with fever and left flank pain. E. coli grew in urine and blood cultures. a. Excretory urogram demonstrates a mass in the lower lateral aspect of the left kidney. The left kidney excretes a smaller volume and less dense contrast medium than the right kidney. b. Gallium image demonstrates diffuse abnormal activity throughout the left kidney. c. Longitudinal sonogram through the left kidney demonstrates an ovoid mass (M) containing low-level echoes in the lateral aspect of the lower pole. d. Arteriogram reveals arteries displaced about a round mass. The displaced arteries are not compressed or attenuated. The only arteriographic abnormality is encasement of a vessel traversing the mass (arrow). e. Epinephrine venography shows severely distorted, narrowed, and obstructed veins, especially in the lower pole. f. CT scan with contrast enhancement demonstrates approximately the same density in the mass (arrow) as in normal renal parenchyma. acute renal infection undergo uroradiological studies during the'aciite phase of the disease. Reports describing "acute pyelonephritis" state that excretory urography is often normal (6-8). If abnormalities are present, however, they characteristically consist of generalized renal enlargement, decreased density of excreted contrast medium, and/or dilatation of the collecting system (6-11). However, in one series of 40 patients with acute pyelonephritis who had excretory urography during the acute phase, 2 had focal renal enlargement similar to ALN (6). Diagnosis of ALN in this series was strongly suggested by symptoms and signs of unilateral renal infection and urographic demonstration of a mass in the symptomatic kidney. In most instances, the mass was slightly lower in nephrographic density than the uninvolved renal lobes. In 2 patients the density of the nephrogram within the mass was markedly decreased. Our series suggests that ultrasonography and gallium scanning may contribute differential diagnostic features while verifying the presence of intrarenal abnormality, thus

8 560 ARTHUR T. ROSENFIELD AND OTHERS September 1979 proving helpful in further evaluating equivocal cases or verifying a suspected diagnosis. On ultrasound examination, high-level central echoes arise from the normal renal sinus. The cortex produces lower-level echoes, while the medulla is virtually echo-free (Fig. 3). Punctate echoes may be reflected from the arcuate vessels at the corticomedullary junction (4, 5). In all of our patients, lobar nephronia appeared at ultrasonography as a focal mass which disrupted corticomedullary differentiation and contained low-level echoes. Lobar nephronia may mimic tumor, abscess, or infection on ultrasonography. An abscess or infected cyst can be sonolucent or contain echoes due to debris (12, 13). If a debris/fluid level is present (13), the diagnosis of ALN is excluded. A mass with an ovoid shape and/or irregular margins suggests lobar nephronia rather than abscess, but the data are not sufficient for a firm diagnosis. Although ALN can usually be distinguished from abscess by combining ultrasound with other uroradiological studies, this may not be crucial, since current evidence suggests that both diseases should initially be treated with antibiotics, with surgery reserved for lesions which fail to resolve (14). Pyonephrosis and perinephric abscess may also be confused with ALN on clinical examination, but they can be distinguished by ultrasound. Pyonephrosis is typically manifested as debris within a hydronephrotic collecting system on ultrasound examination (5, 15), which may also show a debris/fluid level in the dilated collecting system (5); a perinephric abscess is seen as a fluid collection around the kidney. Tumors have a variety of gray-scale ultrasound appearances but invariably disrupt normal renal anatomy and are rarely as sonolucent as ALN. However, demonstration of rapid change throughout sequential examinations may be required to exclude neoplasm. Renal abscess, lobar nephronia, and some neoplasms produce focal abnormalities in the kidney on gallium images (16-18). However, this series suggests that abnormalities which are larger on the gallium image than on the urogram or sonogram favor ALN. Demonstration of bilateral abnormalities on gallium images, correlated with a focal mass on the urogram and sonogram, strongly suggests ALN. Angiography may be necessary in some cases if the delay entailed in therapeutic trial of antibiotic treatment and serial ultrasound examinations is to be avoided. Angiographic findings have been reported in a few patients with acute bacterial nephritis (6, 10, 19-23). An abnormal nephrogram on arteriography and disorganization of venous architecture on epinephrine venography are the predominant findings, a pattern similar to the angiographic abnormalities in ALN in this series. The arteries are relatively unaffected, while the veins are narrowed, irregular, and/or obstructed. Presumably, interstitial edema and pus induce spasm or inflammatory compression of the walls of veins but do not seriously affect arteries, which have thicker, more muscular walls. Although hypovascular renal tumors also tend to produce more severe and more readily visible abnormalities in veins than in arteries, the disparity between venous and arterial abnormalities is, in our experience, considerably more marked in ALN, permitting an accurate differential diagnosis. Focal scars and clubbed calyces have been noted in long-term follow-up studies of children who have had episodes of acute pyelonephritis (19, 24). In adults, follow-up urograms of severe bacterial nephritis have demonstrated uniformly small kidneys with slightly clubbed calyces (20, 25). The 2 patients in our series who had follow-up urograms and sonograms several months after the episode of ALN demonstrated focal loss of parenchyma in the region previously involved by ALN, but without an associated clubbed calyx. However, scars may take two to three years to fully develop (26). CONCLUSIONS In the presence of fever and flank pain, demonstration of a renal mass should raise suspicion of abscess or ALN in addition to neoplasm. The characteristic radiological findings of ALN are (a) a relatively sonolucent, ovoid mass on ultrasound examination which disrupts corticomedullary definition and produces some low-level echoes; (b) a solid-appearing mass on other imaging studies such as excretory urography, CT, or angiography; and (c) abnormal gallium uptake at the location of the mass, which may be associated with increased activity elsewhere in the same or opposite kidney. In addition. if angiography is performed, narrowing and obstruction of veins within the mass associated with only minor arteriographic abnormalities is Characteristic of ALN. The distinction between ALN, abscess, and tumor can also be made by needle aspiration of the affected area (27). Our experience suggests that the coordinated evaluation of a combination of imaging techniques is frequently sufficient to diagnose ALN and permit conservative medical therapy without confirmation by needle biopsy or surgery. However, a relatively sonolucent mass on ultrasonography which is solid on other uroradiological studies and has abnormal gallium activity may occasionally be seen with some tumors such as lymphoma: thus serial uroradiologleal studies such as ultrasound should be used to follow the process to resolution. It must be emphasized that radiological investigation of the kidneys during episodes of acute infection is a relatively new development. The lesions described in this article are of particular interest in that they are not abscesses, nor did they result in abscesses; moreover, they have not yet been shown to result from ascending infection. The natural history is not clear, since follow-up examinations have been possible in only 2 patients, both of whom have exhibited subsequent focal scarring. Further study is required to determine whether all lesions of ALN result in focal scars. ACKNOWLEDGMENTS: We thank Drs. Paul Hoffer and Carl Jaffe for their aid and advice, Drs. Arnold Baskin, Bruce Simonds. and Robert Lowman

9 Vol. 132 ACUTE FOCAL BACTERIAL NEPHRITIS 561 Diagnostic Radiology for their case material, Ms. Joan Wallace for her editorial assistance, Ms. Cheryl Wilcox for her research assistance, and Ms. Sandra Sudac for preparing the manuscript. REFERENCES 1. Hodson CJ: The pathogenesis of reflux nephropathy. [In] Margulis AR, Gooding CA, ed: Diagnostic Radiology. San Francisco, University of California, 1978, pp HodsonCJ, Maling TMJ, McManamon PJ, et al: The pathogenesis of reflux nephropathy (chronic atrophic pyelonephritis). Br J Radiol [Suppl 13]:1-26, Hodson J, Maling TMJ, McManamon PJ, et al: Reflux nephropathy. Kidney Int 8 [Suppl 4]:S50-858, Aug Cook JH III, Rosenfield AT, Taylor KJW: Ultrasonic demonstration of intrarenal anatomy. Am J RoentgenoI129: , Nov Rosenfield AT, Taylor KJW, Crade M, et al: Anatomy and pathology of the kidney by gray scale ultrasound. Radiology 128: , Sep Silver TM, Kass EJ, Thornbury JR, et al: The radiological spectrum of acute pyelonephritis in adults and adolescents. Radiology 118:65-71, Jan Little PJ, McPherson DR, de Wardener HE: The appearance of the intravenous pyelogram during and after acute pyelonephritis. Lancet 1: ,5 Jun Evans JA, Meyers MA, Bosniak MA: Acute renal and perirenal infections. Semin RoentgenoI6: , Jul Bailey RR, Little PJ, Rolleston GL: Renal damage after acute pyelonephritis. Br Med J 1: , 1 Mar Davidson AJ, Talner LB: Urographic and angiographic abnormalities in adult-onset bacterial nephritis. Radiology 106: Feb 1973 '. 11. Kass EJ, 8i1v~~ TM, Konnak JW, et at; The urographic findings In acute pyelonephritis: non-obstructive hydronephrosis. J Urol 116: , Nov Schneider M, Becker JA, Staiano S, et al: Sonographic-radiographic correlation of renal and perirenal infections. Am J Roentgenol 127: , Dec Hill M, Sanders RC: Gray scale B scan characteristics of intraabdominal cystic masses. J Clin Ultrasound 6: , Aug Schiff M Jr, Glickman M, Weiss RM, et al: Antibiotic treatment of renal carbuncle. Ann Intern Med 87: , Sep Rosenfield AT, Taylor KJW: The kidney. [In] Taylor KJW: Atlas of Gray Scale Ultrasonography. New York, Churchill Livingstone, 1978, Chapt 8, pp Hopkins GB, Kan M, Mende CW: Early 67Ga scintigraphy for the localization of abdominal abscesses. J Nucl Med 16: , Nov Antoniades J, Honda T, Croll MN, et aj: Gallium 67 scanning in patients with renal cell carcinoma. J Urol 109: , Apr Hurwitz SR, Kessler WO, Alazraki NP, et al; Gallium-67 imaging to localize urinary-tract infections. Br J Radiol 49: , Feb Lebowitz RL, Fellows KE, Colodny AH: Renal parenchymal infections in children. Radiol Clin North Am 15:37-47, Apr Lilienfeld RM, Lande A: Acute adult onset bacterial nephritis: long-term urographic and angiographic followup. J UroI114:14-20, Jul Koehler PR: The roentgen diagnosis of renal inflammatory masses-special emphasis on angiographic changes. Radiology 112: , Aug Goldman ML, Gorelkin L, Rude JC III, et al: Epinephrine renal venography in severe inflammatory disease of the kidney. Radiology 127:93-101, Apr Rosch J, Antonovic R, Goldman ML, et al: Epinephrine renal venography. Fortschr Geb Roentgenstr Nuklearmed 123: , Dec Hodson J: Radiology in pyelonephritis. Curr Probl RadioI2:1-32, Jul-Aug Davidson AJ, Talner LB: Late sequelae of adult-onset bacterial nephritis. Radiology 127: , May Filly R, Friedland GW, Govan DE, et al: Development and progression of clubbing and scarring in children with recurrent urinary tract infections. Radiology 113: , Oct Pfister RC, Stanley RJ, Geisse G, et al: Percutaneousaspiration of inflammatory renal masses: separation of medical from surgical disease (abst). Am J Roentgenol 128:522, Mar Kay CJ, Rosenfield AT, Taylor KJW, et al: Ultrasound characteristics of chronic atrophic pyelonephritis. Am J Roentgenol 132: 47-49, Jan 1979 Department of Diagnostic Radiology Yale University School of Medicine 333 Cedar St. New Haven, Conn

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