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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
RENAL DATA FROM ASIA–AFRICA  
Year : 2021  |  Volume : 32  |  Issue : 1  |  Page : 209-217
Microbiological Spectrum and Outcomes of Acute Pyelonephritis in North Indian Population


1 Department of Nephrology, Jupiter Hospital, Mumbai, Maharashtra, India
2 Department of Nephrology, Medanta– The Medicity, Gurgaon, Haryana, India

Click here for correspondence address and email

Date of Web Publication16-Jun-2021
 

   Abstract 


A wide range of causative organisms can cause acute pyelonephritis (APN). However, in recent times, these pathogens have increasingly become resistant to most of the antibiotics making treatment difficult. This was a prospective observational single-center study with a aim to study the microbiological spectrum, resistance patterns, and clinical outcome of patients with APN conducted in a private tertiary care hospital in India. All adult patients hospitalized in the department of nephrology at our institute with a diagnosis of APN from February 2016 to May 2017 were included. Patients <18 years of age, kidney-transplant recipients, and pregnant patients were excluded. Demographic details, clinical symptoms, signs, and radiological and laboratory data including urine and blood cultures of all patients were recorded. The details of treatment received and outcomes in hospital and after discharge were noted. Patients were followed up three months post discharge. Decision of antibiotic and duration of antibiotics was documented by treating nephrologists. Quantitative data were presented in terms of means and standard deviation. Student’s “t” test was used for comparison of quantitative outcome parameters. P <0.05 is considered statistically significant. SPSS software version 23.0 was used for statistical analysis. A total of 89 patients with a mean age of 50.33 ± 13.9 years, of which 61.8% were males and were studied; 82/89 had complicated pyelonephritis. The most common risk factor for APN was diabetes mellitus in 64 (72%). Most common symptom was fever in 80 (90%). A triad of fever, flank pain, and dysuria was present only in 27 (30.33%). Overall, 15 patients (16.8%) had severe pyelonephritis requiring intensive care unit admission. The most common organism isolated was Escherichia coli in 26/49 (53%), followed by Klebsiella pneumoniae in 12 (24.40%). Twenty-two (58%) isolates were extended-spectrum beta lactamase producers. Six (12.20%) were resistant to carbapenems and two (4%) were pan-resistant. All 89 were treated with intravenous antibiotics. Older patients, those with diabetes, with poor glycemic control, and with emphysematous pyelonephritis and patients in whom ESBL organisms were grown had poor outcome. Piperacillin tazobactam, aminopenicillins, cefoperazone sulbactam, and carbapenems (in severe pyelonephritis) can be considered as the empirical antibiotic of choice.

How to cite this article:
Hase AN, Bansal SB, Gadde AB, Nandwani A. Microbiological Spectrum and Outcomes of Acute Pyelonephritis in North Indian Population. Saudi J Kidney Dis Transpl 2021;32:209-17

How to cite this URL:
Hase AN, Bansal SB, Gadde AB, Nandwani A. Microbiological Spectrum and Outcomes of Acute Pyelonephritis in North Indian Population. Saudi J Kidney Dis Transpl [serial online] 2021 [cited 2021 Sep 23];32:209-17. Available from: https://www.sjkdt.org/text.asp?2021/32/1/209/318526



   Introduction Top


Acute pyelonephritis (APN) is an infection of renal pelvis and parenchyma, an entity described and studied since ancient Egypt underlining its clinical significance.[1] A wide range of causative organisms can cause APN, mostly Gram-negative bacilli, Escherichia coli being the most prevalent type accounting for 75%–90% of all.[2] These infections are treated with a variety of antibiotics, including fluoro-quinolones, β-lactams, β-lactam plus β-lactamase inhibitor, and carbapenems.[3] However, in recent times, these pathogens have increasingly become resistant to most of these antibiotics due to emergence of organisms producing extended-spectrum β-lactamase (ESBL), which is an enzyme produced by Gram-negative bacilli responsible for the increasing resistances worldwide.[4],[5],[6] More alarming are the recent reports of bacteria carrying the ESBL carbapenemases enzyme (ESBLCARBA) (i.e., New Dehli metallo-β-lactamase: 1) making them resistant to carbapenems.[7]

As spectrum of pyelonephritis is changing and multidrug-resistant strains are emerging in healthcare facilities as well as the community, the empirical treatment with antibiotics has become difficult.[8] There also seems to be a discrepancy between geographical regional resistances and susceptibilities of ESBL organisms.[9] Keeping this background in mind, we planned this study to evaluate clinical presentation, microbiological spectrum, prognostic factors, and outcome of APN in the North Indian population.


   Subjects and Methods Top


It was a prospective observational single-center study in a private tertiary care hospital in India. All adult patients hospitalized in the department of nephrology at our institute with a diagnosis of APN from February 2016 to May 2017 were included. Patients <18 years of age, kidney-transplant recipients, and pregnant patients were excluded.

Demographic details, clinical symptoms, signs, radiological and laboratory data including urine and blood cultures of all patients were recorded. The details of treatment received and outcomes in hospital and after discharge were noted. Patients were followed up three months post discharge. Decision of antibiotic and duration of antibiotics were documented by treating nephrologists.

Diagnostic criteria for acute pyelonephritis

APN was defined as by Infectious Disease Society of America/CDC criteria[10],[11] (i.e., at least one of the symptoms of fever >38°C, urgency, frequency, dysuria, or suprapubic tenderness, costovertebral tenderness).

Along with one of the following:

  1. A positive dipstick for leukocyte esterase or nitrate or >10 white blood cells on a high-power microscopy field and quantitative urine culture with bacterial growth of >105 CFU/mL or 103-4 CFU/mL in symptomatic patient
  2. Organisms cultured from blood/urine
  3. Imaging test evidence of infection [e.g., ultrasound, CT scan, magnetic resonance imaging (MRI), or radiolabel scan (gallium, technetium)].


Complicated acute pyelonephritis

Defined as pyelonephritis associated with a pre-existing condition, such as structural or functional abnormalities of the genitourinary tract or the presence of an underlying disease, which increases the risks of acquiring an infection or of failing therapy. We included the following conditions for defining complicated pyelonephritis: presence of systemic predisposing factors (any factor affecting the immune response, including diabetes, collagen diseases, chemotherapy, HIV positivity, neuro-muscular diseases) and/or anatomical predisposing factors (any factors causing obstruction, including active stone disease, prostatic hypertrophy, kidney malformations, polycystic kidney disease, and indwelling catheters).

Bacterial isolates from urine and blood culture were identified by biochemical profiling using VITEK-2 System. The ESBL test was done using VITEK-2ESBL test.


   Statistical Method Top


Quantitative data were presented in terms of means and standard deviation. Qualitative/ categorical data were presented as absolute numbers and proportions. Student’s t-test was used for comparison of quantitative outcome parameters. P <0.05 is considered statistically significant. IBM SPSS Statistics version 23.0 (IBM Corp., Armonk, NY, USA) was used for statistical analysis.


   Results Top


A total of 89 patients with APN were included in the study. Mean age of the study population was 50.33 ± 13.9 years, majority being from 51 to 60 years of age. APN was more common in males (n = 55, 61.8%).

Out of the 89 APN cases, 82 had complicated pyelonephritis, whereas seven had uncomplicated APN. The most common risk factor was diabetes mellitus in 64 (72%) followed by history of recurrent urinary tract infection (UTI) in 33 (37.07%), renal calculus in 22 (24.71%), and obstructive uropathy in 12 (13.40%). History of previous urological interventions was present in five (5.61%) and four (4.4%) patients were on immunosuppressive drugs.

Thirty-seven patients (42%) had normal renal function before this infection episode, 43 (48.31%) had chronic kidney disease (CKD), and two (2.24%) were on maintenance hemodialysis. Baseline renal functions were not available in 7/89 patients.

Most common symptom was fever in 80 (90%) followed by lower urinary tract symptoms such as dysuria, frequency, urgency, and suprapubic pain in 68 (76.4%), and flank pain/renal angle tenderness was present in 64 (71.91%). Clinical trial of fever, flank pain, and dysuria was present only in 27 patients (30.33%). Fifteen patients (16.8%) had severe pyelonephritis requiring intensive care unit admission (due to severe infection requiring vasopressor support, unstable vitals, and thrombocytopenia).

Urinalysis revealed pyuria in 83 patients (93.23%) followed by hematuria in 54 (60.67%). Leukocyte esterase was positive in 63 (70.78%), and nitrite test was positive in 68 (76.40%). Other investigations showed that 72 (82.5%) had leukocytosis, four (4.49%) had thrombocytopenia, and 80 patients (89.8%) had anemia.

Microbiological spectrum

Urine culture was positive in 49 patients (55%). Blood culture was positive in 21% (n = 19) while both urine and blood cultures were positive in 21% (n = 19) of patients.

The most common organism isolated was E. coli 26/49 (53%) followed by Klebsiella pneumoniae in 12 (24.40%), Enterococcus in 6 (12.24%), Pseudomonas in two (4.08%), candida in two (4.08%), and Proteus in one patient (2%).

Twenty-two (58%) isolates were ESBL producers. Six (12.20%) were resistant to carbapenems and two (4%) were pan-resistant (resistant to all commonly used antibiotics).

E. coli showed high-grade resistance to commonly used antibiotics sch as co-trimoxazole (50%), quinolones (92.30%) and cephalosporin (53.84%). It was sensitive to nitrofurantoin (61.53%), aminoglycosides (84.61%), amino-penicillin (92.31%), betalactam plus beta-lactamase inhibitors (88.46%), carbapenems (92.31%), and colistin/polymyxin B (96.31%).

Microbiological susceptibility for other organisms is mentioned in [Table 1].
Table 1: Showing sensitivities of various classes of antibiotics to isolated organisms.

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ESBLs as defined were resistant to cephalosporin and had high degree of resistance to quinolones (95.45%) but showed good sensitivity to carbapenems, i.e., imipenem (95.45%), meropenem (72.72%), cefoperazone plus sulbactam (63.63%), aminoglycosides (amikacin, gentamicin) (72.72%), and fosfomycin (90.9%), colistin (90.9%), and ceftriaxone EDTA sulbactam (90.9%) [Table 1].

Radiological features

A computerized tomography (CT) scan was done in all the patients suspected to have APN. CT scan revealed bulky kidneys in 77 (86.51%), perinephric fat stranding in 75 (84.26%), and hydroureteronephrosis in 23 (25.8%) patients, of which 52% had calculi disease, 39% had bladder outlet obstruction in the form of prostatomegaly or stricture, and 8.6% had papillary necrosis. Emphysematous pyelonephritis (EPN) was reported in 14 (15.73%) patients while 5.6% had renal abscess [Table 2].
Table 2: Showing frequency of radiological findings in patients with acute pyelonephritis.

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Management

All 89 were treated with intravenous (IV) antibiotics, and 60 (67.40%) of them were treated with IV antibiotics alone. Patients with complicated APN with either obstruction or EPN or abscess (n = 29) required additional intervention. Percutaneous nephrostomy was done in nine (10.11%), and 5 (5.6%) patients required perinephric drain/abscess drain. DJ stenting was done in 12 (13.48%) and three patients (3.3%) required nephrectomy.

Outcomes

Of 89 patients, 68 (76.4%) had worsening of renal function of which 21 (23.5%) had recovery to baseline function by the end of three months, while 11 (12.35%) patients (CKD 4–5 at baseline) became dialysis dependent after this episode of APN. Relapse was observed in two patients, four patients were lost to follow-up, three required nephrectomy, and two died.

Patients who either expired or underwent nephrectomy or had deterioration of renal function requiring dialysis were classified as poor outcome. Older patients, those with diabetes, with poor glycemic control, and with EPN, and patients who grew ESBL organisms had poor outcome and they were statistically significant [Table 3].
Table 3: Parameters favori ng good or poor outcomes.

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Experience with spectrum β-lactamase organisms

Out of the culture positive, 22 were ESBL positive and 16 (42.10%) were non-ESBL. On comparing various parameters of these groups, it was found that patients with ESBL positive organisms were older, had longer hospital stay, poor glycemic control, and deterioration of renal function from baseline at presentation [Table 4].
Table 4: Various characteristics among ESBL producers and non-ESBL.

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   Discussion Top


UTIs are among the most common infections in all age groups which can have a wide presentation from simple cystitis to very severe pyelonephritis.[12],[13],[14] APN is a serious infection, and if not diagnosed, early or treated adequately can lead to severe consequences.[15]

The most common age of presentation was in the sixth decade and males were more commonly affected, which is different from common notions of uncomplicated upper and lower tract UTI.[16],[17] However, a study from India in patients with diabetes and APN had shown predominantly older population with male preponderance as seen in our study.[18]

Most common risk factor for APN in the current study was diabetes. Epidemiological studies have shown that the relative risk of UTI is almost twice higher in diabetics than nondiabetics due to their immunosuppressed state, effect of hyperglycemia on bacterial growth, and presence of complications such as cystopathy.[19],[20],[21],[22] The severity of UTI is also increased in diabetics.[21],[23] Among hospitalized patients with APN, diabetes mellitus has been shown to be the single most common predisposing cause.[24] In our study, out of 64 diabetics, 53 (82%) had AKI, 13 (15.73%) had emphysematous pyelonephritis, and 19 (29%) were ESBL producers. More than half of diabetics (38/64) had poor outcome as compared to only one patient without any apparent risk factors.

Classical triad of fever with rigors, flank pain, and dysuria was seen in 27 (30.33%) patients in our study, which was almost similar (35%) to a study by Dhamotharan et al.[25] The most sensitive modality of diagnosis was CT scan, which was confirmatory in 90% of patients; however, these changes are nonspecific and confirmatory mainly in patients who have one or more of the other symptoms/signs of APN. CT scan also gives other important information which helps in managing these patients since 14 patients showed emphysematous changes on CT requiring invasive procedures, such as percutaneous nephrostomy (PCN) in addition to antibiotics. The reported sensitivity of plain X-ray of kidney, ureter, and bladder, ultra-sound, and CT scan for picking up EPN is 65%, 69%, and 100%, respectively.[26] The most specific test for diagnosis of APN is via cultures as isolation of organism confirms the diagnosis and provides sensitivity pattern of antibiotics.[27] However, in our study, urine culture was positive in only in 55% of patients and blood culture in 21% of cases which is less as compared to others.[28],[29] This could be possible due to many of these patients (85.3%, 76 of 89) already receiving antibiotics, mostly quinolones (46%) and first- and second-generation cephalosporins (44.7%) and few receiving carbapenems (9.2%).

In our study, leukocyte esterase test was positive in 70.78% and nitrite test was positive in 76.40% of patients. Bedside diagnosis of UTI can be made with dipstick with leukocyte esterase and nitrite. Various studies had reported their sensitivity and specificity varying from 50% to 80%.[3] Leukocytosis was present in 82.5%. Four patients (4.49%) had thrombocytopenia. Patients with thrombo-cytopenia also had shock and multiorgan dysfunction, and two died (2.20%). Thus, thrombocytopenia in a patient with APN is a marker of poor prognosis.

In our study, E. coli was the most common pathogen in patients followed by Klebsiella. Similar observations have been made by many other studies from India and other parts of world.[17],[18],[29],[30] In the current study, 58% of all organisms were ESBL producers. ESBLs are variants of beta-lactamases that confer resistance to the extended-spectrum cephalosporin antibiotics such as cefotaxime, monobactams, and aztreonam. This concomitant antimicrobial resistance is common as ESBL production coexists with resistance to several other antibiotics.[13],[31] The reason for this resistance is that ESBLs are encoded by plasmids, which also carry resistance genes for other antibiotics.[32],[33],[34] In previous studies, recent contact with the healthcare system was identified as a major risk factor for community onset ESBL organism.[24],[27],[35] however, recent studies show increasing incidence of ESBL producing organisms in community-acquired infections as well.[34],[36],[37] As per the SMART study conducted in Asia Pacific in 2007, the prevalence of ESBL production in Enterobacteriaceae was reported to be highest from India (79%),[38],[39] which renders empirical therapy difficult.

In our study, E. coli and Klebsiella showed high-grade resistance to all commonly used antibiotics such as co-trimoxazole, quinolones, and cephalosporin and were mostly sensitive to aminoglycosides [%, piperacillin tazobactum, aminopenicillin, carbapenem (92.3%) and colistin/polymixin B (%)]. ESBL producers have good sensitivity to carbapenems, imipenem (95.45%), meropenem (72.72%), cefoperazone plus sulbactam (63.63%), aminoglycosides (amikacin, gentamycin) (72.72%), and fosfomycin (90.9%). This is consistent with other studies.[40],[41],[42],[43]

Our study reiterates the escalating antimicrobial resistance in this region and the difficulty in the choice of empiric therapy. It also underlines the importance of sending appropriate cultures before antibiotic initiation to aid in better outcome. In our study, older age and diabetics with uncontrolled sugars were the risk factors for infection with ESBL organism. Hence, in these patients, carbapenems may be considered as empirical antibiotics of choice, especially in severe pyelonephritis, as these patients are more likely to have poor outcome. The use of carbapenems over noncarbapenems in this subset of patients to improve outcome is debatable.[31] A study from India of critically ill patients with pyelonephritis, however, showed a significant outcome benefit of starting carbapenems as empirical therapy.[34]

Overall, 46 patients had poor outcome in our study. Factors leading to poor outcome on univariate analysis were older age, diabetes mellitus, EPN, and ESBL producers. Buonaiuto et al in their study of 1325 patients with complicated pyelonephritis reported crude mortality of 6.5% and attributable mortality of 4.1%. The factors associated with higher mortality were age >75 years plus a state of immunosuppression, chronic renal failure, permanent bladder catheterization, systolic blood pressure less than 90 mm of Hg, presence of bacteremia, thrombocytopenia, severe sepsis, and septic shock.

There are certain limitations in this study; first, the sample size was small, and this was a single-center study; however, this study is relevant in context of our population. In addition, it was a prospective study with good follow-up and outcome data of patients. This study reveals the prevalence of high rates of antibiotics resistance and its utility in suggesting empirical therapy in patients presenting with APN, especially in North India. The current study highlights that the resistance to commonly used drugs is high in this region, and some patients are resistant to all antibiotics.


   Conclusions Top


To conclude, this study shows that APN requiring hospitalization is more common in older age, diabetic males, and patients with outflow obstruction. E. coli, especially ESBL producing, was the most common organism, followed by K. pneumoniae. These patients have poor outcomes in spite of therapy. Considering the susceptibility profile, piperacillin-tazobactam, aminopenicillins, or cefoperazone sulbactam can be considered as the empirical antibiotic of choice. Carbapenems can be considered empirical therapy in patients with severe pyelonephritis with suspected ESBL organism.

Conflict of interest: None declared.



 
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Correspondence Address:
Aniket Niwrutti Hase
Department of Nephrology, Jupiter Hospital, Mumbai, Maharashtra
India
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DOI: 10.4103/1319-2442.318526

PMID: 34145133

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  [Table 1], [Table 2], [Table 3], [Table 4]



 

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    Abstract
   Introduction
   Subjects and Methods
   Statistical Method
   Results
   Discussion
   Conclusions
    References
    Article Tables
 

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