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Received for publication: 31.3.2011; Accepted in revised form: 30.10.2011 Nephrol Dial Transplant (2012) 27: 3488–3493 doi: 10.1093/ndt/gfr810 Advance Access publication 17 February 2012 Cristiana Rollino1, Giulietta Beltrame1, Michela Ferro1, Giacomo Quattrocchio1, Manuela Sandrone2 and Francesco Quarello1 1 Department of Nephrology and Dialysis, San Giovanni Bosco Hospital, Turin, Italy and 2Department of Radiology, San Giovanni Bosco Hospital, Turin, Italy Correspondence and offprint requests to: Cristiana Rollino; E-mail: [email protected] Abstract Background. Acute pyelonephritis (APN) is a common disease which rarely evolves into abscesses. Methods. We prospectively collected clinical, biochemical and radiological data of patients hospitalized with a diagnosis of APN from 2000 to 2008. Results. Urinary culture was positive in 64/208 patients (30.7%) and blood cultures in 39/182 cases (21.4%). Two hundred and thirteen patients were submitted to computed tomography (CT) or nuclear magnetic resonance (NMR): conﬁrmation of APN was obtained in 196 patients (92%). Among these, 46 (23.5%) had positive urine culture, 31 (15.8%) had positive blood culture and 15 (7.6%) had positive cultures of both urine and blood. In 98 patients, either urine or blood cultures were negative, but CT/NMR were positive for APN. Fifty of the 213 patients submitted to CT/NMR (23.5%) had intrarenal abscesses: only 2 were evidenced by ultrasound examination. No differences were found between patients with positive or negative CT with regards to fever, leucocytosis, C-reactive protein, pyuria, urine cultures and duration of symptoms before hospitalization. No differences were found between patients with or without abscesses with regards to these parameters and risk factors. Patients with abscesses had a longer duration of treatment and hospitalization. Conclusions. Our data suggest that in APN it is not always possible to routinely document urinary infection in a clinical setting. This ﬁnding could be explained by previous antibiotic treatment, low bacterial growth or atypical pathogens. Systematic CT or NMR is necessary to exclude evolution into abscesses, which cannot be suspected on clinical grounds or by ultrasound examination and may also develop in the absence of risk factors. Keywords: acute pyelonephritis; renal abscess; urinary tract infection Introduction Acute pyelonephritis (APN) in the USA has an incidence as high as 250 000 cases per year and requires 100 000 hospitalizations every year [1]. Women are affected ﬁve times more frequently than men but have a lower mortality (7.3 versus 16.5 death/ 1000 cases) [1]. Evolution into abscess is considered infrequent. APN develops when uropathogens, mainly Escherichia coli [2], ascend to the kidneys from faecal ﬂora; rarely, it is caused by seeding of the kidneys by bacteraemia. Risk factors include frequency of sexual intercourse, genetic predisposition, old age, urinary instrumentation, diabetes and urinary tract infections in the previous months [3]. The exact correlation between APN and vesicoureteral reﬂux (VUR) in adults is not clearly deﬁned. Diagnosis of APN is mainly clinical, but computed tomography (CT) or nuclear magnetic resonance (NMR) examination allows precise deﬁnition of the inﬂammatory areas [4, 5] and evidence of abscesses. We conducted a prospective analysis of the cases of APN hospitalized in the Nephrology Unit from January 2000 to August 2008. Materials and methods We prospectively recorded all patients hospitalized in our Nephrology Department from January 2000 to August 2008 with a diagnosis of APN © The Author 2012. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: [email protected] Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 Acute pyelonephritis in adults: a case series of 223 patients APN in adults: a case series made by the Emergency Department and based on the presence of ﬂank pain, fever and leucocytosis or elevated C-reactive protein (CRP). Spiral CT with contrast medium and/or NMR (since 2006) was performed in all patients. In patients with abscesses, a second CT was done after 30 days. Retrograde urethrocystography to search for VUR was performed in case of relapsing APN or in the presence of anatomical urinary abnormalities. Treatment consisted of ceftriaxone 2 g/day for 5 days intravenously, followed by ciproﬂoxacin 500 mg twice daily orally for 14 days, except for patients allergic to these antibiotics and in the case of resistant bacteria. When no response was observed after 72 h, treatment was modulated on the basis of antibiotic sensitivity testing. Patients with abscesses were treated with ceftriaxone 2 g daily for 30 days. Patients <18 years of age were given oral cephalosporin instead of ﬂuoroquinolones. The general practitioner was charged with the follow-up of the patients after hospitalization. Deﬁnitions Statistical analysis Values are expressed as mean ± SD. Statistical analysis was conducted with Student’s t or χ2 tests. Results We collected the records of 223 patients (202 women, 21 men, mean age 37.77 ± 17.61 years; mean age of women was 36.56 ± 0.53, of men 49.43 ± 18.60). Distribution of patients in age groups is reported in Figure 1. Clinical presentation is reported in Table 1. Leucocytosis was evident in 183 patients (82.06%); mean leucocytes of these patients were 16 960 ± 5869/ mm3. Leucocytosis normalized in 4.21 ± 3.73 days. Mean Fig. 1. Distribution of patients for decades of age. CRP was 15.65 ± 8.56 mg/dL. Pyuria was present in 147 patients (65.92%). Renal function was normal in all but 21 patients, whose serum creatinine was >1.2 mg/dL (in these patients glomerular ﬁltration rate ranged from 8 to 47 mL/min/ 1.73m2 according to Modiﬁcation of Diet in Renal Disease formula [6]). In 13 of these patients, renal failure was attributed to the multiple effects of the infection (direct and haemodynamic). In one patient, there was an important diffuse interstitial neutrophilic inﬁltration evidenced by renal biopsy; this patient transiently required dialysis. Risk factors were present in 60 patients (26.9%) (Table 2). The duration of hospitalization was 11 ± 11 days. Urine cultures were available for 208 patients: 64/208 were positive (30.7%) (E. coli 56 patients, Klebsiella pneumoniae 4 patients, Enterococcus faecalis 1 patient, Proteus mirabilis 2 patients, K.pneumoniae plus E.faecalis 1 patient). Blood cultures were positive in 39/182 cases (21.4%): E. coli 35 patients, Acinetobacter lwofﬁi 1 patient, P.mirabilis 1 patient, Streptococcus saprophyticus 1 patient and Staphylococcus hominis 1 patient. Sensitivity of E. coli to ceftriaxone was 100%, to ciproﬂoxacin 85.3% and to levoﬂoxacina 85.7%. Both urine and blood cultures were available for 171 patients (76.6%). They were both positive in 19 of these patients (11.1%). In 34/171 (19.8%), urine cultures were positive and blood cultures negative; in 20/171 (11.6%), blood cultures were positive and urine cultures negative. Concordance between blood and urine cultures was 68.42%. Renal ultrasound examination was performed in 209/ 223 patients (93.7%). It was normal in 109 cases (52.1%) and suggestive of APN in 100 cases (47.8%). In these cases, single or multiple hyperechogenic areas (51 patients), kidney enlargement (16 patients), thickening of pelvic wall (6 patients), hypoechogenic areas (20 patients), pelvic dilation (13 patients), perirenal fat involvement (5 patients) and abscesses (2 patients) were evidenced. Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 ‘Old age’ refers to people >65 years of age. Fever was considered when ear temperature was >37.5°C. Pyuria was deﬁned as >10 white blood cell (WBC)/h.p.f.; leucocytosis as >9500 WBC/mm3; urinary cultures were considered positive if >103 colony-forming units (c.f.u/mL) of bacteria were found. CT was considered diagnostic for APN if single or multiple hypodense parenchymal areas were evidenced after contrast medium infusion. In NMR, APN areas correspond to hypointense areas in T1 after gadolinium medium infusion (Gadovist—Bayer Schering Pharma). APNs were considered complicated when they occurred in pregnant women, old patients, transplanted patients, patients with diabetes, bladder catheters or urinary stones. 3489 3490 C. Rollino et al. Table 1. Characteristics of the patients Patients (N) Female/male Right/left kidney Mean age (years) Duration of symptoms before hospitalization (days) Mean ear temperature (°C) Duration of fever (days) Leucocytosis (N of patients) Mean leucocytes (/mm3) Mean CRP (mg/dL) Positive urine culture (N) Positive blood culture (N) Both urine and blood positive culture (N) Pyuria (N) Risk factors (N of patients) Presence of renal failure Days of hospitalization 223 202/21 1.5 37.77 ± 17.61 5.79 ± 11.15 39.18 ± 0.79 5.34 ± 6.85 183 (82.06%) 16 960 ± 5869 15.65 ± 8.56 64/208 (30.7%) 39/182 (21.4%) 19/171 (11.1%) 147/223 (65.92%) 60/223 (26.9%) 21/223 (9.4%) 11 ± 11 Diabetes Pregnancy Renal transplant Recent hospitalization (by 3 months) Kidney stones Vesico-ureterale reﬂux Anatomical defects (ureteral duplication, ureteropyelic junction stenosis, renal ectopia) Neurological bladder New bladder after cystectomy Prostatitis Self-catheterization Endocarditis Balanoposthitis Actinic cystitis Permanent catheter a Risk factors: number of patients. Fig. 2. Spiral CT: multiple areas of APN in the left kidney. 14 2 6 11 13 9 5 3 3 2 2 1 1 1 1 Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 Table 2. Characteristics of the patientsa CT scan was performed on 183/223 (82.06%) patients. It was normal in 12 cases (6.5%); it showed lesions suggestive for APN in 170/183 cases (92.8%), with evidence of single or multiple areas of parenchymal hypodensity (Figure 2). Concordance between CT scan and ultrasound was 49%. NMR was performed in 57 cases (47 positive and 10 negative). Among the 170 patients with positive CT, 26 were also evaluated with NMR, which resulted positive in 21 and negative in 5. In one case, NMR showed an abscess which had not been documented by CT. Thirty patients were submitted to NMR only: this examination documented APN in 25 patients. In total, 213 patients were submitted for CT and/or NMR (95.5%). A radiological conﬁrmation of APN by CT and/or NMR was obtained in 196/223 (87.9%) patients with symptoms typical for APN. Among these patients, only 46 (23.5%) had positive urine culture, 31 (15.3%) had positive blood culture and 15 (7.6%) had positive cultures of both urine and blood. In 98 patients, urine or blood cultures were negative, but TC/NMR was positive for APN. In the 12 patients with normal CT, blood or urine cultures were positive. No differences were found between patients with positive or negative CT or NMR with regard to body temperature at admission, leucocytosis, CRP and duration of symptoms before hospitalization (Table 3). Urine and blood cultures were positive more frequently in patients with negative CT/NMR (Table 4). Fifty of the 213 patients submitted to CT/NMR (23.5%) had single or multiple intrarenal abscesses (Figure 3). Ultrasound examination evidenced abscesses in only two patients. No differences were found between patients with or without abscesses with regards to body temperature, leucocytosis, duration of fever, duration of symptoms before hospitalization, CRP pyuria and urine cultures (Table 5). Patients with abscesses were APN in adults: a case series 3491 Table 3. Comparison between positive and negative CT/NMR patients Leucocytes (/mm3) CRP (mg/dL) Duration of symptoms before hospitalization (days) Temperature (°C) a a CT/NMR negative CT/NMR positive Signiﬁcance 18 290.59 ± 12 216.05 12.22 ± 80.6 10.63 ± 21.11 39.17 ± 0.94 15 209.19 ± 5777.37 16.09 ± 8.63 5.45 ± 10.10 39.21 ± 0.78 n.s. (P 0.06) n.s. (P 0.08) n.s. (P 0.08) n.s. (P 0.85) n.s., not signiﬁcant. Table 4. Comparison between positive and negative CT/NMR patients concerning urine and blood culturea CT/NMR positive Signiﬁcance, P 10/17 (58.8%) 8/11 (72.7%) 11/13 (84.6%) 46/183 (25.1%) 30/165 (18.1%) 59/192 (30.7%) 0.0033 0.000001 0.0001 a The data express the number of positive urine and/or blood culture out of the number of cultures obtained in the subgroups of CT/NMR negative or positive patients. Note that negative CT/NMR patients were more frequently found to have positive cultures. Fig. 3. Abscess in the right kidney at spiral CT. Table 5. Comparison between patients with and without abscessesa Positive urine culture Pyuria (presence) Leucocytosis (N/mm3) CRP (mg/dL) Temperature (°C) Days of fever Days of hospitalization Duration of symptoms before hospitalization (days) Abscess absence Abscess presence Signiﬁcance 47/149 (31.5%) 102/153 (66.6%) 14 979.67 ± 6434.85 16.06 ± 8.48 39.16 ± 0.81 5.44 ± 7.52 8.63 ± 9.67 6.23 ± 12.69 10/50 (20%) 30/48 (62.5%) 16 912.72 ± 6676.36 14.87 ± 9.09 39.38 ± 0.66 5.48 ± 4.23 16.68 ± 14.15 4.51 ± 4.16 n.s. (P 0.07) n.s. (P 0.59) n.s. (P 0.11) n.s. (P 0.4) n.s. (P 0.12) n.s. (P 0.98) P 0.000008 n.s. (P 0.35) a The data express the number of positive urine and/or blood culture out of the number of cultures obtained in the subgroups of patients with and without abscesses. n.s., not signiﬁcant. Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 Positive urine culture Positive blood culture Urine and blood positive culture CT/NMR negative 3492 hospitalized for a longer time (16.68 ± 14.15 versus 8.63 ± 9.67 days) and were treated for longer (33.06 ± 10.29 versus 19.56 ± 4.7 days) (Table 5). In the 43 patients in whom retrograde urethrocystography was performed, VUR was found in 9 patients (20.9%). Outcome Contrast medium for CT induced a transient increase in serum creatinine in the patients with renal failure; creatinine returned to previous values in all cases afterwards. VUR. Among the patients with VUR, which was thereafter corrected with endoscopic procedure, three patients presented relapses of the urinary infection. One had an evolution towards renal failure (chronic kidney disease Class IV after 5 years) and the others remained with normal renal function. Abscesses. In all the patients with abscesses, a second CT for control performed at 1 month demonstrated the disappearance of the abscesses. Discussion Our interest in APN originated from the observation of the increasing frequency of this disease and from the uncertain indications in the literature with regard to the opportunity of performing CT/NMR. Moreover, we noted that not all our patients had positive urine culture. Hence, since 2000, we prospectively collected data of patients admitted in the Nephrology Unit with a diagnosis of APN made by the Emergency Department; 95.5% of them were submitted to CT scan or NMR (since 2006, when it became available in our hospital) or both. The most signiﬁcant data resulting from our study are that only 23.5% of patients with diagnosis of APN conﬁrmed by either CT scan or NMR had positive urine culture (Table 4) and that 23.5% of the 213 patients submitted to CT/NMR had single or multiple intrarenal abscesses (Figure 3). The low frequency of positive urine culture may be explained by previous antibiotic treatment, either self-prescribed or prescribed by the general practitioner, and by the possibility that infection was conﬁned to the renal parenchyma. Moreover, atypical organisms, such as Ureaplasma urealyticum (responsible for 4.8% of APN cases [7]) and Mycoplasma hominis, which are not found unless particular culture media containing arginine and urea are used, were not searched. Also, pyuria was found in only 65.92% of our patients. Even though these data seem in contrast with the standard deﬁnition of APN, which includes bacterial growth of at least 10 000 c.f.u/mL in presence of symptoms [2, 5, 8], they reﬂect the common medical practice in a big hospital (326 beds for hospitalization) in a town of northern Italy. Twelve patients had negative CT but typical symptoms and positive urine cultures. The explanation for this could be that the inﬂammatory lesions had already improved when the patients were submitted to radiological examination or that they were so mild as to be undetectable. Another crucial point is the frequent ﬁnding of abscesses evidenced in 23.5% of cases by CT/NMR (Figure 3). Treatment of the smallest abscesses may be medical [9], but surgical drainage is needed in the case of size >5 cm [9, 10]. Longer duration of antibiotic therapy is also advised [11]. No elements allowed a clinical differentiation of patients with or without abscesses (Table 5). We think that this ﬁnding strengthens the indication to perform CT or NMR systematically in patients with APN since detection of abscesses can modify therapeutic approach. While the association between APN and VUR has been extensively studied in children [12, 13], the literature does not indicate when VUR must be searched in adults. We performed retrograde urethrocystography in the case of recurrent APN or in the presence of urinary cavities dilation or urinary tract abnormalities: we found VUR in 20.9% of patients. They were successfully treated with endoscopic procedure and only one of them had relapsing APN. In our opinion, the most signiﬁcant elements in the recent literature regarding APN are the revised guidelines for treatment [14]: in this paper, Gupta underlines the need of differentiating patients requiring hospitalization or not. Cases with less severe forms can be treated with ciproﬂoxacin for 7 days, levoﬂoxacin 750 mg once per day for 5 days or trimethoprim/sulphametoxazole for 14 days if the sensitivity is known. More severe cases should be initially treated with an intravenous regimen (a ﬂuoroquinolone, an aminoglycoside with or without ampicillin, an extended spectrum cephalosporin with or without aminoglycoside or a carbapenem). Much concern regards antibiotic resistance [14, 15], which must be monitored. In conclusion, the absence of infected urine does not rule out the diagnosis of APN in common clinical practice. Renal abscesses are frequent and may not be suspected on a clinical basis. Hence, it seems advisable to systematically perform CT or NMR, which have greater sensitivity than ultrasound in detecting them. Conﬂict of interest statement. None declared. (See related article by Abraham et al. Diagnosis of acute pyelonephritis with recent trends in management. Nephrol Dial Transplant 2012; 27: 3391–3394.) References 1. Ramakrishanan K, Schedi DC. Diagnosis and management of acute pyelonephritis in adults. Am Fam Physician 2005; 71: 933–942. Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 The cure rate was 100%. Recurrences. Thirty-six patients had relapses. In four cases, multiple episodes were observed. The time elapsed from the ﬁrst episode to the ﬁrst recurrence ranged from 2 months to 12 years. Renal function. The 21 patients with renal failure were older than the others of this series (median was 64 years). Among them, 13 had a complete recovery of renal function, 1 remained stable, 1 improved but did not normalize (the patients who had required dialysis) and 1 progressed to end-stage renal disease. The remaining patients were lost to follow-up. C. Rollino et al. Markers of aVSMC phenotype 10. Meyrier A, Calderwood SB, Baron EL. Renal and perirenal abscess. http://www.uptodate.com/contents/renal-and-perinephric-abscess (7 December 2011, date last accessed). 11. Meyrier A, Guibert J. Diagnosis and drug treatment of acute pyelonephritis. Drugs 1992; 44: 56–59. 12. Wallin L, Bajc M. Typical technetium dimercaptosuccinic acid distribution patterns in acute pyelonephritis. Acta Paediatr 1993; 82: 1061–1065. 13. Majd M, Rushton HD, Jantausch B et al. Relationship among vesicoureteral reﬂux, P-ﬁmbriated Escherichia coli, and acute pyelonephritis in children with febrile urinary tract infection. J Pediatr 1991; 119: 578–585. 14. Gupta K, Hooton TM, Naber KG et al. International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 2011; 52: e103–e120. 15. Pertel PE, Haverstock D. Risks factors for a poor outcome after therapy for acute pyelonephritis. BJU Int 2006; 98: 141–147. Received for publication: 2.5.2011; Accepted in revised form: 30.12.2011 Nephrol Dial Transplant (2012) 27: 3493–3501 doi: 10.1093/ndt/gfr811 Advance Access publication 8 February 2012 Arteriolar vascular smooth muscle cell differentiation in benign nephrosclerosis Clemens Luitpold Bockmeyer1,*, David Sebastian Kern1, *, Vinzent Forstmeier1, Svjetlana Lovric2, Friedrich Modde1, Putri Andina Agustian1, Sandra Steffens3, Ingvild Birschmann4, Jana Traeder1, Maximilian Ernst Dämmrich1, Anke Schwarz2, Hans Heinrich Kreipe1, Verena Bröcker1 and Jan Ulrich Becker1 1 Institute of Pathology, Hannover Medical School, Hannover, Germany, 2Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany, 3Clinic for Urology, Hannover Medical School, Hannover, Germany and 4Clinic for Haematology, Haemostaseology and Oncology, Hannover Medical School, Hannover, Germany Correspondence and offprint requests to: Jan Ulrich Becker; E-mail: [email protected] *Both authors contributed equally to this work. Abstract Background. Benign nephrosclerosis (bN) is the most prevalent form of hypertensive damage in kidney biopsies. It is deﬁned by early hyalinosis and later ﬁbrosis of renal arterioles. Despite its high prevalence, very little is known about the contribution of arteriolar vascular smooth muscle cells (VSMCs) to bN. We examined classical and novel candidate markers of the normal contractile and the pro-ﬁbrotic secretory phenotype of VSMCs in arterioles in bN. Methods. Sixty-three renal tissue specimens with bN and eight control specimens were examined by immunohistochemistry for the contractile markers caldesmon, alpha- smooth muscle actin (alpha-SMA), JunB, smoothelin and the secretory marker S100A4 and by double stains for caldesmon or smoothelin with S100A4. Results. Smoothelin immunostaining showed an inverse correlation with hyalinosis and ﬁbrosis scores, while S100A4 correlated with ﬁbrosis scores only. Neither caldesmon, alpha-SMA nor JunB correlated with hyalinosis or ﬁbrosis scores. Cells in the arteriolar wall were exclusively positive either for caldesmon/smoothelin or S100A4. Conclusions. This is the ﬁrst systematic analysis of VSMC differentiation in bN. The results suggest that smoothelin is the most sensitive marker for the contractile phenotype and that S100A4 could be a novel marker for the secretory © The Author 2012. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please e-mail: [email protected] Downloaded from http://ndt.oxfordjournals.org/ at University of Auckland on September 4, 2012 2. Efstathiou SF, Pefanis AV, Tsioulos DI et al. Acute pyelonephritis in adults: prediction of mortality and failure of treatment. Arch Int Med 2003; 163: 1206–1212. 3. Scholes D, Hooton TM, Roberts PL et al. Risk factors associated with acute pyelonephritis in healthy women. Ann Intern Med 2005; 142: 20–27. 4. Kawashima A, Le Roy AJ. Radiologic evaluation of patients with renal infections. Infect Dis Clin North Am 2003; 17: 433–456. 5. Majd M, Nussbaum Blask AR, Markle BM et al. Acute pyelonephritis: comparison of diagnosis with 99mTc-DMSA, SPECT, spiral CT, MR imaging, and power Doppler US in an experimental pig model. Radiology 2001; 218: 101–108. 6. Levey AS, Greene T, Kusek JW et al. A simpliﬁed equation to predict glomerular ﬁltration rate from serum creatinine. J Am Soc Nephrol 2000; 11: 155A. 7. Fraser IR, Birch D, Fairley KF et al. A prospective study of cortical scarring in acute febrile pyelonephritis in adults: clinical and bacteriological characteristics. Clin Nephrol 1995; 43: 159–164. 8. Warren JW, Abrutyn E, Hebel JR et al. Guidelines for antimicrobial treatment of uncomplicated acute bacterial cystitis and acute pyelonephritis in women. Infectious Diseases Society of America (IDSA). Clin Infect Dis 1999; 29: 745–758. 9. Siegel JF, Smith A, Moldwin R. Minimally invasive treatment of renal abscess. 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