Review of Imaging Findings in Urinary Tract Infections

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Review of imaging findings in urinary tract infections ˜ MD , EL Martinez-Salazar MD. , J Tran DO , A Patino A Sureshkumar DO. , T Catanzano MD. PII: DOI: Reference:

S0887-2171(19)30062-9 https://doi.org/10.1053/j.sult.2019.09.004 YSULT 888

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Seminars in Ultrasound CT and MRI

˜ MD , Please cite this article as: A Patino EL Martinez-Salazar MD. , J Tran DO , A Sureshkumar DO. , T Catanzano MD. , Review of imaging findings in urinary tract infections, Seminars in Ultrasound CT and MRI (2019), doi: https://doi.org/10.1053/j.sult.2019.09.004

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1 Review of imaging findings in urinary tract infections

Author names and affiliations: Patiño A, MD.; Martinez-Salazar EL, MD.*; Tran J, DO*.; Sureshkumar A, DO.; Catanzano T, MD. *Contributed equally.

Department of Radiology, , University of Massachusetts Medical School-Baystate, Springfield, MA.

Corresponding author: Patiño A, MD Department of Radiology, Baystate Medical Center, 759 Chestnut St, Springfield, MA 01199. E-mail: [email protected]

ABSTRACT Acute urinary tract infection diagnosis is primarily performed on clinical grounds. Diagnostic imaging is, however, often necessary as part of the workup for poor response to treatment, to evaluate causative or contributory factors, complicated infections and chronic presentations. Appropriate knowledge of the most relevant radiological findings in urinary tract infections provides pertinent differential diagnosis and guides clinical management, including emergent and aggressive interventions. In this article we review Ultrasound and CT imaging findings of acute and chronic urinary tract infections.

2 INTRODUCTION

1

Urinary tract infection (UTI) diagnosis is largely made on clinical grounds . However, diagnostic imaging is frequently performed in at least three settings: 1) workup for an unclear clinical presentation; 2) to assess causative or contributory factors for complicated UTI such as obstructive uropathy, congenital malformations, strictures and tumors; 3) poor response to treatment, especially to evaluate complications and conditions that require emergent intervention, such as emphysematous pyelonephritis or renal 2

abscess . Clinically, UTIs are initially divided in complicated and uncomplicated depending on the population and risk factors. As most of the UTIs that require further imaging are complicated cases, we present them divided in acute and chronic infections according to the course of presentation and for each we review the most relevant imaging findings on US and/or CT radiological studies.

Acute infections Pyelonephritis This infection is one of the renal parenchyma and tubulo-interstitial space that results from 2

inoculation of an infective organism . The most common mechanism is ascending infection, in which the pathogen causes a relatively functional obstruction that favors its spread through the genitourinary 3

tract ⁠. An alternate mechanism of infection is hematogenous dissemination, which is less common. After clinical diagnosis is made, ultrasound (US) imaging is usually performed to rapidly evaluate pregnant patients and a small portion of other patients with certain conditions to rule out underlying 4

obstruction . Imaging findings of pyelonephritis in US are often incidental and correspond to only 20% of the positive cases

3,5

. Characteristic features are an enlarged kidney with either hypoechoic areas (due to

edema) or hyperechoic areas (due to hemorrhage) that follow a peripheral distribution and wedge-shaped morphology. These areas are associated with focal decreased perfusion on Doppler US compared to the renal parenchyma due to physiologic tubular ischemia

2

(Figure 1A) It should be noted that Spectral

Doppler imaging is superior to Color Doppler for defining hypoperfusion in general. CT is the imaging modality of choice to evaluate complicated pyelonephritis as it provides information 3

regarding the causative factors, the extension of infection and complications . CT features in acute

3 pyelonephritis are broad and include ill-defined wedge-shaped areas of low attenuation with decreased cortico-medullary differentiation radiating from the papilla to the cortical surface (Figure 1B). The pathophysiology of this finding corresponds to poorly or non-functioning parenchyma caused by vasospasm, tubular obstruction or interstitial edema

2, 4

.

Interestingly, when there are peripherally located rounded or masslike hypodensities, hematogenous spread of infection rather than direct inoculation should be suspected. This difference in anatomic involvement is the result of hematogenous infection seeding the cortex first, while ascending 4

pyelonephritis seeds the medulla initially . If the assessment is performed on unenhanced CT, it may be useful to narrow the window and level parameters to increase the contrast of the wedge-shaped areas. On a contrast enhanced CT, the optimal timing to assess for renal lesions is that corresponding to the nephrographic phase, given the 4

increased conspicuity of the abnormal perfusion areas .

A striated nephrogram is another imaging feature of acute pyelonephritis on CT. This term describes alternating linear areas of decreased enhancement from the papilla to the cortex, attributed to inflammatory debris obstructing the renal tubules with intervening normal tubules

2, 4

. This finding is

nonspecific and can also be seen in renal vein thrombosis, ureteric obstruction and contusion as the 6

same pathologic process occurs, namely tubular ischemia .

Pyelonephritis can also be encountered in two forms: focal and diffuse. The focal form is limited 7

to a localized area of a peripheral wedge or mass like hypodense lesion with surrounding fat stranding . In diffuse pyelonephritis, nephromegaly, poor enhancement of the parenchyma (delayed nephrogram) 7

and perinephric stranding are frequently seen in proportion to the severity of infection . Other specific findings may suggest certain pathologies, for example, urothelial thickening and hyperenhancement

without

renal

parenchymal

involvement

indicates

pyelitis

and

multiple

hyperattenuating foci on noncontrast CT (areas of hemorrhage) suggest acute hemorrhagic pyelonephritis, a rare form of infection.

4

It is important to keep in mind that pyelonephritis occurs as a dynamic process with areas of improvement and areas of progression. Resolution of imaging abnormalities lag behind clinical improvement. In moderate to severe cases, CT abnormalities may persist for weeks or months, thus, 4

follow-up can easily be misleading .

The differential diagnosis for acute pyelonephritis includes neoplasms (particularly in the setting of focal pyelonephritis), sarcoidosis and infiltrative malignant processes such as lymphoma or Castleman’s disease

2

. Similar findings between these entities occur as they have a common 3

pathophysiologic mechanism: interstitial nephritis . Striated nephrograms and wedge-shaped areas are also frequently seen with renal infarcts; to differentiate from infection, the presence of a thin rim of cortical enhancement due to collateral blood flow from the capsule may be helpful.

Renal and perinephric abscess Abscess formation may occur secondary to coalescent areas of infection in pyelonephritis or superimposed infection of a pre-existing hematoma or urinoma

2,8

. Immunosuppression, diabetes and

obstructive uropathy increase the risk of abscess formation. The most frequently isolated organisms in 7

renal abscesses are E. Coli, Proteus Mirabilis and Staphylococcus Aureus , while Candida species are more commonly seen in diabetic patients. Up to 20% of patients with an abscess may have a negative urine culture.

Renal abscess If acute pyelonephritis is not treated, the infection can lead to liquefactive necrosis and abscess formation. A renal abscess is confined to the renal parenchyma and, if the urinary tract is not obstructed, 4

it may drain spontaneously into the collecting system . Small abscesses may respond to antibiotics, but the mainstay of treatment is percutaneous drainage under US or CT guidance.

5 CT is the most accurate modality for diagnosis, evaluation of the extent of infection and follow-up. Renal abscesses initially appear as poorly marginated, cortical wedge-shaped/rounded non-enhancing areas of decreased attenuation (Figure 2A). As the abscess matures, it becomes well-marginated with a thick wall/pseudocapsule that can enhance in up to half of the cases and is better demonstrated on delayed 4

images during the excretory phase . The presence of gas in the abscess is rare, however in the absence 6

of invasive procedures, it strongly suggests that the lesion is secondary to a gas-forming pathogen . CT imaging appearance of a renal abscess can frequently be confused with a renal cystic lesion (Figure 2B); if present, an ill-defined surrounding area of decreased enhancement around the lesion may be helpful as it is suggestive of infection. Additionally, a secondarily infected renal cyst is indistinguishable from an 6

abscess clinically and radiologically . 4

US often fails to detect abscesses seen on CT . An abscess under US is frequently seen as a hypoechoic or anechoic complex lesion with increased through transmission and no internal vascularity on color Doppler. This former feature is important to distinguish it from a malignant process. Internal echogenic areas with dirty shadowing suggest the presence of internal air. Loculation and septations may also be present.

Perinephric abscess A perinephric abscess is an organized collection of purulent material that most often develops 6

directly from acute pyelonephritis or extension/rupture of a renal abscess into the perinephric space . It can also result after decompression of pyonephrosis. One third of the cases are seen in diabetic patients 4, 9

. The perinephric space is limited by the anterior and posterior pararenal fascia. It has an inverted

cone morphology and contains the kidneys, proximal ureters, adrenal glands and the perinephric bridging 8

septa (kunin septi) . A perinephric abscess extends from the renal capsule to the aforementioned perinephric space. On contrast enhanced CT, a perinephric abscess demonstrates central low density with rim enhancement and peripheral inflammatory changes such as perinephric fat stranding and thickening of the fascia

6 (Figure 3). If the lesion has thickened enhancing septa and regions of higher attenuation, a cystic 9

neoplasm should be suspected . On US, the radiographic findings correspond to a round mass-like lesion with a thick wall and variable internal echogenicity due to the presence of proteinaceous fluid, cellular debris, hemorrhages 9

and liquefied regions with flow in the periphery due to hyperemia .

Emphysematous Pyelonephritis (EPN) Emphysematous pyelonephritis is a life-threatening necrotizing infection with mortality as high as 70%. It consists of renal parenchyma and/or perinephric tissue necrosis. The presence of gas is attributed 7

to fermentation by bacteria in the presence of glucose . As with renal and perinephric abscess, this condition is almost exclusively seen in diabetics and non-diabetics who have a coexisting obstruction or are immunosuppressed. It is twice as common in women and is characteristically unilateral. Causative organisms are E. Coli, Klebsiella, Proteus Mirabilis and Pseudomonas

9, 10

.

US findings are nonspecific, and the only finding may be low-level echoes and dirty shadowing in the 11

renal parenchyma and collecting system corresponding with foci of air . CT again is the study of choice as it has the best sensitivity and specificity, and allows for evaluation of the extent of disease, which is 6

important for treatment options . The mainstay of treatment is emergent nephrectomy, however CT guided drainage may be attempted in cases of focal involvement or in solitary kidneys

3, 4

.

CT findings classify emphysematous pyelonephritis in two types: Type 1 consists of intraparenchymal gas and necrosis but no fluid collections. This is the more severe form with mortality rate of 69-80 %. Type 2 is less common and is characterized by a lower mortality rate (18-20%), less parenchymal necrosis, and the presence of renal/perinephric collections (Figure 4). The 9

presence of fluid collections is associated with a favorable immune response . If there is a gas-forming infection limited to the collecting system, it is called emphysematous pyelitis (Figure 5). Differentiation is crucial as this presentation is less aggressive and has lower

7 12

mortality than emphysematous pyelonephritis. A necrotizing infection should always be suspected in the absence of prior instrumentation or fistula formation.

Pyonephrosis 3

Pyonephrosis is defined as pus in an obstructed collecting system . The most common causes of obstructive uropathy include calculus, stricture, tumor, congenital anomaly and rarely, retroperitoneal fibrosis. The obstruction may predispose to and precede the infection, however, the opposite can also 4

occur . Similar to emphysematous pyelonephritis, pyonephrosis is a medical emergency as it may lead to renal parenchymal destruction, loss of function and sepsis

2,5

. Decompression and aspiration are

performed under CT, US or fluoroscopy in which a percutaneous nephrostomy is placed. On US, pyonephrosis is seen as a dilated pyelocalyceal system containing debris and fluid-fluid levels. It has been described that the presence of echogenic material in the collecting system has a 100 % positive predictive value for suspected pyonephrosis, however features on US are often the same as simple 4

hydronephrosis . Contrary to the previously discussed infections, CT has less value, and differentiation of pyonephrosis from hydronephrosis can be limited

2,4

. Frequently, both conditions present with the same

findings except for the fact that they are more severe in pyonephrosis (Figure 6). Indirect signs include thickening and hyperenhancement of the pelvic wall (sensitivity of 76 % for pyonephrosis), high density material in a dilated collecting system and parenchymal or perinephric inflammatory changes which are the less specific. Gas in the collecting system is the most accurate indicator of underlying infection in the absence of instrumentation.

Acute and Emphysematous cystitis Similar to other infections of the urinary tract, the diagnosis of cystitis is clinical. Imaging is required to evaluate for infection of unclear etiology, unusual presentation, to differentiate between upper and lower tract infection and to evaluate for complications. Often, underlying abnormalities or concomitant pathologies are detected.

8 CT findings of cystitis are vague and may be seen as a diffusely thickened bladder wall with stranding of the perivesical fat (Figure 7). If there is air in the bladder lumen or linear streaks of air dissecting the bladder wall, the diagnosis is one of emphysematous cystitis (Figure 8). Before suggesting the diagnosis, correlation with a history of recent instrumentation should be made and a vesicoenteric fistula should be excluded as both will demonstrate imaging findings mimicking emphysematous cystitis. Emphysematous cystitis is rare and, contrary to emphysematous pyelonephritis is not an emergency, however, should be treated promptly.

Chronic infections Chronic pyelonephritis There remains controversy over the pathophysiology of chronic pyelonephritis as to whether there is an active chronic infection involved. Classically, this condition corresponds to imaging findings that arise secondary to long-standing recurrent infections as well as from sequelae from a prior single infection

3, 4,7

.

Risk factors for recurrent infection include vesicoureteral reflux, nephrolithiasis, chronic obstruction, neurogenic bladder, urinary diversion and in general causes of stasis. The sequence of reflux-UTI-pyelonephritis-scarring is known as reflux nephropathy. Approximately 20% of patients with acute pyelonephritis develop focal scarring. Typical scarring in chronic pyelonephritis is seen as focal atrophy in the polar regions with calyceal distortion and dilation 6

of the collecting system . Compensatory hypertrophy of residual tissue may result in kidney deformation 4

or pseudotumor . Differentiation of an infarct from scarring involves the absence of calyceal involvement in infarction. To differentiate fetal lobulations from scar, the cortex is preserved and the depressions lie between calyces rather than overlying them. On US, scars are seen as linear hyperechoic areas perpendicular to the surface and cortical loss 4

throughout the parenchyma .

Xanthogranulomatous pyelonephritis (XGP)

9 XGP is an atypical immune response to chronic infection in the setting of long standing obstruction. Pathogens are frequently E. Coli and Proteus mirabilis. Classically, the obstruction is due to a 2

longstanding staghorn calculus . There are no specific risk factors and no specific symptoms of XGP. The literature indicates that it typically affects perimenopausal women with a history of recurrent urinary tract infections, diabetes or urinary obstruction, however, XGP has also been described in all ages and both genders

4, 9

.

The response to chronic infection consists of a chronic destructive granulomatous process that leads to progressive destruction and replacement of the renal parenchyma by lipid laden macrophages 7

(xanthoma cells) . The process typically starts from the renal pelvis with extension into the medulla, cortex, perinephric space and retroperitoneum

3,4

. Two forms are seen: a diffuse form and a localized/tumefactive

2

form, the former being more common . CT findings of the diffuse form correspond to an enlarged kidney with low attenuating rounded areas that classically surround a central staghorn calculus (bear paw sign) (Figure 9). These low density areas are not fluid but inflammatory xanthomatous infiltrate. The infiltrates can easily mimic 4

hydronephrosis as the lesions are arranged in a hydronephrotic pattern . In the absence of an obstructive calculus, the diagnosis may be difficult and up to 20% of cases are acalculous. The tumefactive form is commonly confused with a renal mass; it consists of low attenuation masses of xanthomatous content limited to a focal area. In XGP, the perirenal and pararenal spaces are typically involved and extension to adjacent structures may also occur. Diffuse XGP may be treated with complete nephrectomy and focal XGP with partial nephrectomy.

Renal tuberculosis The urinary tract is the most common site of extrapulmonary tuberculosis infection. It typically occurs secondary to hematogenous spread in which bacilli are lodged in the capillaries of the glomeruli. 3

Half of the patients with renal tuberculosis may have no radiographic pulmonary involvement at all . In immunocompetent patients, the disease remains stable for several years with only cortical granulomata

10 formation. If there is reinfection or reactivation, the organisms spread into the medulla, causing papillitis and from there extend to the collecting system. This results in extensive destruction and calcification of the entire kidney. While both kidneys are usually involved, imaging may show only unilateral involvement 4

. There are often no specific clinical symptoms, with the most common being recurrent UTI despite

appropriate treatment. Imaging findings are diverse and include focal scars, cavitary lesions and dystrophic parenchymal calcification which could be amorphous, speckled, within a mass or calcified material in a dilated collecting system. The earliest findings are similar to those of acute pyelonephritis however it also involves the collecting system. It presents with focal caliectasis demonstrating a feathery contour (moth eaten/cotton ball), that later appears as a phantom calyx. Over time, mass-like lesions called tuberculomas form. The most characteristic CT finding is uneven caliectasis due to multifocal strictures. Advanced infection shows cavitary lesions communicating with the collecting system whereas late stage kidney damage corresponds to a completely calcified kidney (putty kidney) or autonephrectomy 13

secondary to complete caseous necrosis . TB infection of the collecting system presents as wall thickening and fibrosis resulting in infundibular, pelvic or ureteral stenosis that leads to different patterns of hydronephrosis including hydrocalyx and a beaded, corkscrew, pipestem or sawtooth ureter.

7

CT imaging is also appropriate to evaluate perinephric and extrarenal extension such a psoas ‘cold abscess’ formation. US evaluation is limited. Two main forms have been described in US evaluation of renal TB, an infiltrating pattern with increased echogenicity secondary to calcifications and the second, an obstructive pattern with hydronephrosis but a small renal pelvis.

Bladder Tuberculosis 4

Tuberculous bladder infection is seen in one third of the genitourinary TB cases . It appears as a 13

contracted bladder with loss of capacity , multiple diverticula and wall thickening (Thimble bladder). Granulomas may present as filling defects and mimic carcinoma. Bladder wall calcification is rare and when seen, is most likely to correspond to schistosomiasis rather than tuberculosis. Once the diagnosis 4

of bladder TB is made, strict follow up is recommended as strictures may develop or worsen on therapy .

11

Genitourinary Schistosomiasis Genitourinary Schistosomiasis is a rare infection, with the only finding being nodular bladder wall thickening (Figure 10). In the chronic form, there is a severe granulomatous reaction secondary to the deposition of eggs in the bladder that leads to fibrosis, thickened walled and a network of dense calcifications involving the bladder and distal ureters

7,14

. Despite these findings, the bladder capacity is

relatively preserved, however, strictures may develop. Most of the findings of schistosomiasis are limited to the bladder and ureters, until a late stage of disease in which the kidneys may also be affected. Chronic schistosomiasis is considered a premalignant condition especially in an endemic region, where it accounts for 50% of bladder cancers. Although imaging findings of developing malignancy are nonspecific, any change in previous calcifications as well as nodular masses should raise concern for 14

squamous cell carcinoma .

Conclusion

Urinary tract infections are among the most common infections and constitute a significant cause of morbidity. Complicated cases need further work up and imaging provides excellent information for accurate diagnosis and treatment to prevent poor outcomes. Acute infections are most frequently related to bacterial pathogens and fungi whereas chronic infections are mostly secondary to atypical bacteria and parasites. For these conditions, imaging findings have been well described, predominantly for US and CT modalities. Appropriate radiological knowledge is a helpful resource to evaluate the broad spectrum of UTIs, guide emergent interventions in a timely fashion and prevent poor outcomes.

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14 Urinary tract infections - Captions

Figure 1. Acute pyelonephritis. A) Color Doppler US. Focal area of decreased vascularity (arrow). B) Contrast enhanced CT. Right kidney wedge-shaped area of decreased attenuation with corticomedullary differentiation loss (arrow).

15 Figure 2. Renal abscess. Contrast-enhanced CT. A) In the lower pole of the right kidney there is a welldefined low-attenuation lesion (arrow). B) There is a rounded low attenuation lesion with peripheral illdefined hypodensity in the lower pole of the right kidney suggestive of edema (arrow).

Figure 3. Perinephric abscess. Contrast-enhanced CT. A) Axial. B) Coronal. There is a rim-enhancing fluid collection adjacent to the lower pole of the left kidney in the perirenal space (arrows).

16 Figure 4. Emphysematous pyelonephritis. Non-contrast CT. There are locules of gas along the periphery of the right kidney extending into the perinephric space (arrow), and a trace amount of perinephric fluid.

Figure 5. Emphysematous pyelitis. Non-contrast CT. There are locules of gas contained in the right renal pelvis (arrow).

Figure 6. Pyonephrosis. Contrast-enhanced CT. A) Coronal. B) Axial. There is a severely dilated left

17 collecting system with gas and fluid associated with perinephric fat stranding (arrows).

Figure 7. Acute cystitis. Contrast-enhanced CT reveals diffuse bladder wall thickening with perivesical fat stranding (arrow).

Figure 8. Emphysematous cystitis. Contrast-enhanced CT. Soft tissue window. There are locules of gas contained within the bladder wall (arrow).

18

Figure 9. Xanthogranulomatous pyelonephritis. Contrast-enhanced CT. A) Central branching calculus conforming to the renal pelvis and calyces consistent with a staghorn calculus (arrow): B) Multiple peripheral low attenuation areas (Bear’s paw sign, arrow).

Figure 10. Suspected bladder schistosomiasis. Non-contrast CT. Coronal. Bone window. There is extensive bladder wall calcification (arrow). Note the Foley catheter in the bladder lumen.