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785738 JFM Journal of Feline Medicine and SurgeryCole et al

Original Article

Journal of Feline Medicine and Surgery

Ultrasonographic findings in 1­–6


© The Author(s) 2018
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DOI: 10.1177/1098612X18785738
https://doi.org/10.1177/1098612X18785738

a retrospective study journals.sagepub.com/home/jfm


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Laura P Cole1 , Panagiotis Manits2 and Karen Humm1

Abstract
Objectives  The aims of the study were to identify the ultrasonographic findings in cats with acute kidney injury (AKI)
and to assess whether they had prognostic value.
Methods  This was a descriptive case series. A search of the computerised records of the Queen Mother Hospital
for Animals (Hatfield, UK) was performed for cats presenting with AKI between 2007 and 2016. Patients were
excluded if they had historical data consistent with chronic kidney disease. Ultrasound images were reviewed
for the presence of six renal ultrasonographic abnormalities: nephromegaly, cortical and medullary echogenicity,
pyelectasia, retroperitoneal and peritoneal fluid. Ultrasonographic findings were assessed individually and
cumulatively to give an ultrasound score out of 6. Ultrasonographic findings were assessed for association with
oligouria/anuria and survival.
Results  Forty-five cats with AKI fulfilled the inclusion criteria. In total, 6.7% (3/45) of cats had normal renal size and
architecture. The most common renal ultrasonographic findings were nephromegaly, pyelectasia and increased
renal echogenicity. The presence of retroperitoneal fluid was associated with oligouria/anuria. Total ultrasound
score (out of 6) was significantly associated with oligouria/anuria and 6 month survival.
Conclusions and relevance Ultrasonographic findings are common in cats presenting with AKI. The increasing
number of renal ultrasonographic abnormalities and the presence of retroperitoneal fluid alone is associated with
oligouria/anuria and a higher ultrasound score may suggest a poorer long-term prognosis.

Keywords: Acute kidney injury, ultrasonography, survival, uroliths

Accepted: 18 May 2018

Introduction
Acute kidney injury (AKI) is defined as an acute and renal echogenicity are suggested to be the most
abrupt decrease in renal function resulting in abnormal valuable in diagnosing and decision-making when
­
glomerular filtration rate, tubular function and urine out- managing renal disease in humans.3,4
put, and can be graded to encompass a continuum of func- Published ultrasonographic findings in dogs and cats
tional and parenchymal damage.1 The International Renal with AKI include increased renal size, increased cortical
Interest Society (IRIS) has developed guidelines for the echogenicity, the presence of perirenal fluid, medullary
diagnosis of AKI.1 These guidelines include ‘imaging find- rim sign, pyelectasia, increased echogenicity of the
ings suggestive of AKI’ as a diagnostic criterion, but there perirenal fat and abnormal echogenicity of the urine
­
is no guidance given regarding what findings are expected.
Ultrasonography is a non-invasive procedure that 1Department of Clinical Science and Services, Royal Veterinary
can be performed in the majority of unstable patients, College, Hatfield, UK
making it a useful first-line tool in the investigation of 2Dick White Referrals, Newmarket, UK

AKI. It can be used to assess renal dimensions, charac-


Corresponding author:
terise the pelvis and parenchymal echogenicity, and Laura P Cole MA, VetMB, PgCert VPS, CertAVP (ECC), MRCVS,
may have a role in identifying the causal mechanism of Royal Veterinary College, Hawkshead Lane, Hatfield AL9 7TA, UK
kidney injury.2 Information relating to renal size and Email: lcole3@rvc.ac.uk
2 Journal of Feline Medicine and Surgery

Figure 1  Pyelectasia: (a) mild, (b) moderate and (c) severe

present in the pelvis.5,6 Some of these findings have been (defined as kidney length >4.4 mm in the maximal sagit-
suggested to be associated with a particular aetiological tal view),5 cortical and medullary echogenicity (hyper-,
cause and prognosis.7–10 A recent study comparing azo- iso- or hypoechoic to the liver and spleen)5,6 and pyelec-
taemic cats with non-azotaemic cats found perirenal tasia (measured from the pelvic crest to the beginning of
fluid was the ultrasonographic finding most associated the ureter). Additional findings, including the presence
with azotaemia.11 of uroliths and the presence of a hypo- (halo sign) or
The aims of this study were to identify the ultrasono- hyperechoic (medullary rim sign) echogenicity at the
graphic findings in cats with AKI and to assess whether corticomedullary junction, were also recorded. Normal
any specific findings had a prognostic value. The hypoth- renal architecture was identified by three findings in the
eses were that most feline AKI patients would have renal sagittal view: bright central echo complex (the renal
ultrasonographic abnormalities and some findings sinus and peripelvic fat), a hypoechoic region surround-
would be associated with increased mortality. ing the pelvis (the medulla) and a peripheral zone of
intermediate echogenicity (the renal cortex).12
Materials and methods The degree of pyelectasia was evaluated as follows:
The clinical records of the Queen Mother Hospital for if  the shape of the pelvis was still triangular (⩽4 mm)
Animals (Hatfield, UK) were searched using a comput- pyelectasia was considered mild (Figure 1a), if the pelvis
erised search of feline cats with a diagnosis of AKI of was oval shaped (5–10 mm) pyelectasia was considered
between 2007 and 2016. For patients to be included in the moderate (Figure 1b) and if there was reduction in corti-
AKI group they should have satisfied the following cri- cal size (pelvis >10 mm) pyelectasia was considered
teria based on the IRIS (2013) guidelines for the diagno- severe (Figure 1c). Significant pyelectasia was defined as
sis of azotaemic AKI: creatinine ⩾141 μmol/l or above renal pelvis measurement of >4 mm.
the reference interval of the individual analyser, and one An ultrasound score out of 6 was given to each
or more of the following criteria: urine analysis compat- patient. This score was comprised of 1 point for each of
ible with AKI (glucosuria, proteinuria with an inactive the six sonongraphic findings: nephromegaly, increased
sediment or renal casts) or persistent, documented clini- cortical echogenicity, increased medullary echogenicity,
cal oliguria or anuria (<1 ml/kg/h). Clinical oligouria/ pyelectasia, the presence of retroperitoneal fluid and the
anuria was determined retrospectively based on the use presence of peritoneal fluid.
of furosemide or continuous renal replacement therapy. The need for furosemide or continuous renal replace-
Patients were excluded if they had any historical or clini- ment therapy was documented in order to classify a
cal findings or clinicopathological data consistent with patient as oligouric/anuric. The suspected aetiology of the
chronic kidney disease (chronic polyuria or polydipsia, AKI and survival to discharge were also documented.
body condition score <2/9 or the presence of a non- A Shapiro–Wilk test was used to assess the data for
regenerative anaemia). normality. For normally distributed data the mean and
Static ultrasound images were retrieved from the SD were calculated, whereas for non-normally distrib-
Picture Archiving and Communication System (PACS) uted data the median and range were calculated.
server (Osirix) and were reviewed in a randomised man- Descriptive statistics on the population of cats was per-
ner by a board-certified radiologist blinded to the patient formed using a commercial statistical application (SPSS
diagnosis. Ultrasound images of the kidneys were Stasitics, Version 22.0; IBM). Binary univariable and
assessed for the following parameters: nephromegaly multivariable logistic regression analysis was used to
­
Cole et al 3

Figure 2  Ultrasonographic findings in cats with acute kidney injury. (a) Nephrolith, (b) increased cortical and medullary
echogenicity and (c) retroperitoneal fluid

evaluate associations between ultrasonographic findings (3/26) of cats; the median pelvic dimension was 2.5 mm
and survival, and presence of oligouria/anuria. (range 0.5–15 mm). Pyelectasia was considered mild in
Independent ultrasound variables included in the logis- 79.6% of cases (39/49), moderate in 12.2% of cases (6/49)
tic regression analysis were nephromegaly, increased cor- and severe in 8.16% of cases (4/49). All cats had received
tical echogenicity, increased medullary echogenicity, intravenous fluid therapy prior to ultrasound. Of the 26
pyelectasia, presence of retroperitoneal fluid and the cats with pyelectasia 26.9% (7/26) of cats were docu-
presence of peritoneal fluid. Univariable logistic regres- mented to have uroliths, of which 3/7 had ureteroliths
sion was used to evaluate the association between ultra- only, 2/7 had both ureteroliths and nephroliths, and 2/7
sound score and survival to discharge, survival at 6 had only nephroliths (Figure 2a). In total, 75% (3/4) of
months and the presence of oligouria/anuria. P values patients with severe pyelectasia were documented to
were computed for each predictor in each regression have ureteroliths. Overall, the presence of uroliths in
analysis, alongside an odds ratio (OR) and 95% confi- AKI cats was 15.6% (7/45). Increased cortical and med-
dence intervals (CIs). A P value of <0.05 was considered ullary echogenicity was documented in 40% (18/45) and
significant. 51.1% (23/45) of cats, respectively. All cats with increased
cortical echogenicity had increased medullary echo-
Results genicity (Figure 2b). A halo sign was detected in single
Forty-five cats with AKI fulfilled the inclusion criteria. cat. In total, 33.3% (15/45) of the cats had retroperitoneal
The median age of the cats was 42 months (range 2–154 fluid (Figure 2c) and 46.7% (21/45) of the cats had peri-
months). There were 29 domestic shorthair cats, four toneal fluid. The total ultrasound score ranged from 0–6.
domestic longhairs and 12 pedigrees. Twenty-two cats Nephromegaly was identified in 100% (2/2) of cases
were male neutered, 19 female neutered and four were of lily toxicity, 75% (3/4) of cases of ethylene glycol toxic-
male entire. The median weight of the cats was 4.18 kg ity, 75% (3/4) of trauma cases, 60% (3/5) of cats with ure-
(0.9–8.2 kg, n = 42). The median creatinine of the cats teroliths and 50% (3/6) of cats with NSAID toxicity.
was 864 μmol/l (range 182–2576 μmol/l; n = 39). Cortical and medullary increased echogenicity was
The cause of AKI was identified in 29/45 cats. Based identified in 75% (3/4) of cats with ethylene glycol toxic-
on historical exposure to toxins and supporting bio- ity, and in 50% (2/4 and 1/2) of those cats with history of
chemical findings ethylene glycol toxicity was diag- trauma and lily exposure. Significant pyelectasia was
nosed in 4/45 cases, lily toxicity was reported in 2/45 seen in 100% (5/5) of cases with confirmed ureteroliths
cases and other toxins were suspected in 8/45 cases. and 75% (3/4) of trauma cases. Retroperitoneal fluid was
Furthermore, 6/45 cases had a recent history of non-­ seen in 50% (1/2) of reported lily intoxication and
steroidal anti-inflammatory drug (NSAID) administra- between 16.67% and 25% for other causes. Peritoneal
tion and 4/45 cases had a history of trauma. Identification fluid was present in 50% (2/4) of cases of ethylene glycol
of a ureterolith and ureteral obstruction on ultrasound toxicity and in 40% of cases of ureteroliths (Table 1).
was reported in 5/45 cases. Out of the 45 cats with AKI, 42.2% (19/45) survived to
Nephromegaly was present in 68.9% (31/45) of cats discharge and 35.6% (16/45) were alive at 6 months. All
with AKI and, of these, 35.5% (11/31) had unilateral patients that died were euthanased as a result of their
nephromegaly. Median renal length for all cats was 4.5 disease.
cm (range 2.7–5.4 cm). Pyelectasia was present in 57.8% Univariable and multivariable logistic regression
(26/45) of cats with AKI and this was unilateral in 11.5% showed that no single ultrasonographic finding or total
4 Journal of Feline Medicine and Surgery

Table 1  Ultrasonographic findings and cause of acute kidney injury

Non-steroidals Ethylene glycol Ureterolithiasis Trauma Lily exposure


(n = 6) (n = 4) (n = 5) (n = 4) (n = 2)

Normal renal ultrasound 1 (16.67) 1 (25) 0 (0) 0 (0) 0 (0)


Nephromegaly 3 (50) 3 (75) 3 (60) 3 (75) 2 (100)
Increased cortical echogenicity 1 (16.67) 3 (75) 1 (20) 2 (50) 1 (50)
Increased medullary echogenicity 2 (33.33) 3 (75) 2 (40) 2 (50) 1 (50)
Significant pyelectasia (>4 mm) 4 (66.6) 1 (25) 5 (100) 3 (75) 1 (50)
Retroperitoneal fluid 1 (16.67) 1 (25) 1 (20) 1 (25) 1 (50)
Peritoneal fluid 2 (33.33) 2 (50) 2 (40) 1 (25) 0 (0)

Data are n (%)

Table 2  Univariable logistic regression analysis for ultrasonographic findings associated with survival to discharge in
cats with acute kidney injury

Ultrasonographic finding P value OR 95% CI

Nephromegaly 0.48 0.63 0.177–2.255


Increased cortical echogenicity 0.33 0.54 0.156–1.855
Increased medullary echogenicity 0.11 0.37 0.107–1.237
Significant pyelectasia (>4 mm) 0.99 1.01 0.304–3.340
Retroperitoneal fluid 0.40 0.57 0.157–2.078
Peritoneal fluid 0.09 0.34 0.098–1.171

Table 3  Univariable and multivariable logistic regression analysis for ultrasonographic findings associated with the
presence of oligouria/anuria

Univariable analysis Multivariable analysis

Ultrasonographic finding P value OR 95% CI P value OR 95% CI

Nephromegaly 0.07 3.46 0.887–13.506 0.271 2.611 0.472–14.431


Increased cortical echogenicity 0.18 2.29 0.675–7.739 0.676 1.660 0.154–17.846
Increased medullary 0.30 1.88 0.575–6.136 0.716 0.641 0.058–7.026
echogenicity
Significant pyelectasia (>4 mm) 0.30 0.53 0.161–1.767 0.207 0.392 0.091–1.679
Retroperitoneal fluid 0.006 8.00 1.8–34.9 0.020 6.697 1.348–33.281
Peritoneal fluid 0.11 2.71 0.809–9.06 0.206 2.516 0.602–10.521

Data in bold are statistically significant

ultrasound score was statistically associated with the Discussion


survival to discharge (Table 2). However, there was a sta- This retrospective study illustrates that abnormalities in
tistically significant association between the total ultra- ultrasonography are common in cats with AKI. Renal and
sound score and 6 month survival time (P = 0.029, OR perirenal ultrasonographic abnormalities were reported in
0.628, 95% CI 0.415–0.953). >90% of cases and >50% of cases had at least three ultra-
There was a statistically significant association sonographic abnormalities of the recorded study parame-
between the total ultrasound score and the presence of ters, suggesting the more renal/perirenal abnormalities
oligouria/anuria (P = 0.04, OR 1.507; 95% CI 1.02–2.229) with compatible history and physical examination find-
and, when considering the individual ultrasonographic ings there are, the more likely the patient is to have AKI.
findings, there was a statistically significant association Nephromegaly is the most commonly cited abnor-
between the presence of retroperitoneal fluid and olig- mality in AKI and this study supports this, with approxi-
ouria/anuria (P = 0.006, OR 8; 95% CI 1.8–34.9) in both mately 70% of patients with AKI having nephromegaly.5
univariable and multivariable analysis (Table 3). This is similar to the reported findings in dogs with
Cole et al 5

leptospirosis and renal lymphoma; 50% (10/20) and 80% In this study the presence of retroperitoneal fluid was
(8/10), respectively.8,10 associated with the presence of oligouria/anuria. It is
The second most common ultrasound finding in unclear whether the association between retroperitoneal
our study was pyelectasia, reported in approximately fluid and oligouria/anuria is a result of fluid overload,
60% of cases. Pyelectasia is considered a non-specific or if retroperitoneal fluid indicates the severity of the
finding and should be interpreted with caution as it underlying disease. If fluid overload was the only cause
has been reported that feline patients with clinically of retroperitoneal fluid it would be expected that the
normal renal function with evidence of diuresis have presence of peritoneal fluid would also be associated
recorded pelvic diameters up to 3.4 mm.13 All patients with oligouria/anuria. Another potential mechanism of
had been referred and therefore had intravenous fluid retroperitoneal fluid production is tubular back leak fol-
administration for an unknown period of time prior to lowing increased permeability of proximal tubular
ultrasound, which may be the cause of mild pyelecta- epithelium secondary to nephrotoxins or ischaemic
­
sia seen in some of these animals. Sub-categorising damage.20 Holloway and O’Brien described 12 dogs and
pyelectasia into mild, moderate and severe, based on six cats with non-obstructive AKI and perirenal fluid,9 of
the effect of pyelectasia on the rest of the renal paren- which 15/18 had bilateral perirenal fluid and no evi-
chyma, was useful, especially when attempting to dence of peritoneal or pleural fluid suggestive of fluid
determine the underlying cause of AKI. Pyelectasia overload. The presence of retroperitoneal fluid has pre-
was present in all cases (5/5) diagnosed with uretero- viously been shown to correlate with severity of azotae-
liths and 75% (3/4) of patients with severe pyelectasia mia, supporting the theory that perirenal fluid is
were documented to have uroliths. These findings associated with severity of renal dysfunction.11 In the
suggest, alongside previous literature, that severe current study 6/15 cases with retroperitoneal fluid had
pyelectasia may be sufficient enough to support a reported toxin exposure and in another five cases the
diagnosis of ureteral obstruction.11–16 cause was unknown and therefore was a potentially
Increased renal echogenicity has been reported in a toxic cause, most of which are associated with poor
wide range of renal diseases, including glomerular and outcome.
interstitial nephritis, acute tubular necrosis, nephrocalci- No ultrasonographic abnormalities were statistically
nosis and end-stage renal disease.4 In the current study associated with survival when considered in isolation.
22/45 (48.9%) patients had increased renal echogenicity; However, when using an ultrasound scoring system
of these 77% (17/22) had both increased cortical and there was a trend towards significance with regard to
medullary echogenicity. Increases in cortical echogenic- survival to discharge and a statistically significant asso-
ity alone should be interpreted with caution as proximal ciation with higher score and lower survival at 6 months,
tubular lipidosis occurs in normal cats and has been with most cases being euthanased within weeks of dis-
shown to increase renal cortical echogenicity in other- charge. The failure to report a statistically significant
wise architecturally normal kidneys.17,18 Furthermore, finding between survival to discharge and ultrasound
renal echogenicity has been shown to poorly correlate score may be the result of a type II error. A larger study
with histopathological findings in cats with chronic renal population may have shown more significant results.
disease.19 When considering the conclusions of the study one
Increased cortical and medullary echogenicity was must be aware of the study limitations. This study was a
detected in 75% (3/4) of cases with ethylene glycol toxic- retrospective study with a small sample size. The retro-
ity. This is similar to a previous study, which reported a spective nature of the study only allowed review of static
mild-to-marked increased echogenicity in all 15 patients ultrasound images and this may have hindered image
suspected to have ethylene glycol toxicity.7 In the same interpretation. Furthermore, we only captured patients
study, 7/12 dogs and 1/3 cats had a persistence of a with azotaemic AKI, thereby reducing the sample size. It
reduced echogenicity at the corticomedullary junction, is therefore possible that results are liable to type II sta-
termed a halo sign, and this appeared to be associated tistical error, especially with regard to prognostication.
with anuria. In the current study only one cat, suspected Furthermore, the association between the ultrasono-
to have AKI secondary to trauma, was recorded as hav- graphic findings and aetiology could not be determined
ing a halo sign and this patient was not oligouric/anuric. owing to the small number of cases in which a diagnosis
The current study therefore questions the significance of was made. Finally, the study population itself was from
a ‘halo sign’ as a sole marker of renal dysfunction. This is a referral hospital. Therefore, all cases of AKI had prior
supported by other studies comparing the corticomedul- fluid therapy at the primary care practice making it dif-
lary junction echogenicity in cats with and without renal ficult to assess if the ultrasonographic findings, particu-
disease.18,19 These studies suggest that either hypo- (halo larly pyelectasia, retroperitoneal fluid and peritoneal
sign) or hyperechoic (medullary rim sign) echogenicities fluid, were due to fluid administration or as a result of
cannot be used in isolation to characterise AKI. the underlying disease process.
6 Journal of Feline Medicine and Surgery

Conclusions to ethylene glycol intoxicition: 15 cases (1984–1988). J Vet


Ultrasonographic findings are common in cats with AKI. Med Assoc 1991; 199: 492–496.
8 Forrest LJ, O’Brien RT and Tremelling MS. Sonographic
A 6-point scoring system, as used in this study, may be
renal findings in 20 dogs with leptospirosis. Vet Radiol
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