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Original Paper

Urol Int 2007;78:13–22 DOI: 10.1159/000096929

Presentation and Outcome of Emphysematous Renal Tract Disease in Patients with Diabetes Mellitus

Pinaki Dutta

a Anil Bhansali

a S.K. Singh

b K.L. Gupta

c M.H. Bhat

a

S.R. Masoodi

a Yashwant Kumar

d

Departments of a Endocrinology, b

Urology, c Nephrology and d

Pathology, Postgraduate Institute ofMedical Education and Research, Chandigarh , India

and cystitis, and 1 patient had EPN with cholecystitis, and 1 patient had EPN with pyomyositis. Only 7 (35%) patients had a history of pneumaturia. Escherichia coli was the common-est microorganism. The radiological distribution in 18 (2 had isolated cystitis) patients with EPN was: 2 patients had class 1; 1 had class 2; 2 had class 3A; 11 had class 3B, and 2 had class 4. Of 20 patients 11 (55%) survived. However, those patients who died had severe EPN based on radiological class (6 had class 3B and 1 had class 4). There was no significant differ-ence between the survivor and non-survivor groups with re-spect to age, gender, duration of diabetes mellitus, duration of symptoms, serum creatinine level, total leukocyte count, hemoglobin, platelet count and culture positivity. Conclu-sion: Computerized tomographic class 3B or 4 is the most reliable predictor of outcome in patients with ERTD.

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Introduction

Emphysematous renal tract disease (ERTD) has been defined as a necrotizing infection of the renal parenchy-ma and its surrounding areas resulting in gas collection in the renal parenchyma, collecting system, perinephric tissue and urinary bladder [1] . ERTD occurs exclusively (90%) in patents with diabetes mellitus (DM), but occa-sionally in patients with obstructive uropathy, polycystic kidney disease, end-stage renal disease and on immuno-

Key Words Renal tract disease, emphysematous � Diabetes mellitus � Pyelonephritis � Cystitis � Cholecystitis � Pyomyositis � Escherichia coli

Abstract Background: Emphysematous renal tract disease (ERTD) is a rare necrotizing infection of the renal parenchyma and uri-nary tract caused by gas-producing organisms. ERTD de-serves special attention because of its life-threatening po-tential. Objectives: To study the clinical features, radiological classification and prognostic factors of ERTD; and to com-pare the modalities of management and the outcome among the various radiological classes of ERTD. Patients and Meth-ods: Twenty consecutive patients with diabetes and ERTD, seen over last 3 years in a tertiary care institute of north India, were included in the study. All patients were subjected to computerized tomography (CT) after initial diagnosis by ul-trasonography. They were classified into 5 classes as previ-ously described. All patients included in the study were con-servatively managed with appropriate antibiotics and/or percutaneous drainage or surgery if required. Result: Mean age ( 8 SD) of these subjects was 54.4 8 20.6 years; duration of diabetes mellitus 8.6 8 5.8 years, and duration of symp-toms related with ERTD ranged from 3 days to 3 months. Two patients had isolated emphysematous cystitis, 13 patients had emphysematous pyelonephritis (EPN), 3 had both EPN

Internationalis

Urologia

Dr. Anil BhansaliDepartment of EndocrinologyPostgraduate Institute of Medical Education and Research, Chandigarh 160012 (India)Tel. +91 172 274 7585 600/ext. 6583, Fax +91 172 274 4401E-Mail anilbhansali_endocrine@rediffmail.com

© 2007 S. Karger AG, Basel0042–1138/07/0781–0013$23.50/0

Accessible online at:www.karger.com/uin

Dutta /Bhansali /Singh /Gupta /Bhat /Masoodi /Kumar

Urol Int 2007;78:13–2214

suppression in the absence of DM [2, 3] . It is usually re-garded as a rare infection with mortality ranging from 7 to 75% in various studies [1, 4, 5] . With the widespread availability of abdominal ultrasonography and computed tomography more cases of ERTD are being recognized. ERTD deserves special attention because of its life-threat-ening complications. Except for two studies there is a lack of large clinical experience concerned with modes of treatments and prognostications. Various previous small studies concluded that appropriate medical treatment along with early nephrectomy should be attempted in all cases of emphysematous pyelonephritis (EPN) [3, 6] . Suc-cessful treatment of EPN using percutaneous catheter drainage and appropriate antibiotic therapy is gaining fa-vor [5, 7–12] . However, the prognostic factors still remain uncertain.

We describe the clinical profile, management strate-gies and outcome in 20 patients with ERTD and compare the prognostic factors between survivors and non-survi-vors.

Patients and Methods

Twenty consecutive patients (13 women and 7 men) with DM and ERTD, seen in the endocrinology department of a tertiary care institute in north India between February 2003 and June 2005, were prospectively studied. They met the imaging criteria of gas collection in the renal parenchyma, collecting system, peri-nephric spaces and/or urinary bladder without any fistulous com-

munication between the urinary tract and the intestine or any other iatrogenic causes. All of them had symptoms and signs of upper urinary tract infection, pyuria and/or positive urine culture without any identifiable infectious focus elsewhere.

The baseline characteristics, clinical features and laboratory data at the initial presentation, management, and outcome were noted. The baseline characteristics included age, gender, duration of DM, duration of symptoms before presenting to our hospital; diabetes-related complications, history of alcohol, smoking or any other diseases. The clinical features at diagnosis included fever, flank pain, pyuria, hematuria, pneumaturia, shock and altered sensorium. Laboratory parameters included spot blood glucose, serum creatinine at diagnosis and, at last follow-up, complete he-mogram, complete urinalysis, 24-hour urinary protein, urine, blood and/or culture of drainage material from the renal tract. At least two blood cultures were taken more than 6 h apart in all pa-tients. Leukocytosis was defined as a count of 1 11,500 mm 3 , thrombocytopenia as a platelet count of ! 1.5 ! 10 9 /l, macrohe-maturia as 1 100 RBCs/high power field. All patients underwent plain radiograph, ultrasound and CT scan of the abdomen se-quentially within 24 h of the suspected diagnosis. Once the diag-nosis of ERTD was suspected on ultrasonography, it was recon-firmed and further classifications were done accordingly by CT scan as described previously [13] : class 1, gas in the collecting sys-tem only; class 2, gas in the renal parenchyma without extension to the extrarenal space; class 3A, extension of gas or abscess to the perinephric spaces; class 3B, extension of gas or abscess to the pararenal space; class 4, bilateral ERTD or EPN in a solitary or a transplanted kidney ( fig. 1–5 ). The differences in clinical features, radiology and management between survivors and non-survivors were analyzed. The modalities of treatment included antibiotics, image-guided aspiration, percutaneous drainage (PCD) or ne-phrectomy. Unsuccessful PCD was defined as persistent or pro-gressive lesions on follow-up imaging studies with unchanged or

Fig. 1. Plain kidney ureter and bladder X-ray showing gas collec-tion in the right kidney.

Fig. 2. Kidney ureter and bladder ultrasound showing gas collec-tion in the right kidney.

Emphysematous Renal Tract Disease in Patients with Diabetes Mellitus

Urol Int 2007;78:13–22 15

Fig. 3. CECT showing emphysematous cystitis ( A ), class 2 emphysematous pyelonephritis (EPN; B ), class 3A EPN ( C ), right class 3B EPN with perinephric spread (arrow; D ), and CECT showing marked resolution as in C following percutaneous catheter drainage (arrow; E ).

Dutta /Bhansali /Singh /Gupta /Bhat /Masoodi /Kumar

Urol Int 2007;78:13–2216

deteriorated clinical and laboratory parameters. The outcome was analyzed as death or discharge. On follow-up, all surviving pa-tients were reinvestigated for obstruction. Patients with advanced ERTD (classes 3B and 4) were compared with less advanced dis-ease (only cystitis, classes 1, 2 and 3A). The pathological findings from 4 patients who underwent nephrectomy were also analyzed and compared with their radiological manifestations.

Statistical Methods Because of the skewed nature of the data, robust nonparame-

teric procedures have been used. The difference between those who died and those who were discharged was tested using the Wilcoxon rank sum and Mann-Whitney’s test for continuous variables and Fisher’s exact test for categorical variables. Stepwise logistic regression and multivariate analysis were used to identify significant prognostic factors between survivors and non-survi-vors. A p value of ! 0.05 was considered statistically significant. Data are presented as mean, standard deviation and standard error of mean (SEM).

Results

The mean ( 8 SD) age at presentation was 54.4 8 20.6 (median 50, range 42–67) years. Women outnumbered men (13: 7) and all of them had type-2 DM except 1 who had type-1 DM. Three (15%) patients had ERTD as the presenting manifestation of diabetes and 2 had diabetic ketoacidosis at presentation. Seven (35%) patients had a history of pneumaturia, 9 (45%) had urinary tract ob-struction due to stone disease, and one each had benign prostatic hyperplasia with obstruction, neurogenic blad-der, and urethral stricture. Five (25%) of the 20 patients had a history of recurrent urinary tract infection. All pa-tients had large/small fiber of neuropathy, 11 (55%) had diabetic retinopathy, 4 (20%) had coronary artery disease, and 2 suffered acute myocardial infarction during hospi-tal stay. Clinical features and laboratory data at the initial presentation are given in table 1 . The site involved was more frequent in the right (50%) than in the left kidney (30%), 2 (10%) had bilateral involvement, and 2 had cys-titis only. Pathogens were identified in 17 (85%) of the 20 patients. Escherichia coli was the most common organism isolated in 15 (88%) of 17 culture-positive cases. Proteus species, Klebsiella pneumoniae , Acinetobacter, Staphylo-coccus saphrophyticus, Pseudomonas aeruginosa and Clos-tridium perfringens were isolated along with E. coli in 5 patients. One patient grew only Proteus mirabilis and an-other Enterococcus fecalis with Candida tropicalis. Urine culture served as a clue to the type of pathogen except in 1 patient where the PCD fluid gave bacteriological proof. As most of our patients had been empirically treated else-where for fever and urinary tract infection with paren-

Fig. 4. T2WI axial MRI showing hyperintensity on the upper pole of right kidney suggestive of residual abscess (same patient as in fig. 3D).

Fig. 5. CECT showing bilateral renal involvement (class 4 EPN).

Emphysematous Renal Tract Disease in Patients with Diabetes Mellitus

Urol Int 2007;78:13–22 17

teral third-generation cephalosporins and amikacin, the initial blood cultures were sterile in 12 (60%) patients.

Prognostic Factors of Mortality and Poor Outcome The baseline characteristics, clinical features and labo-

ratory data at the initial presentation in survivors and non-survivors are given in tables 2 and 3 . No statistically sig-nificant differences were seen in the age, gender, presence of fever, flank pain, hematuria, pyuria, pneumaturia, du-ration of diabetes, microvascular complications, obstruc-tive uropathy, and mean duration from onset of symptoms to diagnosis of ERTD. Thrombocytopenia, high total leu-kocyte count, low hemoglobin, high baseline serum cre-atinine, high blood glucose at presentation, altered senso-rium and shock did not predict the adverse outcome. Elev-en patients (55%) survived, and 8 died because of overwhelming sepsis and 1 died of acute coronary syn-drome. However the survivors were younger than non-survivors (p = 0.039) and the mean duration of symptoms was greater in non-survivors (53.2 vs. 19.6 days, p = 0.370). When the median duration of symptoms was taken into consideration, there was not much difference between sur-vivors and non-survivors (21 vs. 24 days, p 1 0.05).

Table 1. Clinical features and laboratory data of patients with ERTD at presentation (n = 20)

n

Fever 18 (90%)Flank pain 16 (80%)Gross hematuria 9 (45%)Pyuria 12 (60%)Pneumaturia 7 (35%)Shock 7 (35%)Altered sensorium 13 (65%)Acute renal function impairment 20 (100%)Stone/obstructive uropathy of other causes 11 (55%)Recurrent urinary tract infection 5 (25%)Leukocytosis 17 (85%)Thrombocytopenia 8 (40%)Anemia (Hb <10 g/dl) 17 (85%)Diabetic ketoacidosis 2 (10%)ERTD as presenting feature of DM 3 (15%)Culture positivity

E. coli 15 (75%)Monomicrobial organisms 10 (50%)Polymicrobial organisms 5 (25%)Enterococcus fecalis 1 (5%)Proteus mirabilis 1 (5%)

Outcome Number Mean SD SEM p value

Age, yearsSurvivors 11 49.55 4.03 1.22 0.039Non-survivors 9 54.44 5.79 1.93

Duration of diabetes, years Survivors 11 8.95 4.75 1.43 0.908Non-survivors 9 8.63 7.42 2.47

Duration of symptoms, daysSurvivors 11 19.64 11.10 3.35 0.370Non-survivors 9 53.22 62.50 20.83

Random blood glucose, mg/dlSurvivors 11 322.55 134.69 40.61 0.668Non-survivors 9 347.44 117.22 39.07

Serum creatinin, mg/dlSurvivors 11 4.982 2.223 0.670 0.407Non-survivors 9 6.067 3.465 1.155

Total leukocyte count, n/cm3

Survivors 11 17,736.36 6,889.74 2,077.34 0.913Non-survivors 9 17,400.00 6,612.87 2,204.29

Hemoglobin, g/dlSurvivors 11 8.818 2.205 0.665 0.874Non-survivors 9 9.011 3.144 1.048

Table 2. Baseline characteristics and laboratory parameters between survivors and non-survivors

Dutta /Bhansali /Singh /Gupta /Bhat /Masoodi /Kumar

Urol Int 2007;78:13–2218

Management, Radiological Classification and Outcome The modalities of management and outcome in these

patients are summarized in tables 4 and 5 . The mortality rate of patients treated only with appropriate antibiotics was 20%. The success rate of combined treatment with PCD and antibiotics was 50%, and another 50% suc-cumbed to their illness. The success rate of nephrectomy was 66%. One patient each who was shifted from PCD to nephrectomy and PCD to open debridement due to fail-ure of the initial mode of therapy died. The mortality rate in our series was 45% (9 of 20). The distribution of differ-ent radiological classes were as follows: 2 patients had class 1 (gas confined to collecting system); 1 patient had class 2 (gas within renal parenchyma); 2 patients had

Table 3. Correlation coefficient of different variables found by multivariate analysis in patients with different classes of ERTD

Class of ERTD

Numberof patients

Ageyears

DS days

DDMyears

RBGmg/dl

SCrmg/dl

Hbg/dl

TLCn/mm3

0 2 52.5 22.5 8.2 297 3.6 9.0 15,7501 2 43 11.0 8.0 265 7.0 6.8 24,5002 1 53 30.0 12.0 362 1.7 8.2 16,8003A 2 49.5 16.5 7.0 515 1.3 9.9 11,0003B 11 52.7 34.5 8.0 337 3.1 8.5 16,3004 2 50.5 92.5 14.5 223 2.0 13.1 7,700

p value 0.388 0.876 0.901 0.389 0.874 0.448 0.917

ERTD = Emphysematous renal tract disease; DS = duration of symptoms; DDM = duration of diabetes mel-litus; SCr = serum creatinine; RBG = random blood glucose; Hb = hemoglobin; TLC = total leukocyte count.

Management Number of patients/total number of patients

success failure mortality

Antibiotics only 3/5 2/5 1/5 (20%)a

Antibiotics and PCD 5/10 5/10 5/10 (50%)Direct nephrectomy 2/3 1/3 1PCD failure–nephrectomy 1/1 0 1PCD failure–open debridement 1/1 0 1

Total 9/20

PCD = Percutaneous drainage. All patients received appropriate antibiotics even if not mentioned in the group table.

a Died at home after discharge due to an undefined cause.

Table 4. Management and outcome in patients with ERTD

Table 5. Management and outcome of different radiological classes of ERTD

Type of ERTD PCD failure Mortality

Only cystitis (n = 2) – 1 (50%)Class 1 (n = 2) 0 (0) 0 (0)Class 2 (n = 1) 0 (0) 0 (0)Class 3A (n = 2) 0 (0) 0 (0)Class 3B (n = 11) 6 (54.5%) 6 (54.5%)Class 4 (n = 2) 2 (100%) 2 (100%)

– = PCD not done.One patient underwent open drainage after PCD failure.

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Urol Int 2007;78:13–22 19

class 3A (gas and/or abscess extending to perinephric space); 11 patients had class 3B (further spread to parare-nal space), and 2 patients were grouped into class 4 ERTD (1 patient had bilateral disease and the other had involve-ment of the transplanted kidney). Seven patients had em-physematous cystitis (5 had associated pyelonephritis and 2 had isolated cystitis). Interestingly, 1 patient each had emphysematous pyomyositis involving the gluteal and thigh muscles, and cholecystitis. As a predisposing factor for EPN, 5 patients gave a history of recurrent uri-nary tract infection in the past few months and another 3 gave a history of papillary necrosis which was also doc-umented radiologically. No significant differences were noted in the different radiological classes and outcome (p = 0.339). Even after using multivariate analysis there was no statistically significant predictor of outcome in different classes of ERTD. Patients with classes 1, 2 and 3A EPN had the best prognosis and all of them survived after antibiotic treatment and PCD. Of the 11 patients with class 3B, 3 underwent nephrectomy directly and 2 survived, and 1 patient was subjected to nephrectomy af-ter PCD failure and succumbed to her illness. Of the re-maining 7 patients who were managed with PCD and an-tibiotics, 4 died. Two patients with class 4 ERTD, who were managed conservatively either due to poor surgical risk or refusal for surgery, died later ( table 5 ). The re-maining 2 patients who had only cystitis were managed with antibiotics only and 1 of them died.

Pathological Findings Four patients underwent nephrectomy and all of them

had complete histopathology reports. All 4 had class 3B ERTD and 2 of them died and 2 survived. The patholog-ical findings in all revealed thick yellowish necrotic mate-rial, blurred corticomedullary differentiation, congested medulla, patchy areas of hemorrhage, multiple abscesses, vascular thrombosis and infarcts in various combina-tions. One patient had features of chronic pyelonephritis

on histopathology with superimposed acute EPN. Empty spaces were found in 2 patients presumably caused by au-tolysis and areas of previous gas accumulation ( fig. 6, 7 ).

Discussion

Since the first description of the disease in 1898 by Kelly and MacCallum [14] , it has been given various names such as renal emphysema, pneumonephritis, EPN and ERTD. The latter is most favored because it includes gas collection in the renal parenchyma, perinephric tis-sue and collecting system. This entity occurs most often in diabetics (90%) as observed in the present study. In our study, there was a female predominance (1.9: 1) which is probably due to increased susceptibility of females to uri-nary tract infections [15] . The right kidney was involved more often in our series as opposed to the literature [1] . This is probably due to more cases of right-sided obstruc-tive uropathy in our patients. The majority of the patients had predisposing factors for ERTD as seen in the firm obstructive uropathy or recurrent urosepsis. The most common clinical manifestations in our patients were fe-ver, flank pain, pyuria and hematuria as compared to other previous reported studies [1, 2, 13, 16–19] . But these symptoms were nonspecific and not different from the classical triad of upper urinary tract infection. Pneuma-turia, which is considered as a clue to the diagnosis, was present in only 7 (35%) patients. Previous studies do not mention the frequency of this typical symptom. Our study is similar to a previous study with regard to the presence of diabetic ketoacidosis [6] .

The diagnosis of ERTD is solely radiological. Plain abdominal X-ray had a very low specificity and sensitiv-ity (33%) in a previous study [9] . However, analysis of the kidney ureter and bladder X-ray in our patients was pos-itive in 55% of the patients. Ultrasound is usually consid-ered to be less sensitive because of its inability to distin-

Modality Positiven

Negativen

Sensitivity%

Specificity%

PPV NPV

X-Ray 11 (55%) 9 (45%) 63.6 55.5 63.6 55.5USG 18 (90%) 2 (10%) 61.1 100 100 22.2CT 20 (100%) 0 (0%) 100 100 100 –

PPV = Positive predictive value; NPV = negative predictive value; USG = ultrasonog-raphy; CT = computed tomography.

Table 6. Relationship between different radiological investigations

Dutta /Bhansali /Singh /Gupta /Bhat /Masoodi /Kumar

Urol Int 2007;78:13–2220

guish necrotic gas-filled areas from the bowel gas [20] . In our study, 18 (90%) patients were diagnosed by ultra-sonography. Computerized tomography not only con-firms the diagnosis but also substantiates the extent of the disease and proper classification [7, 17–19] . It was positive in all of our patients. However, due to the pres-ence of renal failure and dehydration, contrast-enhanced CT scan is relatively contraindicated in these patients. Therefore, a diabetic patient with suspected upper uri-nary tract infection, whose fever persists after 3 days of appropriate antibiotics, should be subjected to sonogra-

phy as a screening test and CT scan to confirm the diag-nosis of ERTD.

Gram-negative bacilli of the Entero bacteriaceae group are the most common causative agents for ERTD, the commonest being E. coli (50–70%), followed by Klebsiel-la, Enterobacter, Proteus, and Pseudomonas species in previous studies [1, 2] . Fungi like C andida, Cryptococcus, and Aspergillus are infrequent causes [15] . Polymicrobial infection is seen in 14–19% of cases [1, 2, 21] . As in previ-ous reports, E. coli was also the commonest micro-organ-ism isolated in our study.

Fig. 6. Low power photomicrograph from sections of a nephrectomy specimen show-ing empty spaces (arrow) and acute in-flammatory cell infiltration in the sur-rounding areas. HE. ! 20. Inset in the right corner showing Gram-negative ba-cilli in colonies (arrow).

Fig. 7. Low power photomicrograph from sections of a nephrectomy specimen show-ing acute neutrophilic infiltration in a background of diabetic glomerulosclero-sis.

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Urol Int 2007;78:13–22 21

Prognostic Factors Previous authors have attempted to correlate the clin-

ical features and laboratory parameters to predict out-come. In most of the studies age, gender, site of infections, and initial blood glucose levels were not associated with mortality or poor outcome. Our study is concordant in this with previous studies [13, 18, 22] . Features of severe sepsis in the form of hypotension, altered sensorium, uri-nary obstruction, lag period from onset of symptoms/signs to diagnosis, serum creatinine, low hemoglobin, high leukocyte count, thrombocytopenia were not able to predict an increased mortality in our series. This is in sharp contrast to a previous study [13] . We believe that this result came about because most of our patients with urinary tract obstruction were treated with an early drainage procedure and there was a relatively small num-ber of patients in our series. Though it is expected that patients with organ dysfunction will run a rapid and ful-minant course, it was not found in our series. Many of our patients had massive proteinuria at the time of diagnosis of ERTD. When we tried to correlate this with mortality, there was significant difference between survivors and non-survivors. However, proteinuria may be exaggerated during this kind of illness as previously reported by Huang et al. [13] .

Radiological Classification, Management and Outcome We used the radiological classification used by Huang

et al. [13] as the previously described classification did not demonstrate prognostic implication, and the rela-tionship between the staging system and management outcomes has not been validated [13, 22] . At baseline there were no significant differences in the clinical fea-tures and laboratory parameters in the 4 classes of ERTD. Although there was an increased tendency towards mor-tality in class 3B and 4 ERTD as opposed to the other classes, this was not statistically significant (p = 0.339). Patients with class 1–3A ERTD had the best prognosis. There was only 1 death as opposed to 8 deaths in classes 3B and 4. But when death and survival were considered there was no difference in any of the parameters in either group.

All patients with class 1, 2 and 3A ERTD were man-aged by antibiotics and PCD, but in the class 3B group, 4 patients underwent nephrectomy and 2 of them died. In 1 patient, nephrectomy was performed immediately after the diagnosis had been confirmed, and in another after conservative management with PCD and antibiotics failed. Previously reported studies differ in management

strategies of these patients [5–7, 13, 16] . Our study dem-onstrated that PCD and antibiotics should be the modal-ity of treatment in limited ERTD, and adequate manage-ment of extensive ERTD requires early judicious nephrec-tomy with aggressive supportive measures. However, in unstable patients PCD can be tried as a bridge to nephrec-tomy. Our study showed a higher mortality and failure rate of PCD in extensive disease (class 3B and 4). Previous studies reporting the success of PCD has not used a strict CT classification to define management, and it is possible that the good outcome may be due to the inclusion of milder cases [5, 7, 9, 19] . So probably early aggressive PCD and, if failed, nephrectomy should be considered in these subjects.

Conclusion

Patients with DM having a history of underlying ob-structive uropathy and/or recurrent urinary tract infec-tion and poor response to antimicrobial therapy should be worked-up for ERTD. Rarely, it can be the presenting manifestation of diabetes. Ultrasonography is a very sen-sitive method for detecting this disease in experienced hands and CT scan-based radiological classification is a very good modality to classify the extent of the disease and to plan treatment options.

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