320
UROLOGY, NEPHROLOGY
Zdrav Vestn | July – August 2023 | Volume 92 | https://doi.org/10.6016/ZdravVestn.3413
Copyright (c) 2023 Slovenian Medical Journal. This work is licensed under a
Creative Commons Attribution-NonCommercial 4.0 International License.
Emphysematous pyelonephritis and sepsis in a diabetic 
female patient caused by extended-spectrum beta-
lactamase-producing Escherichia coli – case report
Emfizematozni pielonefritis in sepsa pri sladkorni bolnici, povzročena z Escherichia coli 
s podaljšanim spektrom beta-laktamaze – prikaz primera
Vlatko Karanfilovski,1,2 Pavlina Dzekova Vidimliski,1,2 Olivera Gjeorgjieva Janev,3 Nikola Gjorgjievski,1,2 Svetlana 
Pavleska Kuzmanoska,1,2 Irena Rambabova-Bushljetik,1,2 Zvezdana Petronijevic,1,2 Gjulsen Selim,1,2 Biljana 
Gerasimovska1,2
Abstract
Emphysematous pyelonephritis (EPN) is a rare, severe, spontaneous gas-forming infection of renal parenchyma and its 
surrounding areas. EPN was detected in diabetic patients. A 49-year-old female with type I diabetes mellitus presented 
with severe thrombocytopenia, acute kidney injury (AKI) and was in need of haemodialysis treatment. She had impaired 
liver function tests, with active urine sediment, indicating severe upper urinary tract infection with suspected sepsis. The 
contrast enhanced CT scan of the abdomen showed multiple areas of air density in renal parenchyma and perirenal re-
gions, suggestive of left-side EPN. The blood and urine cultures reported growth of extended-spectrum beta-lactamase 
(ESBL) producing Escherichia coli. The final diagnosis of emphysematous pyelonephritis complicated with severe sepsis 
and AKI was established. The patient was managed conservatively with wide-spectrum antibiotics, fluid resuscitation, 
consistent blood sugar control, and haemodialysis treatment. Percutaneous drainage techniques (PCD) and nephrectomy 
were postponed because of the initial clinical response to the antibiotics treatment. However, the patient experienced 
sudden clinical deterioration and died only a few hours after the established diagnosis. An autopsy was not performed 
upon the patient’s family’s request. EPN should be highly suspected in poorly controlled diabetic patients with urinary 
tract infection and should be promptly recognized and aggressively treated. The patients with multiple risk factors had 
high mortality, even with timely diagnosis and combined (conservative and surgical) treatment.
1 University Clinic of Nephrology, Skopje, Republic of N. Macedonia
2 Medical Faculty Skopje, Un. Ss Cyril and Methodius, Skopje, Republic of N. Macedonia
3 University Clinic of Rheumatology, Skopje, Republic of N. Macedonia
Correspondence / Korespondenca: Vlatko Karanfilovski, e: vlatko1994@live.com
Key words: pyelonephritis; sepsis; diabetes mellitus; Escherichia coli; acute kidney injury
Ključne besede: pielonefritis; sepsa; sladkorna bolezen; Escherichia coli; akutna poškodba ledvic
Received / Prispelo: 27. 12. 2022 | Accepted / Sprejeto: 2. 4. 2023
Cite as / Citirajte kot: Karanfilovski V, Dzekova Vidimliski P, Gjeorgjieva Janev O, Gjorgjievski N, Pavleska Kuzmanoska P, Rambabova-
Bushljetik I, et al. Emphysematous pyelonephritis and sepsis in a diabetic female patient caused by extended-spectrum beta-lactamase-
producing Escherichia coli – case report . Zdrav Vestn. 2023;92(7–8):320–6. DOI: https://doi.org/10.6016/ZdravVestn.3413
eng slo element
en article-lang
10.6016/ZdravVestn.3413 doi
27.12.2022 date-received
2.4.2023 date-accepted
Urology, nephrology Urologija, nefrologija discipline
Case report Klinični primer article-type
Emphysematous pyelonephritis and sepsis in 
a diabetic female patient caused by extend-
ed-spectrum beta-lactamase-producing 
Escherichia coli – case report 
Emfizematozni pielonefritis in sepsa pri sladkorni 
bolnici, povzročena z Escherichia coli s podal-
jšanim spektrom beta-laktamaze – prikaz primera
article-title
Emphysematous pyelonephritis and sepsis in 
a diabetic female patient caused by extend-
ed-spectrum beta-lactamase-producing 
Escherichia coli
Emfizematozni pielonefritis in sepsa pri sladkorni 
bolnici, povzročena z Escherichia coli s podal-
jšanim spektrom beta-laktamaze
alt-title
pyelonephritis, sepsis, diabetes mellitus, Esch-
erichia coli, acute kidney injury
pielonefritis, sepsa, sladkorna bolezen, Escherich-
ia coli, akutna poškodba ledvic kwd-group
The authors declare that there are no conflicts 
of interest present.
Avtorji so izjavili, da ne obstajajo nobeni 
konkurenčni interesi. conflict
year volume first month last month first page last page
2023 92 7 8 320 326
name surname aff email
Vlatko Karanfilovski 1,2 vlatko1994@live.com
name surname aff
Pavlina Dzekova Vidimliski 1,2
Olivera Gjeorgjieva Janev 3
Nikola Gjorgjievski 1,2
Svetlana Pavleska Kuzmanoska 1,2
Irena Rambabova-Bushljetik 1,2
Zvezdana Petronijevic 1,2
Gjulsen Selim 1,2
Biljana Gerasimovska 1,2
eng slo aff-id
University Clinic of Nephrology, 
Skopje, Republic of N. 
Macedonia
University Clinic of Nephrology, 
Skopje, Republika Severna 
Makedonija
1
Medical Faculty Skopje, Un. Ss 
Cyril and Methodius, Skopje, 
Republic of N. Macedonia
Medical Faculty Skopje, Un. Ss 
Cyril and Methodius, Skopje, 
Republika Severna Makedonija
2
University Clinic of 
Rheumatology, Skopje, Republic 
of N. Macedonia
University Clinic of 
Rheumatology, Skopje, 
Republika Severna Makedonija
3
Slovenian Medical Journallovenian Medical Journal
321
CASE REPORT
Emphysematous pyelonephritis and sepsis in a diabetic female patient
1 Introduction
Emphysematous pyelonephritis (EPN) is a rare, 
life-threatening, acute necrotizing infection of the 
renal parenchyma and perirenal tissues caused by 
gas-forming uropathogens (1,2). Kelly H. and MacCal-
lum reported the first case of EPN in 1898. Since then, 
all the following cases have been described mostly as 
single case reports, predominantly in female patients 
with poorly controlled diabetes mellitus or obstruction 
of the urinary tract (3). Escherichia coli and Klebsiella 
pneumonia were the most common causative patho-
gens isolated in up to 90% of the reported cases (4). 
EPN was mainly unilateral, with predominant left side 
involvement (60%) (1-4). 
The symptoms of EPN were nonspecific, and more 
than 70% of cases presented with the classic triad of 
upper urinary tract infections (fever, flank pain, and 
pyuria) (1,2,4). In patients presenting with sepsis, sep-
tic shock, thrombocytopenia, altered consciousness, 
and acute kidney injury (AKI), EPN might have a ful-
minant course leading to death in 54.4% of the cases, 
despite the aggressive therapy (5,6). 
The management of patients with EPN consists of 
fluid resuscitation, antibiotics, consistent blood sug-
ar control, surgical or percutaneous drainage (PCD), 
and/or nephrectomy (3-5). There is no well-defined al-
gorithm for management and treatment (conservative 
vs. PCD vs. nephrectomy). The treatment is guided by 
individual experience, severity of clinical presentation, 
risk factors, and evolution of the clinical symptoms (4).
We report a case of left-side EPN in a diabetic fe-
male caused by ESBL-producing Escherichia coli, who 
presented with sepsis and AKI with a need for hemo-
dialysis treatment.
Izvleček
Emfizematozni pielonefritis (EPN) je redka, huda, spontana plinska okužba ledvičnega parenhima in njegove okolice. EPN 
smo odkrili pri bolnikih s sladkorno boleznijo. Pri 49-letni ženski s sladkorno boleznijo tipa I so se pojavili huda trombocito-
penija, akutna okvara ledvic (AKL) in je potrebovala hemodializno zdravljenje. Testi so pokazali oslabljeno delovanje jeter, 
z aktivnim urinskim sedimentom, kar je kazalo na hudo okužbo zgornjih sečil s sumom na sepso. Računalniška tomografija 
trebuha s kontrastom je pokazala številne zgostitve zraka v ledvičnem parenhimu in perirenalnih predelih, kar je kazalo 
na levostranski EPN. Kulture krvi in urina so pokazale rast Escherichia coli z razširjenim spektrom beta-laktamaze (ESBL). 
Končna diagnoza je bila emfizematozni pielonefritis, ki ga je spremljal zaplet s hudo sepso in AKI. Bolnico so zdravili kon-
zervativno z antibiotiki širokega spektra, tekočinskim oživljanjem, doslednim nadzorom krvnega sladkorja in hemodializo. 
Zaradi začetnega kliničnega odziva na zdravljenje z antibiotiki so bile perkutane drenažne tehnike (PCD) in nefrektomija 
odložene. Vendar je pri bolnici prišlo do nenadnega kliničnega poslabšanja in je umrla le nekaj ur po postavljeni diagnozi. 
Na željo bolničine družine obdukcija ni bila opravljena. Pri slabo nadzorovanih sladkornih bolnikih z okužbo sečil je treba 
takoj posumiti na EPN ter jo nemudoma prepoznati in agresivno zdraviti. Pri bolnikih z več dejavniki tveganja je bila umr-
ljivost kljub pravočasni diagnozi in kombiniranemu (konzervativnemu in kirurškemu) zdravljenju visoka.
2 Case presentation
A 49-year-old female was admitted to our hospital 
with high inflammatory parameters, suspected sep-
sis, severe thrombocytopenia, high fibrin degradation 
products, and acute kidney injury. The symptoms had 
started three days before admission, with high fever 
(up to 39°C), vomiting, diarrhoea, dysuria, and left 
flank pain. In the next few days, the clinical picture 
rapidly deteriorated with spontaneous bleeding from 
the mouth, dyspnoea, and oliguria. The patient had a 
medical history of poorly controlled type I diabetes 
mellitus, hypertension, coronary artery disease with 
PCI stenting (July 2022), surgically treated endometri-
al carcinoma (year 2005), and frequent cutaneous sup-
purative infections, treated with antibiotics. On phys-
ical examination, the patient was febrile (38°C), with 
heart rate of 105 beats per minute, blood pressure of 
110/65 mmHg, normal oxygen saturation, with slight 
petechial bleeding on the lower extremities, and pain 
in the left flank region on percussion.
The laboratory investigations on admission showed 
high procalcitonin and C-reactive protein (CRP) lev-
els with anaemia, severe thrombocytopenia, and high 
fibrin degradation products but normal haemostat-
ic parameters. Urine analysis showed excess white 
blood cells (WBC) with nitrites and bacteria. The test 
for SARS-CoV-2 infection was negative. The patient 
had slightly impaired liver function tests with mixed 
hyperbilirubinaemia and high lactate dehydrogenase 
(LDH) of 1022 U/L (normal <248 U/L) (Table 1). 
Urgent abdominal ultrasound reported a slightly en-
larged left kidney with increased parenchymal echoge-
nicity and two small calculi in the left kidney with no 
hydronephrosis. The patient was diagnosed with acute 
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pyelonephritis, sepsis, and/or suspected disseminated 
intravascular coagulation (DIC). The empirical double 
parenteral antibiotic treatment with ceftriaxon and ci-
profloxacine was started immediately.
On hospital day 2, the patient was treated with ur-
gent hemodialysis due to oliguria and continuous rise 
of serum creatinine levels, with temporary clinical im-
provement. The contrast-enhanced CT scan of the ab-
domen reported an enlarged left kidney with multiple 
areas of air density in renal parenchyma and perirenal 
regions, suggestive of left-sided emphysematous pyelo-
nephritis (Figure 1). The right kidney had normal CT 
findings. The peripheral blood smear revealed predom-
inant neutrophilia (86%) with toxic granulations and 
rarely fragmented erythrocytes. After 24 hours, blood 
and urine cultures reported growth of resistant Esch-
erichia coli (ESBL positive). Coproculture for Shiga 
toxin-producing Escherichia coli was negative. Direct 
and indirect Coombs test and serological identification 
for atypical pulmonary pathogens (pneumoslide) were 
negative. The final diagnosis of emphysematous pyelo-
nephritis complicated with severe sepsis and AKI was 
established. The empirical double parenteral antibiotic 
treatment was changed to the intravenous application 
of carbapenems (meropenem 500 mg IV q8hr). A mul-
tidisciplinary team consisting of a nephrologist, an in-
fectologist, and a urologist decided on conservative pa-
tient management because of the initial good clinical 
response with decreased serum procalcitonin levels. 
However, the patient experienced sudden clinical de-
terioration with hypotension, bradycardia, respirato-
ry insufficiency, and acute neurological suffering. The 
patient died only a few hours after the diagnosis was 
set. An autopsy was not performed upon the patient’s 
family’s request.
3 Discussion
Emphysematous pyelonephritis is characterized 
by spontaneous gas-forming infection of the renal 
parenchyma and the surrounding areas (1,2). The ex-
act pathogenesis and mechanisms of gas production 
in EPN are still unknown. The majority of published 
cases emphasized the presence of high tissue glucose 
in patients with poorly controlled diabetes as an ex-
cellent microenvironment for severe infection and 
Classification On admission
2nd 
day
Referent 
values 
On 
admission
2nd 
day
Referent 
values 
White blood cells (x109/L) 5.4 11.1 4.0-9.0
Serum aspartate 
aminotransferase 
(U/L)
50 67 10-34
Lymphocytes (%) 10.9 10.5 15-50 Serum alkaline phosphatase (U/L) 81 101 36-126
Neutrophils (%) 85.6 85.6 35-80
Serum alanine 
aminotransferase 
(U/L)
18 23 10-45
Procalcitonin (ng/ml) 50.21 27 < 0.5 Total bilirubin (µmol/l) 65 111 < 20.6 
C-reactive protein mg/L 358 411 < 6 Direct bilirubin (µmol/l) 33.7 73.2 < 6.6 
Hemoglobin (g/L) 91 88 120-180 Serum glucose (mmol/l) 14.58 10.38 3.5-6.1 
Platelet count (x109/L) 25 37 150-450 Serum creatinine (µmol/l) 326 45-109 
Albumin g/L 33 34 35-50 Fibrinogen (g/L) 8.2 2.0-4.0 
Serum lactate 
dehydrogenase (U/L) 1022 1464 < 248 D-dimer (ng/ml) 6791 9273 0-500 
Serum creatine kinase (U/L) 73 419 24-173
Table 1: Laboratory analyses on admission and on the second day of the hospitalization of the patient.
323
CASE REPORT
Emphysematous pyelonephritis and sepsis in a diabetic female patient
growth of enteric gram-negative bacteria (E. Coli, Pro-
teus mirabilis, Klebsiella pneumoniae) and fungi (Can-
dida albicans) (7). The mentioned microorganisms 
obtain energy through the fermentation of glucose 
via the glycolytic pathway. The overgrowth of micro-
organisms leads to glucose metabolizing with massive 
production and accumulation of carbon dioxide and 
hydrogen in tissues, with consecutive infarction and 
further renal parenchyma damage (5,7). The presence 
of diabetic microangiopathy also impairs the clearance 
of these metabolic waste products and promotes vas-
cular thrombosis and tissue inflammation. In cases of 
urinary tract obstruction, compromised renal circu-
lation due to an increased intrapelvicalyceal pressure 
leads to poor tissue perfusion that favours the growth 
of gas-producing bacteria and failure of the antibacte-
rial therapy (7).
The clinical manifestation of EPN tends to be 
non-specific and similar to the clinical presentations 
of classic upper urinary tract infections (uncompli-
cated acute pyelonephritis). Thrombocytopenia, AKI, 
altered consciousness, sepsis, and septic shock with 
high mortality were present in cases caused by mul-
tidrug-resistant bacteria (e.g., extended-spectrum 
beta-lactamase-producing bacteria) and/or patients 
with multiple risk factors (1-7). Diabetes, female gen-
der, obstructive uropathy, and hypertension are well-
known predisposing risk factors for the development 
of EPN and were found in more than 96% of all di-
agnosed cases. Immunocompromising diseases, such 
as tuberculosis, alcohol and drug abuse, neurogenic 
bladder, and acquired immunodeficiency syndrome, 
were often present among non-diabetic EPN patients 
(2). Rarely, EPN might also be seen in patients with 
Figure 1: The contrast enhanced CT scan of the abdomen.
Image is showing enlarged left kidney with multiple areas of air density in renal parenchyma, and perirenal regions, suggestive 
for left-sided emphysematous pyelonephritis: red arrow on image A and B – axial view and image C and D – coronal view.
Image is from authors’ own archive.
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autoimmune liver cirrhosis, hepatitis B infection, and 
hepatocellular carcinoma (8).
Our patient presented with severe thrombocyto-
penia, spontaneous mouth bleeding, anaemia, acute 
kidney injury, impaired liver function tests with mixed 
hyperbilirubinaemia, high LDH, and CRP levels, and 
active urine sediment, which indicated a severe up-
per urinary tract infection with sepsis. The absence 
of fragmented erythrocytes in peripheral blood smear 
and normal haemostatic parameters excluded the dis-
seminated intravascular coagulation (DIC) diagnosis. 
A fulminant course of the upper urinary tract infec-
tion in a high-risk diabetic female accompanied with 
no response to dual empyrical antibiotic treatment 
raised the suspicion of sepsis with ESBL-producing 
Escherichia coli. The patient’s initial antibiotic therapy 
was changed to an intravenous application of carbap-
enems. ESBL-producing bacteria were responsible for 
6.3% to 37.8% of cases with acute pyelonephritis (APN) 
(9). Park et al. identified acute pyelonephritis with ES-
BL-producing bacteria as an independent prognostic 
factor for sepsis, septic shock, and poor treatment 
outcome (9). Almost one-third (31.7%) of EPN cases 
were caused by ESBL-producing bacteria (10). The ES-
BL-positive E. coli and ESBL-positive Klebsiella spp. 
were the most frequently isolated strains (22.2% and 
9.5%, respectively) (9). Highly virulent strains of ESBL 
positive E.coli, such as a special CTX-M-15-positive 
ST131 clonal group, have very high antibiotic resis-
tance and were associated with emphysematous pyelo-
nephritis with a fulminant course (10). Counterintui-
tively, no significant association of ESBL infection was 
found with the patient’s admission to the intensive care 
unit or with increased mortality (11).
Prompt radiological diagnosis is vital for patients 
with EPN as early recognition could expedite the med-
ical treatment, potentially avoiding more invasive in-
terventions, including nephrectomy. The abdominal 
ultrasound in EPN typically shows echogenic foci in 
the kidney with posterior “dirty shadowing” caused by 
a reverberation artifact from the air. However, in se-
vere cases, as in our patient, the significant amount of 
air might completely obscure the kidney and make ul-
trasound differentiation from surrounding bowel gas 
even impossible (12). Hence, CT is often necessary 
to make an accurate diagnosis of EPN. To avoid de-
lay in diagnosis, Kone et al. proposed that a CT scan 
should be performed in all diabetic patients who have 
unexplained fever and systemic symptoms (13). CT 
provided better visualization and precise assessment 
of the amount of gas, the degree of renal parenchymal 
destruction, the presence of fluid collections, focal ne-
crosis, and abscess (14). According to CT scan findings, 
Huang and Tseng et al. classified patients with EPN in-
to the following classes: Class 1: gas in the collecting 
system only; Class 2: gas in the renal parenchyma with-
out extension to the extrarenal space; Class 3A: exten-
sion of gas or abscess to the perinephric space; Class 
3B: extension of gas or abscess to the pararenal space; 
and Class 4: bilateral EPN or solitary kidney with EPN 
(14). The severity of the process increases with each 
class, with Class 4 representing the worst form of EPN. 
This classification has an important predictive value 
for patients’ outcome and is part of all prognostic scor-
ing systems.
Recently, Jain et al. proposed a prognostic scoring 
based on several adverse factors: age (>50 years), num-
ber of comorbidities (>2), leukocytosis, body mass 
index - BMI (> 30 kg/m2 or < 18 kg/m2), thrombo-
cytopenia, serum creatinine levels (> 265 µmol/l), hy-
poalbuminaemia, Huang class II or III, hyponatremia, 
and multidrug resistance (4). The patients are further 
classified into three groups: good-risk group (0-4 ad-
verse factors), intermediate-risk group (5-7 adverse 
factors), and poor-risk group (8-10 adverse factors) 
(4). Based on the mentioned prognostic scoring model 
for risk stratification of these patients, the same authors 
developed an algorithm for managing patients with 
EPN. Prompt fluid resuscitation, wide-spectrum anti-
biotics, and consistent blood sugar control are corner-
stones for effective treatment. Percutaneous drainage 
(PCD) and/or early or late nephrectomy is reserved for 
selected cases with initial conservative treatment fail-
ure (1,2,4,15). In the mentioned study, patients in the 
good-risk group were managed with antibiotics, fol-
lowed by double J (DJ) stenting in case of a document-
ed obstruction or percutaneous nephrostomy (PCN) if 
needed after stabilization. Percutaneous drainage was 
required in intermediate and poor-risk groups of pa-
tients with at least > 3 cm renal parenchymal collection 
(4). Early nephrectomy (EN) was reserved only for 
non-responders to other treatments. Treated with this 
algorithm for EPN management, patients in the good-
risk group showed no mortality, and only one patient 
needed surgical treatment. From the intermediate-risk 
group, 14 patients (66.6%) were salvaged with PCD, 
and 3 (14.2%) survived after EN, with an overall mor-
tality rate of 19%. All three patients (100%) from the 
poor-risk group have died (4).
Despite the morbidity and mortality of EPN, there 
are still conflicting reports regarding the most appro-
priate management. Over the years, the treatment of 
325
CASE REPORT
Emphysematous pyelonephritis and sepsis in a diabetic female patient
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4 Conclusion
Emphysematosus pyelonephritis should be highly 
suspected in poorly controlled diabetic patients with 
an upper urinary tract infection and should be prompt-
ly recognized and aggressively treated. ESBL-produc-
ing bacteria, especially Escherichia coli, might be the 
causative pathogen in a significant number of these 
patients. The patients should be promptly evaluated by 
CT scan and stratified according to their risk factors, 
which is a useful guideline for further management of 
these patients. Patients with multiple adverse risk fac-
tors were associated with high mortality, despite the 
timely diagnosis and combined (conservative and sur-
gical) treatment.
Conflict of interest
None declared.
Inform consent of the relative of the patient
The close relative of the patient gave informed con-
sent for the publication of her case.
Acknowledgements
To all nurses from the Intensive Care Unit at the 
University Clinic of Nephrology, Skopje, Republic of 
N. Macedonia, led by Mirjana Zdravkovska.
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