You are on page 1of 19

241_259_Griffin_pancreas2.

qxp_FAB 03/02/2020 12:52 Page 241

Journal of Feline Medicine and Surgery (2020) 22, 241–259

CLINICAL REVIEW

FELINE ABDOMINAL
ULTRASONOGRAPHY: WHAT’S
NORMAL? WHAT’S ABNORMAL?
The pancreas
Sally Griffin

Scanning the pancreas Practical relevance:  Abdominal


ultrasound plays a vital role in the
B-mode ultrasonography is the modality of choice to image the feline diagnostic work-up of many cats
pancreas and is widely available to most practitioners. It provides presenting to general and specialist
information regarding the size, echotexture and echogenicity of the practitioners. Ultrasound examination
pancreas, while permitting concurrent evaluation of the peripancreatic of the pancreas is a vital part of the
fat and regional lymph nodes. Aspiration of the investigation into feline pancreatic disease.
The main pancreas, regional lymph nodes and suspected Clinical challenges: Despite ultrasonography
metastatic disease is also facilitated using ultra- being a commonly used modality, many
indications for sound guidance.1 Abdominal radiographs are practitioners are not comfortable performing an
ultrasonography of very insensitive in the evaluation of the pancreas. ultrasound examination or interpreting the resulting
Ultrasound is superior to radiography, particu- images. Even for the experienced ultrasonographer,
the feline pancreas larly in cats in poor body condition or those differentiating between incidental findings such as

are suspected that have an abdominal effusion, both of which nodular hyperplasia and pathological changes such
decrease serosal detail and reduce the clinician’s as neoplasia can be challenging.
pancreatitis and ability to assess the pancreas radiographically. Aim: This review, part of an occasional series on
The main indications for ultrasonography of feline abdominal ultrasonography, discusses the
pancreatic the feline pancreas are suspected pancreatitis ultrasonographic examination and appearance
neoplasia or for and pancreatic neoplasia; ultrasonography may of the normal and diseased pancreas. Aimed at
also be conducted as part of an investigation general practitioners who wish to improve their
investigation into into extrahepatic biliary obstruction.2 As men- knowledge of and confidence in feline abdominal
tioned in previous articles in this series, the ultrasound, this review is accompanied by high-
extrahepatic biliary principal disadvantage of ultrasonography is that resolution images and videos available online
obstruction. its use as a diagnostic tool is largely dependent as supplementary material.
upon clinician experience, which is very variable. Equipment: Ultrasound facilities are readily
available to most practitioners, although use
Preparation of ultrasonography as a diagnostic tool is highly
Where possible, animals waiting for an elective dependent on operator experience.
examination should be fasted for 12 h prior to Evidence base: Information provided in this article
ultrasound. Any abdominal hair in the region to is drawn from the published literature and the
be scanned should be clipped and acoustic coupling gel applied to author’s own clinical experience.
remove the air gap between the transducer surface and the skin. Sedation
is preferable wherever possible to immobilise the patient and achieve Keywords: Ultrasound; pancreatitis; neoplasia;
maximum relaxation of the abdominal wall muscles. Owing to the pancreatic; cyst; abscess
inherently small size of the feline pancreas, the use of a high frequency
(around 11–15 MHz) linear transducer is advisable to provide optimum
image resolution, thereby allowing the pancreas to be assessed in detail.
Readers are referred to the articles on the liver and normal gastroin-
testinal tract in this series (see the box on page 255) for a more detailed
discussion pertaining to patient preparation and transducer choice.

Sally Griffin
BVSc, CertAVP, DipECVDI
Radiology Department,
Willows Veterinary Centre and Referral Service,
Highlands Road, Shirley,
Solihull B90 4NH, UK
Email: sally.griffin@willows.uk.net

DOI: 10.1177/1098612X20903599
© The Author(s) 2020 JFMS CLINICAL PRACTICE 241
241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 242

R E V I E W / Feline abdominal ultrasonography – the pancreas

a b

Figure 1 Transducer positioning for the left (a) and right (b) lobes of the pancreas

Scanning technique
The pancreas can be scanned with the cat The author’s preference is to scan
in left or right lateral, dorsal or ventral
recumbency.1 The author’s preference is
the left and right pancreatic lobes
to scan the left lobe while the animal is in while the cat is in right and left lateral
right lateral recumbency and the right lobe
with the animal in left lateral recumbency recumbency, respectively.
(Figure 1).

Anatomy and ultrasonographic identification of the pancreas


The pancreas is divided into two lobes that are
united at the body of the pancreas, which is sit-
uated ventral to the portal vein. The close proxim-
ity of these two structures makes the portal vein an
excellent landmark for the identification of the
pancreatic body (Figure 2). It should be noted that Colon
the pancreatic body in the cat is much closer to the Liver
midline than in the dog, and the angle between left Stomach
and right pancreatic lobes is also much smaller.3
Recognition of adjacent landmarks is key to the
successful identification of the pancreas. The left
pancreatic lobe is sandwiched between the stom-
ach cranially and the transverse colon caudally Portal vein
(Figure 3). The tip often extends medially to the
head and body of the spleen, which acts as an
acoustic window, and the splenic vein usually runs
caudally and dorsally to the left pancreatic lobe.
The right lobe of the pancreas is located medially
or dorsomedially to the descending limb of the
duodenum (Figure 4).1 Unlike the dog, the distal
portion of the right pancreatic lobe in the cat
turns back on itself, creating a hook-like shape Figure 2 Ultrasonographic landmarks for the pancreatic body (arrows)
(Figure 4c).4 The left lobe of the pancreas is larger
(5–9 mm thickness) in the cat than the right lobe
In all ultrasound images, unless stated otherwise,
(3–6 mm thickness) and usually, therefore, more
cranial is to the left and caudal is to the right of
easily identified.5,6 This is in contrast to the dog, in
the image.
which the right lobe of the pancreas is normally
easier to locate with ultrasound.

Recognition of adjacent landmarks is key to the successful


identification of the pancreas.
Continued on page 243

242 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 243

R E V I E W / Feline abdominal ultrasonography – the pancreas

Continued from page 242


a b

Spleen

Colon

Stomach

c d

Figure 3 Ultrasound images of the normal left pancreatic lobe (arrows) in transverse (a,b) and sagittal (c,d) planes in healthy cats. In (d) the thin-walled colon
(*) is visible just caudal to the pancreas

a b

Figure 4 (a,b) Ultrasound images from two cats to show the normal
c appearance and location of the right pancreatic lobe (arrowheads). The
descending limb of the duodenum (arrow) is visible in transverse in (b).
(c) The white line indicates the margins of the distal right pancreatic lobe
where it forms a hook-like shape

In contrast to the dog,


the left pancreatic lobe is usually
more easily identified than
the right in the cat.

JFMS CLINICAL PRACTICE 243


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 244

R E V I E W / Feline abdominal ultrasonography – the pancreas

Normal appearance of the


pancreas

The feline pancreas is a well-defined organ


when imaged with a good quality ultrasound
machine and a high frequency transducer,
although it can initially appear somewhat
inconspicuous to the untrained eye. It is
isoechoic to slightly hypoechoic relative to the
surrounding fat and has a similar echogenici-
ty to the liver.1,6,7
Most dogs have two larger pancreatic ducts
into which the smaller ducts that link the
pancreatic acini drain.8 In contrast, there is
usually just one pancreatic duct in the cat,
known as the major pancreatic duct. This duct
is consistently visible on ultrasound as an
anechoic tubular structure, flanked by thin
hyperechoic walls, running within the central
Figure 5 Ultrasound image of the normal major pancreatic duct (arrows) within the left lobe of
portion of the left lobe from the tip towards the pancreas of a 6-year-old male neutered domestic longhair cat. A video showing the normal
the body (Figure 5).1,9 It can be differentiated pancreatic duct within the left lobe of the pancreas is available as supplementary material

There is usually just one pancreatic duct in the cat,


known as the major pancreatic duct, but a second minor
or accessory duct is also present in around 20% of cats.

from a blood vessel by the absence of flow


signal when interrogated with colour Doppler.
This is because flow within a pancreatic duct
is considerably slower than blood flow and, as
such, does not generate a Doppler signal.
The diameter of the major pancreatic duct
has been reported in 20 healthy cats <10 years
of age. In these cats, the mean diameter was
determined to be 0.8 ± 0.25 mm (range 0.5–1.3
mm).7 In a separate study involving a group
of cats >10 years of age, the mean diameter of
the pancreatic duct was recorded as 1.3 ± 0.4
mm (range 0.6–2.4 mm).5 Dilation of the duct
up to 2.5 mm diameter has been shown to
a occur as an incidental ageing change in older
cats with no signs of pancreatic disease
(Figure 6).5–7 A satisfactory explanation for
this phenomenon has yet to be found. One
suggested hypothesis for the same change in
humans is that widening of the pancreatic
duct with age occurs as a result of atrophy of
the pancreas.5,10

The major pancreatic duct


can be differentiated from a
blood vessel by the absence
of flow signal when interrogated
b
with colour Doppler.
Figure 6 (a) Mild dilation of the pancreatic duct (arrows) within the left pancreatic lobe of
an 11-year-old male neutered domestic shorthair cat. This was presumed to be an incidental
age-related change. (b) Note the absence of colour within the pancreatic duct when a colour
Doppler window is applied over the pancreas

244 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 245

R E V I E W / Feline abdominal ultrasonography – the pancreas

Abnormalities of the pancreas

Pancreatitis
Pancreatitis is the most commonly diagnosed
disorder of the feline exocrine pancreas14 and
yet, despite this, an underlying cause is not
identified in the majority of cases and the con-
dition is often considered to be idiopathic.15–17
Cats of all ages may be affected, with reports
in animals from 3 weeks to 20 years.16,18 While
any breed may be affected, Siamese are
thought to be over-represented.18 The left lobe
and body are usually more commonly affect-
ed by inflammation, in contrast to the situa-
tion in dogs in which the right lobe is more
commonly affected, although any portion
may be affected in either species.3
The clinical signs and results of clinico-
pathological tests in cats with pancreatitis are
often vague and non-specific, making the
diagnosis challenging.19 Furthermore, since
Figure 7 Ultrasound image of a normal duodenal papilla (arrows). A video showing the the disease can affect the pancreas multifocal-
pancreatic and common bile ducts fusing before entering the duodenal papilla is available ly, histopathology may fail to detect evidence
as supplementary material
of inflammation in biopsy specimens.15
Fortunately, the clinician’s ability to detect
Abnormalities of the pancreaticoduodenal, pancreatitis has improved over the years,
thanks to the development of a feline-specific
jejunal, hepatic and splenic lymph nodes are not pancreatic lipase assay. One potential draw-
necessarily indicative of pancreatic disease. back of this assay, however, is that it may be
less well suited to the diagnosis of mild and
chronic forms of the disease.15 Consequently,
diagnostic imaging still has an important role
The major pancreatic duct merges with the to play in the diagnosis of pancreatitis.
common bile duct at the ampulla of Vater Anticipated radiographic changes include a
immediately prior to its entry into the mass effect in the region of the pancreas, loss
duodenum at the major duodenal papilla.11 of serosal detail due to peripancreatic effusion
The major duodenal papilla is located along and the presence of dilated bowel loops due
the dorsal wall of the duodenum, approxi- to ileus.20–23 Nevertheless, in spite of these
mately 3 cm distal to the pylorus (Figure 7).12 potential abnormalities, abdominal radiogra-
In a minority of cats, the major pancreatic duct phy is neither sensitive nor specific for feline
and common bile duct open into the duode- pancreatitis. Ultrasound, on the other hand,
num separately, but immediately adjacent to provides much more comprehensive informa-
each other.13 In around 20% of cats, a second tion relating to the health of the pancreas and
minor or accessory duct is present that drains surrounding tissue, and is recommended in
into the duodenum via the minor duodenal cats with suspected pancreatitis.
papilla, which is located approximately 2 cm The sensitivity of ultrasound for the detec-
distal to the major duodenal papilla.12 tion of pancreatitis in the cat has traditionally
Lymphatic drainage from the pancreas is been regarded as relatively low, with three
supplied by the pancreaticoduodenal, jejunal, studies between 2000 and 2002 reporting
hepatic and splenic lymph nodes. Each node values of 11%, 24% and 35%.22,24,25 In 2004, a
also supplies other organs and hence abnor- further study reported a much higher sensi-
malities of these lymph nodes are not neces- tivity of 80% for cats with moderate to severe
sarily indicative of pancreatic disease. pancreatitis and 62% for those with mild

Compared with radiography, ultrasound provides much more


comprehensive information relating to the health of the pancreas and
surrounding tissue, and is recommended in cats with suspected pancreatitis.

JFMS CLINICAL PRACTICE 245


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 246

R E V I E W / Feline abdominal ultrasonography – the pancreas

Due to the link between pancreatitis and intestinal tract


and hepatic disease, the liver and gastrointestinal tract should be evaluated
ultrasonographically at the same time as the pancreas.

pancreatitis.26 Two potential explanations Acute pancreatitis


were offered by the authors for this dramatic In contrast to the situation in dogs, chronic
difference in sensitivity relative to the earlier pancreatitis has traditionally been considered
studies. The first was an inherent bias towards to be more common than acute necrotic
a diagnosis of pancreatitis such that the radi- pancreatitis in the cat, although both may be
ologist, being aware of the nature of the study, relatively under-diagnosed.3,15,23,32,33 Several
would have evaluated the pancreas more studies have, however, resulted in increased
extensively than in previous ultrasound stud- recognition of the acute form of the disease in
ies, which were of a retrospective nature. In this species.18,24,34,35 Acute pancreatitis can
these earlier studies, the pancreas was evalu- be mild, moderate or severe and affect the
ated during a routine ultrasound examination pancreas focally, or as a multifocal or diffuse
and hence was not the focus of the study. disease. When ultrasonographic abnormali-
Secondly, there have been, and continue to be, ties suggestive of acute pancreatitis are identi-
significant advances in ultrasound technology fied, they are often more subtle than those
and markedly improved radiologist skill lev- seen in the dog; furthermore, and in the light
els that are likely to contribute to greater sen- of the sensitivities discussed above,3,24 the
sitivity levels.26 Interestingly, an even higher absence of changes on ultrasound is not suffi-
sensitivity of 84% and a specificity of 75% for cient to rule out the possibility of pancreatitis.
diagnosing pancreatitis were reported in a In those cases where the ultrasonographic
much more recent study.27 However, in this appearance of the pancreas is unremarkable
study elevated serum feline pancreatic lipase but the clinical suspicion of pancreatitis
immunoreactivity (fPLI) was used as the stan- remains high, ultrasound can be repeated
dard for diagnosis of pancreatitis, which has after 2–4 days, which may allow sufficient
been shown to have only fair agreement with time for ultrasonographic changes to appear.36
ultrasonography in cats with a suspicion of The ultrasonographic features of acute
pancreatitis.28 Of the 35 cats included in the pancreatitis in cats are reasonably specific and
study, only six cats had histopathological eval- mirror those described in dogs. Typical abnor-
uation of the pancreas;27 therefore, this figure malities include enlargement of the pancreas
for sensitivity should be interpreted with cau- (which if sufficiently substantial can result in
tion. It should also be noted that all of these a mass effect), a reduction in echogenicity of
studies were conducted at university teaching pancreatic tissue (owing to necrosis and/or
hospitals and most ultrasound examinations oedema), severely irregular pancreatic mar-
would have been performed by board- gins, hyperechogenicity and hyperattenuation
certified radiologists using high-end equip- of peripancreatic mesenteric fat (due to
ment. Hence, it is reasonable to assume that saponification following the release of pancre-
sensitivity is liable to be reduced when scans atic enzymes) and localised peritoneal effu-
are performed by clinicians less experienced sion (Figure 8).20,25,27,29,35 When inflammation
in ultrasound using lower quality equipment.14 of peripancreatic fat is severe, it can become
Concurrent inflammatory bowel disease, hazy in appearance and pancreatic margins
cholangitis/cholangiohepatitis and hepatic may appear ill-defined.
lipidosis have been reported in 50–56% of cats Hyperechoic peripancreatic fat may be one
diagnosed with pancreatitis.24,26,29,30 In a study of the most sensitive indicators of pancreatitis;
of 23 cats with inflammatory bowel disease, it was identified in 68% of cats (n = 35) that
16 cats had elevated serum fPLI concentra- had concurrently elevated serum fPLI in one
tions (>6.9 μg/l).31 Therefore, due to the link study27 and was the most frequently identi-
between pancreatitis and intestinal tract and fied ultrasonographic abnormality in 55% of
hepatic disease, the liver and gastrointestinal cats with raised fPLI in another study.37
tract should be evaluated ultrasonographical- Accordingly, this would suggest that there is a
ly at the same time as the pancreas. moderate probability of cats with pancreatitis

When ultrasonographic abnormalities suggestive of acute pancreatitis are identified,


they are often more subtle than those seen in the dog. Furthermore, the absence of
changes on ultrasound is not sufficient to rule out pancreatitis.

246 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 247

R E V I E W / Feline abdominal ultrasonography – the pancreas

a b

* **

Figure 8 Acute pancreatitis. (a) Left lobe of the pancreas (transverse plane)
c of a 14-year-old female neutered Birman presenting with a 10-day history of
lethargy and inappetence, and severe weight loss over a longer period of time.
* The pancreas (arrows) is enlarged and hypoechoic and surrounded by markedly
hyperechoic peripancreatic fat. The spleen (*) is to the left of the pancreas and
the transverse colon (**) is to the right. (b) The right pancreatic lobe in the same
cat is also affected. Note the hyperechoic fat (arrowheads) adjacent to the
pancreas. The duodenum (arrow) is seen in the transverse plane to the left of
the pancreas. Videos showing the left and right pancreatic lobes in this cat are
available in the supplementary material. (c) Pancreatitis affecting the left lobe
of the pancreas (longitudinal plane) of a 4-year-old female neutered domestic
shorthair cat referred for further investigation of icterus that had developed
following a period of reduced appetite and weight loss. The pancreas is diffusely
hypoechoic and surrounded by hyperechoic fat. The anechoic tubular structure
(arrows) running through the centre of the left lobe is the pancreatic duct.
The spleen (*) is visible in the top right of the image. (d,e) Pancreatic changes
affecting the caudal tip of the left pancreatic lobe of an 11-year-old female
neutered domestic shorthair cat presenting with a recent history of weight loss
and inappetence. (d) The left lobe (being measured between the calipers) is
predominantly normal in appearance, although the pancreatic duct is mildly
dilated. (e) In contrast, the caudal tip (arrows) is enlarged, hypoechoic and
irregularly marginated and surrounded by hyperechoic fat

d e

The presence of a thick left pancreatic limb, severely irregular


pancreatic margins and hyperechoic peripancreatic fat in cats with appropriate
clinical signs and raised serum feline pancreatic lipase immunoreactivity
concentrations is highly supportive of pancreatitis.

having this abnormality on ultrasonographic in addition to hyperechoic pancreatic fat,


examination, although it is important to the presence of a thick left pancreatic limb
note that the authors of these studies do not and severely irregular pancreatic margins
differentiate between cats with acute and in cats with appropriate clinical signs and
chronic pancreatitis.27,37 The authors of the raised serum fPLI concentrations is highly
earlier of these two studies report that, supportive of pancreatitis.27

JFMS CLINICAL PRACTICE 247


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 248

R E V I E W / Feline abdominal ultrasonography – the pancreas

* *
*

a b

Figure 9 Pancreatic oedema in two cats. (a) Ultrasound image from a 5-year-old female neutered domestic shorthair cat presenting for further investigation of
acute renal failure. Pleural and peritoneal effusion developed as a result of poor urine output. The pancreas is enlarged (arrows) and multiple anechoic striations
(asterisks) dissect between pancreatic lobules giving rise to a ‘tiger stripe’ appearance, indicative of pancreatic oedema. (b) Ultrasound image from a 4-year-old
male neutered domestic shorthair cat presenting with marked hypoalbuminaemia, ascites and peripheral oedema secondary to protein-losing nephropathy.
The arrows indicate the margins of the pancreas, and the asterisks indicate the anechoic striations within the pancreas. Videos showing pancreatic oedema,
including in a cat with severe hypoalbuminaemia, are available in the supplementary material

Pancreatic oedema results in pancreatic Chronic pancreatitis


enlargement and fluid accumulation within Recurrent episodes of inflammation over
the interlobular septae. This gives rise to months or years can lead to the development
multiple hypoechoic striations dispersed of chronic pancreatitis. Whereas acute pancre-
throughout the parenchyma – the so-called atitis is typically associated with neutrophilic
‘tiger stripe’ appearance.38 Although this inflammation, necrosis and oedema, chronic
finding is reported specifically in dogs, the pancreatitis leads to irreversible acinar loss
author has also observed this change in cats and fibrosis,9 and resembles the process seen in Ultrasonographic
(Figure 9). It can be seen in cases of pancreati- humans where fibrosis is more pronounced than changes
tis but can also occur as a result of portal inflammation.32 The condition is often mild and
hypertension and hypoalbuminaemia and asymptomatic and has a high prevalence in observed in cats
hence is not considered to be pathognomonic apparently healthy cats, causing some to
for inflammation.38 question its clinical significance.15 Histological
with chronic
Dilation of the biliary tree owing to evidence of chronic pancreatitis was identified pancreatitis
compression of the common bile duct by in 67/115 cats undergoing necropsy in one
an inflamed pancreas and mesenteric study; in comparison, 18 cats showed histo- tend to vary
lymphadenopathy are further changes that logical evidence of acute pancreatitis.32 between
have also been reported in association with Despite this, there is relatively little in the
pancreatitis.11,22,39,40 On ultrasound, the nor- literature regarding the ultrasonographic individuals.
mal common bile duct should measure no appearance of feline chronic pancreatitis.
greater than 4 mm in diameter, whereas As for acute pancreatitis, a normal ultra- In addition,
a diameter >5 mm is suggestive of extra- sound examination does not exclude the a normal
hepatic biliary obstruction (EHBO).11 It possibility of chronic pancreatitis, since the
should, of course, be remembered that disease processes present may be insufficient ultrasound does
there are several other differentials for EHBO to induce an alteration in the appearance of
aside from pancreatitis, such as cholelith- the pancreas on ultrasound.14 Similarly, the not exclude the
iasis.11 The ultrasonographic appearance of ultrasonographic changes observed have a possibility of
EHBO was discussed in more detail in the tendency to be somewhat variable between
article on the biliary tree in this series (see box individuals, thus complicating the diagnosis chronic
on page 255). further.1 In the dog, reported abnormalities
Further changes that may be appreciated include an increase or decrease in the size
pancreatitis.
on ultrasound in cats with acute pancreatitis of the pancreas, increased (possibly due
include thickening and/or altered layering of to fibrosis), decreased or mixed echogenicity
the gastric or duodenal wall and a mildly of the pancreatic parenchyma and normal or
dilated, hypomotile descending duodenum, mildly hyperechoic peripancreatic mesentery,
possibly with concurrent corrugation (due to although any increases in mesenteric
paralytic ileus).1,25,41 In some cats, these may echogenicity are usually less pronounced
be the only abnormalities present. than those seen with acute pancreatitis.1,42–44

248 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 249

R E V I E W / Feline abdominal ultrasonography – the pancreas

a
However, a further separate study found no
correlation between pancreatic duct width
and clinically significant pancreatic disease.5
Furthermore, since dilation of the pancreatic
duct can occur as a normal ageing change, it
should not be used as the sole indicator of
pancreatitis in the geriatric cat.
As with most diagnostic tests, ultrasound
has its limitations. As mentioned above, results
suggest that it may not be possible to distin-
guish between acute necrotising and chronic
non-suppurative pancreatitis with ultrasound,
even when the history, physical examination
findings, results of clinicopathological testing
b
and any radiographic abnormalities present
are taken into account.20 Furthermore, the
authors of a recent retrospective study of 42
cats presenting with at least two clinical signs
of pancreatitis and raised fPLI values were
unable to identify any significant correlation
between ultrasonographic changes and out-
come;37 thus the use of ultrasound for prognos-
tic purposes appears limited.
In view of the fact that the ultrasonographic
diagnosis of chronic pancreatitis is not always
straightforward, attempts have been made to
discover alternative means of obtaining a
more definitive diagnosis using ultrasound in
combination with a hormone called secretin.
In healthy individuals, secretin stimulates
Figure 10 (a,b) Chronic pancreatitis in a 5-year-old male neutered domestic the pancreas to secrete bicarbonate, resulting
shorthair cat presenting with a history of lethargy, inappetence and occasional
vomiting of 1 week’s duration. The left lobe of the pancreas (arrows) is enlarged, in dilation of the pancreatic duct, which is iden-
diffusely hypoechoic and surrounded by abnormally hyperechoic fat suggestive
of a localised steatitis. Exploratory coeliotomy was performed to acquire biopsies
tifiable ultrasonographically.46,47 It has been
of the liver, small intestine and pancreas. Final diagnoses based on histopathology shown that in humans with chronic pancreati-
were cholangiohepatitis, inflammatory bowel disease and marked chronic tis, the duct fails to dilate and it is thought that
pancreatitis with accompanying fibrosis and nodular regeneration. A video
showing chronic pancreatitis affecting the left lobe of the pancreas in the this occurs as a result of periductal fibrosis.47,48
same cat with triaditis is available in the supplementary material To investigate the potential use of this hormone
as a diagnostic tool for chronic pancreatitis in
Abnormal pancreatic thickness, an irregular cats, the effect of exogenous administration of
pancreatic margin, nodularity and hypo- secretin on the diameter of the pancreatic duct
echogenicity of the pancreas, hyperechoic in healthy cats was recorded.49 Mean pancreat-
mesentery and abdominal effusion have all ic duct diameter increased from 0.77 ± 0.33 mm
been reported in cats with chronic pancreatitis to 1.42 ± 0.40 mm following secretin administra-
confirmed by histopathology (Figure 10).5,20,27 tion and the mean percentage increase in pan-
Thus, it appears that there is a degree of over- creatic duct diameter over basal diameter up to
lap in the ultrasonographic appearance of 15 mins after secretin administration was 101.9
acute and chronic pancreatitis in the cat. There is a ± 58.8%.49 To date, the relationship between
Fibrosis and calcification of the pancreas as secretin administration and ductal diameter
a result of chronic pancreatitis can lead to the degree of in the diseased feline pancreas has not been
presence of shadowing hyperechoic foci. evaluated and, therefore, the ability of this
As with acute pancreatitis, dilation of the overlap in the diagnostic procedure to identify cats with
common bile duct may also be recognised ultrasonographic chronic pancreatitis has yet to be determined.
and, if adhesions form secondarily to chronic
inflammation, the duodenum and/or part of appearance of
Detection and differentiation of pancreatitis
the stomach can become displaced from their
normal position within the abdomen.1
acute and Differentiating acute from chronic pancreatitis
in the cat is challenging, and in some cases
In humans with chronic pancreatitis, irregu- chronic may not be possible without histopathology.
lar widening of the pancreatic ducts has been
reported and is believed to be due to periduc- pancreatitis Combining the results of tests such as fPLI and
ultrasound findings, rather than relying solely on
tal fibrosis.10 Dilation of the pancreatic duct in the cat. any one test, is likely to improve the detection of
has also been reported in cats with chronic
pancreatitis in cats.26
pancreatitis by the authors of one study.45

JFMS CLINICAL PRACTICE 249


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:52 Page 250

R E V I E W / Feline abdominal ultrasonography – the pancreas

Exocrine pancreatic insufficiency inflammatory exudate forms, eventually


Chronic pancreatitis is the most common becoming enclosed within a fibrous connec-
cause of exocrine pancreatic insufficiency tive tissue capsule. The term ‘pseudocyst’ is
(EPI), a condition seen only rarely in the appropriate because they lack a true epithelial
cat.36,50 Pancreatic nodularity and inhomo- lining. Identification of a pancreatic cystic
geneity have been reported in two cats with lesion in a patient with a clinical history of
EPI based on feline trypsin-like immunoreac- pancreatitis should raise the suspicion of a
tivity assay results.5 Hyperechogenicity and a pseudocyst.58
reduced volume of the pancreatic parenchy- There are occasional descriptions in the
ma, in association with dilation of the pancre- veterinary literature detailing the ultrasono-
atic duct with or without pancreatic calculi, graphic appearance of pancreatic pseudocysts
have also been reported with this condition.3 in cats.59,60 The wall of a pseudocyst is typical-
Hypermotility and distension of the intestinal ly much thicker and more irregular than that
tract may be observed concurrently due to of a true cyst and the lumen may be septated
EPI-related malabsorption.3 and contain internal echoes.59,61 An accompa-
nying distal acoustic enhancement artefact is
Cystic pancreatic abnormalities Identification often present owing to the fluid component of
Cystic pancreatic abnormalities include pan- the cyst. Complications arising from larger
creatic cysts and pseudocysts, abscesses and of a pancreatic pseudocysts, such as compression of the
pancreatic bladder. Neoplasia is discussed in cystic lesion in common bile duct causing EHBO, have been
a separate section below, alongside nodular reported in humans.62 Furthermore, pseudo-
hyperplasia. a patient with a cysts that become infected may form abscess-
es and ruptured pseudocyts in humans have
Pancreatic cysts clinical history been reported to cause severe peritonitis.63
Pancreatic cysts are occasionally identified of pancreatitis Spontaneous regression of human pancreatic
in cats1 and can be classified as true cysts, pseudocysts has also been reported.64
pseudocysts or retention cysts. True cysts should raise Aspiration of luminal contents from a
have an epithelial lining, do not communicate pseudocyst under ultrasound guidance is con-
with the pancreatic duct and are usually inci- the suspicion sidered to be a safe procedure and will typi-
dental.51,52 To date, they have only been of a cally reveal high levels of amylase and/or
reported in a handful of cases.53–55 A peduncu- lipase.59,65 This can be invaluable in helping to
lated true cyst attached to the body of the pan- pseudocyst. differentiate pseudocysts from abscesses
creas, which was presumed to be congenital in and cystic neoplasms, all of which can appear
origin, has been reported in a 5-year-old cat.53 similar ultrasonographically.59,65
On ultrasound examination, the cyst was The third type of cyst described in the pan-
3.91 cm in length, multilocular and had a thick creas, the retention cyst, forms due to the
wall with anechoic contents and occasional blockage of a pancreatic duct followed by the
septations. Histopathological examination of accumulation of glandular secretions. In
the cyst confirmed the presence of a lining humans, retention cysts are reported to be
comprising a single layer of cuboidal to incidental findings and have no clinical signif-
columnar epithelial cells.53 Multiple recurrent icance.58 They are usually small and have an
true pancreatic cysts of unknown aetiology, epithelial lining and are more likely to contain
associated with pancreatic inflammation, anechoic rather than echogenic fluid, in con-
atrophy and diabetes mellitus, have also been trast to inflammatory pseudocysts.1,58 To the
reported in a 14-year-old domestic shorthair author’s knowledge, retention cysts associat-
cat.54 Similar ultrasonographic findings are ed with the pancreas have not been reported
described in the most recent report: a well- in the cat.
defined multilobulated cystic structure locat- Cats with polycystic kidney disease develop
ed craniomedial to the left kidney was numerous cysts throughout the kidneys but
described on ultrasound in a 15-year-old can also develop cysts concurrently within the
female neutered domestic shorthair cat. liver and pancreas (Figure 11).66 Consequently,
At laparoscopy, a 7 cm diameter cyst was con- it is prudent to scan both the liver and pan-
firmed originating from the left pancreatic creas in cats presenting with this condition.
limb and subsequently omentalised.55
Pseudocysts form as a result of pancreatitis Aspiration of luminal contents from a
and pancreatic duct rupture. They have a non-
epithelialised fibrous capsule and are filled pseudocyst under ultrasound guidance can be
with fluid rich in pancreatic enzymes and invaluable in helping to differentiate pseudocysts
debris.56,57 It is postulated that focal pancreatic
necrosis and pancreatic duct rupture occur from abscesses and cystic neoplasms, all of which
as a result of pancreatitis. Pancreatic juices
leak into the area of necrotic tissue and an can appear similar ultrasonographically.

250 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 251

R E V I E W / Feline abdominal ultrasonography – the pancreas

Figure 11 Ultrasound images from a 14-year-old male neutered Persian cat with
polycystic kidney disease. (a) Large (approximately 8 cm diameter) thin-walled cyst
containing mildly echogenic fluid associated with the pancreas. (b) Multiple, variably
a sized, smaller cysts are visible throughout the entire pancreas (arrows). Concurrent
cysts were also present throughout both kidneys and the liver (not shown)

Pancreatic abscesses can be highly


Pancreatic abscessation
variable in appearance but usually present Pancreatic abscesses are uncommon in cats but
may develop as a consequence of pancreatitis
as thick-walled cavitary lesions with or an infected pseudocyst.67 Pancreatic absces-
hyperechoic or flocculent contents. sation has also been identified in a cat with
diabetes mellitus.68 Abscesses can be highly
a variable in appearance but usually present as
thick-walled cavitary lesions with hyper-
echoic or flocculent contents (Figure 12).67,68
Occasionally gas is also present and recognised
on ultrasound by the presence of hyperechoic
foci associated with a reverberation artefact.1

Figure 12 Pancreatic abscessation in two cats. (a,b) Ultrasound images from


an 11-year-old male neutered Norwegian Forest Cat presenting for investigation
of weight loss. Abdominal ultrasound revealed the presence of multiple, variably
sized cavitary lesions throughout the pancreas. Most lesions had a thick wall
and contained gravity-dependent sediment (arrows). Hyperechoic fat is also
visible adjacent to the lesions. Aspiration of the fluid from the largest of these
yielded a non-septic, neutrophilic exudate consistent with abscessation.
(c) Ultrasound image from an 8-year-old female neutered diabetic Bengal cat.
Multiple thick-walled cavitary lesions (arrows) are present within the right lobe
of the pancreas. Lesion contents varied from anechoic to echogenic. Note the
marked hyperechogenicity of the peripancreatic fat, reflecting adjacent
steatitis. Lesion aspiration was consistent with abscessation. Three videos
showing pancreatic abscessation are available in the supplementary material

b c

JFMS CLINICAL PRACTICE 251


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 252

R E V I E W / Feline abdominal ultrasonography – the pancreas

Pancreatic bladder old Maine Coon with chronic pancreatitis.70


A pancreatic bladder refers to cystic dilation It was thought that the obstruction of the
of the pancreatic duct, a rare condition in the duct resulted in pancreatic duct dilation and
cat.50,69,70 Some prefer the term pancreatic subsequent pancreatitis. In the same cat an
pseudobladder since there is no true bladder anomalous cystic structure containing calculi
associated with the pancreas, unlike the uri- that communicated with the pancreatic ductal
nary and biliary systems.1 On ultrasound, system was also identified and found to repre-
pancreatic bladders are fluid-filled structures sent a pancreatic pseudobladder following
associated with the pancreas that can be con- exploratory surgery. Migration of a calculus
fused with a bipartite gall bladder or a pancre- from the pseudobladder into the pancreatic
atic cyst.69,70 Identifying a connection between duct was considered to be the most likely
the cystic structure and the ductal system of explanation for the pancreaticolithiasis.70
the pancreas confirms the true nature of the
lesion.70 While they may be incidental, they Nodular hyperplasia and pancreatic
can reach a size sufficient to obstruct the com- neoplasia
mon bile duct, thereby causing icterus.69 The Nodular hyperplasia of the pancreas is a com-
presence of marked saccular dilation of the mon incidental finding in older cats.71 The
pancreatic duct in the absence of an obstruc- ultrasonographic appearance of nodular hyper-
tive process has also been described in cats.3 plasia in five cats has been described as multi-
Concurrent thickening of the pancreatic duct ple hypoechoic nodules within the pancreas
wall and the presence of anechoic to echo- varying in size from 3 mm to 10 mm in diame-
genic fluid within the duct lumen were addi- ter.72 Small pancreatic cysts have the potential to
tional findings reported in these cases.3 appear similar on ultrasound, although a distal
The cause of the severe ductal distension acoustic enhancement artefact is expected with
could not be determined. cysts due to their fluid content, thus allowing
Pancreatic bladder has also been reported them to be distinguished from solid nodules.3
in association with pancreaticolithiasis. The Exocrine pancreatic neoplasia, of which
latter is a rare condition that describes the adenocarcinoma is the most frequently
presence of one or more calculi within the encountered type, is rare in the cat, partic-
ductal system or parenchyma of the pancreas. ularly when compared with pancreatitis, with
Calculi are usually easily recognised by their incidences of 0.013% and 0.05% being report-
characteristic strongly hyperechoic interface ed in large cohorts of cats.73,74 Pancreatic
and distal acoustic shadowing (Figure 13). adenocarcinoma usually affects older cats;
Obstruction of the pancreatic duct by a stone in two studies comprising a total of 48 cats
(pancreatolith) has been reported in a 14-year- with malignant pancreatic tumours, the

Calculi associated with pancreaticolithiasis


can usually be easily recognised by their characteristic strongly
hyperechoic interface and distal acoustic shadowing.

a b

Figure 13 Pancreaticolithiasis in an 8-year-old female neutered domestic shorthair cat. (a) Two calculi (arrows) are visible within the dilated pancreatic duct of the
left lobe. (b) Marked dilation of the pancreatic duct within the right lobe (arrows) in association with further calculi (arrowheads)

252 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 253

R E V I E W / Feline abdominal ultrasonography – the pancreas

approximate mean age was 12 years.72,75 cytology and/or histopathology remains


Any part of the pancreas may be affected75 necessary for definitive differentiation.
and cases of pancreatic adenocarcinoma have Ancillary findings in cases of pancreatic
been reported in association with paraneo- neoplasia include evidence of pancreatic
plastic alopecia.76–78 On ultrasound examina- mineralisation,72 invasion of the duodenal
tion, pancreatic neoplasia typically presents as wall, free abdominal fluid, hyperechogenicity
a hypoechoic nodule or mass in the region of of peripancreatic fat, lymphadenopathy and
the pancreas, although diffuse infiltration or obstruction of the common bile duct.72,75 The
even a normal-appearing pancreas is also pos- presence or absence of abdominal effusion can
sible (Figure 14).1,72,75,79 Solitary masses exceed- also be used as a prognostic indicator. In one
ing 2 cm diameter in at least one dimension report of 34 cats with pancreatic adeno-
are reported to be more likely to be neoplas- carcinoma, the median survival of those cats
tic.72 The presence of multiple pancreatic nod- with abdominal effusion at diagnosis (16 in
ules measuring 1.5 cm to 6 cm in diameter has total) was 30 days compared with 165 days for
also been reported in cats with pancreatic cats with no effusion.79 Unfortunately, feline
adenocarcinoma.75 Although hyperplastic nod- pancreatic adenocarcinoma has a poor prog-
ules tend to be smaller than this, there is still nosis and has often metastasised by the time
considerable overlap in the ultrasonographic of diagnosis, particularly to the liver, lung and
appearance of both conditions and hence small intestine.73,75

On ultrasound, pancreatic neoplasia typically presents


as a hypoechoic nodule or mass in the region of the pancreas, although diffuse
infiltration or even a normal-appearing pancreas is also possible.

Figure 14 Pancreatic adenocarcinoma in three cats. (a) Ultrasound image of


the pancreas of a 10-year-old male neutered domestic shorthair cat presenting
with a 2-month history of progressive lethargy, intermittent diarrhoea and, more
recently, vomiting. The pancreas is moderately and diffusely enlarged up to
2.4 cm in thickness, with a mass in the right lobe (arrows). Pancreatic borders
are irregular and the parenchyma is heterogeneous throughout. Cytology
from ultrasound-guided fine-needle aspiration (FNA) was most consistent with
pancreatic adenocarcinoma. (b) A 1.5 cm x 2.5 cm mixed echogenicity mass
(arrows) within the right lobe of the pancreas of an 8-year-old male neutered
domestic shorthair cat presenting for further investigation of inappetence
and weight loss. Histopathology results were consistent with tubular
adenocarcinoma of the exocrine pancreas and concurrent nodular hyperplasia.
(c) Ultrasound image of a poorly circumscribed hypoechoic mass (arrowheads)
associated with the left lobe of the pancreas in a 14-year-old British Shorthair
presenting with lethargy, inappetence and ascites. The spleen is visible in the
near field of the image. Multiple poorly defined hypoechoic nodules (arrows)
are visible throughout the hyperechoic mesentery and a moderate volume of
a slightly echogenic peritoneal fluid is also present. FNA results were consistent
with pancreatic adenocarcinoma and widespread carcinomatosis

b c

JFMS CLINICAL PRACTICE 253


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 254

R E V I E W / Feline abdominal ultrasonography – the pancreas

Lymphoma of the pancreas is also recog- Neoplasia of the endocrine pancreas


nised in the cat but may represent pancreatic Neoplasia of the endocrine pancreas is
involvement in multicentric disease rather extremely rare in the cat and, as a result,
than a primary tumour of the pancreas.72 descriptions of the ultrasonographic findings
It has been reported to result in irregular are scarce. An insulinoma has been described
margination, diffuse enlargement and hypo- in a 15-year-old female neutered domestic
echogenicity of the pancreas (Figure 15).3 shorthair cat in which it presented as a 9 mm
Pancreatic adenomas have likewise been diameter, mildly hyperechoic, spherical
described in the cat and can present nodule within the left pancreatic lobe.80 The
as smoothly defined nodules with an tumour was considered to be a benign islet
echogenicity similar to that of adjacent cell adenoma based on well-differentiated cell
pancreatic tissue.3,73 However, the concurrent morphology and lack of invasive growth.80
ancillary changes described above, including Another report documents the presence of a
lymphadenopathy, would not usually be 1 cm diameter nodule in the body of the pan-
expected. creas of a 17-year-old male neutered Siamese
cat, confirmed to be an islet cell carcinoma fol-
lowing histopathology.81 In this cat, metas-
tases were identified in the liver and regional
lymph nodes.81 The ultrasonographic findings
from both of these reports in cats are similar to
those in dogs; canine endocrine pancreatic
tumours are also typically small nodules (usu-
ally <2.5 cm diameter) that can be challenging
to detect on ultrasound.1,82 These descriptions
are further supported by the most recent
report of insulinoma, in a 14-year-old male
neutered domestic shorthair cat, which
describes the presence of a focal, well-defined
hypoechoic pancreatic mass measuring 16
mm x 23 mm diameter.83

Metastatic neoplasia
There are only occasional reports of metastatic
disease occurring within the pancreas in cats.
a
Pancreatic metastases were identified in 2/26
cats with visceral haemangiosarcoma in one
study,84 and in an 11-year-old cat secondarily
to a prostatic adenocarcinoma,85 although the
specific ultrasonographic features were not
described.

Rupture of the pancreas


Pancreatic rupture is a very rare event that
has been documented in cats with high-rise
syndrome.86 Leakage of pancreatic enzymes
into the abdominal cavity ensues, resulting in
pancreatic autodigestion and saponification of

Lymphoma of the
pancreas has been reported to
result in irregular margination,
diffuse enlargement and
hypoechogenicity of
b
the pancreas.
Figure 15 (a,b) Pancreatic lymphoma in a 16-year-old male neutered domestic shorthair cat
referred for assessment of an abdominal mass. The pancreas is markedly enlarged and contains
multiple well-circumscribed hypoechoic masses throughout. Fat surrounding the pancreas is
mildly hyperechoic. Concurrent hepatosplenomegaly and a gastric mass were noted at the time
of abdominal ultrasound in addition to marked enlargement of hepatic, gastric and jejunal
lymph nodes

254 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 255

R E V I E W / Feline abdominal ultrasonography – the pancreas

adjacent fat. Without the correct diagnosis and the normal pancreatic parenchyma has been
treatment, the condition can lead to multi- described in detail in 10 clinically healthy cats
organ failure and death. On ultrasound, the using a second-generation contrast medium
pancreas in four affected cats appeared hyper- containing sulfur hexafluoride (SonoVue;
echoic and was surrounded by hyperechoic Bracco UK).92 Additionally, significantly high-
peripancreatic mesenteric fat.86 Additional er pancreatic blood volumes and vascularity
findings in all affected cats included ascites are present in cats with pancreatic disease
and hypomotility of the gastrointestinal tract. compared with normal cats, regardless of
It is thought that the left pancreatic lobe may the Doppler method used (ie, pre-contrast
be particularly vulnerable to rupture and, vs post-contrast, colour vs power Doppler).91
in the four cases described, the diagnosis of As expected, power Doppler yields higher
pancreatic rupture was confirmed either at Doppler values than colour Doppler and is
surgery or at post-mortem examination. thus superior. Contrast-enhanced ultrasonog-
Traumatic pancreatitis has also been report- raphy has also been used in the diagnosis of
ed in association with high-rise syndrome.87 pancreatic insulinoma in a cat.83 Further
Abdominal ultrasonography of affected cats research is required to determine whether this
may reveal any combination of pancreatic technique can be used in cats that are suspect-
enlargement, decreased or heterogeneous ed of having pancreatic pathology but have
pancreatic echogenicity, hyperechoic mesen- normal B-mode scans, and to determine the
tery and peritoneal effusion.87 accuracy of Doppler with regard to differenti-
ating the various disorders of the pancreas.
Contrast-enhanced Doppler
ultrasound
Earlier articles in the series
Contrast-enhanced Doppler techniques have ✜ The liver (2019; 21: 12–24)
been used in the human field to differentiate ✜ The biliary tree (2019; 21: 429–441)
between pancreatitis and neoplasia, to detect ✜ Hepatic vascular anomalies (2019; 21:
parenchymal necrosis in individuals with 645–654)
acute severe pancreatitis and to assess pancre- ✜ The normal gastrointestinal tract (2019; 21:
atic tumours.88–90 Accordingly, the feasibility 1039–1046)
of using contrast-enhanced Doppler ultra- ✜ The diseased gastrointestinal tract (2019; 21:
sound to evaluate the feline pancreas has also 1047–1060)
been investigated.91,92 The perfusion pattern of

Interventional procedures: sampling considerations


There is significant overlap in the ultrasonographic appearance leakage. Where abdominal fluid is present, it may be possible to
of pancreatic neoplasia, nodular hyperplasia and pancreatitis, achieve a diagnosis based on cytology of a sample of fluid,
and hence it is often not possible to discriminate between these although the success rate is typically higher when using tissue
conditions on the basis of ultrasound appearance alone.79 aspiration.79 This is thought to be due to difficulty in differentiat-
Tissue sampling via either biopsy or fine-needle aspiration (FNA) ing carcinoma cells from reactive mesothelial cells.79 It should
is usually required to make a definitive diagnosis and is diagnos- be noted that a negative FNA cytology result does not necessar-
tic in a high proportion of cases.79 ily exclude a diagnosis of pancreatitis due to the potential for the
Pancreatic FNA has been performed in several studies and no disease to be focal or multifocal in nature.14 Samples may also
complications were reported.59,73,79 The safety of percutaneous be poorly cellular in cases of chronic pancreatitis, most likely
ultrasound-guided pancreatic FNA in the cat has also been due to fibrotic replacement of normal pancreatic tissue.94
specifically evaluated.93 In that study, there was no difference in
the complication rate between cats undergoing ultrasound- There is significant overlap in the
guided FNA of the pancreas and those in which sampling was
not performed, and many of the complications reported, such as ultrasonographic appearance of
hypotension and respiratory distress, were considered unlikely pancreatic neoplasia, nodular hyperplasia
to have been caused by the aspiration procedure.93 Cytology
samples were of diagnostic quality in 67% of cases and agreed and pancreatitis, and so tissue sampling
with histopathology in 6/7 cases in which histopathology was
also available.93
via either biopsy or fine-needle aspiration
The author’s preference is to use a 23 G hypodermic needle is usually required to make a
attached to a 5 ml syringe with either a suction or non-suction
technique. Where possible, three aspirates are collected to definitive diagnosis.
increase diagnostic yield. Cavitary lesions such as abscesses
and pseudocysts can be drained safely, although as much fluid
as possible should be aspirated to reduce the risk of subsequent

JFMS CLINICAL PRACTICE 255


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 256

R E V I E W / Feline abdominal ultrasonography – the pancreas

Case notes
Charlie, a 16-year-old male neutered domestic
shorthair cat, was referred for further investigation
of anorexia and jaundice.

Recent history For the previous 6 weeks, Charlie’s


appetite had been significantly reduced and he had been
vomiting intermittently, usually food but sometimes just froth
with a small volume of fluid. He became moderately jaundiced
during this period, although this had improved slightly
immediately prior to referral.

Long-term history Charlie had been with his current owners


for 14 years and was rescued as a stray, at which time he was
estimated to be about 2 years old. He had generally been a well
cat until 2 years prior to referral when he was diagnosed with
hyperthyroidism. This was treated with methimazole until he
developed icterus, at which point his medication was stopped.
Figure A Dilation of an intrahepatic bile duct (arrowheads). Note the typical
Physical examination and laboratory findings On tortuosity of the duct and free peritoneal fluid surrounding the liver lobe
physical examination, Charlie was quiet, alert and responsive
with a body condition score of 2/9 and rectal temperature of
38.2ºC. His mucous membranes were pink with a capillary
refill time of 1 s. Heart rate was 180 beats per minute and
no murmur was detected. His skin and sclerae were noted
to be icteric and he had a non-painful pendulous abdomen
suspected to be due to a peritoneal effusion. Peripheral
lymph nodes were unremarkable on palpation.
Abnormal laboratory findings are shown in the table.

Abnormal laboratory findings


Parameter Result Reference interval
Albumin (g/l) 23.8 25.0–45.0
Alanine aminotransferase (U/l) 391.4 5.0–60.0
Alkaline phosphatase (U/l) 717.0 ⩽60.0
Aspartate transaminase (U/l) 175.0 10.0–50.0 Figure B Several dilated extrahepatic bile ducts

Total bilirubin (µmol/l) 193.1 0.1–5.1


Bile acids (fasting; µmol/l)) 359.6 0.1–5.0
Glucose (mmol/l) 10.2 3.9–8.0
Thyroxine (nmol/l) 102.2 10.0–60.0

Imaging Abdominal ultrasound revealed the presence of


marked distension of the intra- and extrahepatic portions
of the biliary tract (Figures A and B). The gall bladder was
subjectively enlarged and contained a moderate amount
of non-shadowing echogenic sediment. A 3 cm diameter,
irregularly marginated, hypoechoic mass was identified in
the region of the junction between the right lobe and body
of the pancreas (Figure C). The mass partially enveloped and
invaded the adjacent segment of duodenum, causing loss of
wall layering (Figure D). A small volume of anechoic peritoneal
fluid was also visible throughout the abdomen. Findings
were consistent with a pancreatic mass causing extrahepatic
biliary obstruction. The primary differential for the mass was
neoplasia. Fine-needle aspirates of the pancreatic mass were
Figure C Large pancreatic mass (arrowheads) adjacent to the duodenum
acquired under ultrasound guidance at the time of the scan. in transverse (arrow)
As anticipated, cytology results confirmed the mass to be
pancreatic adenocarcinoma. Continued on page 257

256 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 257

R E V I E W / Feline abdominal ultrasonography – the pancreas

Continued from page 256


Treatment and follow-up Due to the poor prognosis, the
owners opted for euthanasia at the referring veterinary practice.

✜ What this case demonstrates: Strictly speaking,


it is not normally possible to differentiate between pancreatic
neoplasia and pancreatitis based on ultrasonographic
appearance alone. Although pancreatitis is much more
common than neoplasia, most ultrasonographic features
are common to both conditions. Evidence of invasion of
the duodenal wall is a characteristic of an aggressive
lesion and one of the few imaging features that is much
more suggestive of pancreatic neoplasia than pancreatitis.
In rare cases where this is identified, and in the light of
the poor prognosis, sampling of the pancreas/pancreatic
mass is recommended to allow expedient confirmation
Figure D Close-up view showing invasion of the duodenal wall (arrow) by of the suspected diagnosis.
the pancreatic mass

Conflict of interest Ethical approval


SUPPLEMENTARY
The author declared no potential MATERIAL This work did not involve the use of animals and
conflicts of interest with respect to Videos to accompany the still therefore ethical approval was not required.
the research, authorship, and/or figures within this article – see legends
to Figures 5, 7–10 and 12 for more
publication of this article. information – are available as
Informed consent
supplementary material at: jfms.com
Funding DOI: 10.1177/1098612X20903599 This work did not involve the use of animals and
therefore informed consent was not required.
The author received no financial No animals or humans are identifiable within
support for the research, authorship this publication, and therefore additional informed
and/or publication of this article. consent for publication was not required.

KEY POINTS
✜ The left lobe of the pancreas is larger than the right in the cat and easier to identify on ultrasound examination.
The pancreatic duct within the left lobe is usually clearly visible on ultrasound.
✜ The landmarks that facilitate identification of the left pancreatic lobe are the stomach cranially, colon caudally
and spleen laterally.
✜ The landmark for the right lobe of the pancreas is the descending limb of the duodenum.
✜ The feline pancreas is well-defined and isoechoic to slightly hypoechoic relative to surrounding fat.
✜ Key ultrasonographic abnormalities suggestive of acute pancreatitis include enlargement and reduced echogenicity
of the pancreas, and increased echogenicity of peripancreatic fat.
✜ Ultrasonographic findings suggestive of chronic pancreatitis include abnormal echogenicity and/or size of the
pancreas, irregularity of pancreatic margins, a nodular appearance and mild hyperechogenicity of peripancreatic fat.
✜ As a minimum, the liver and small intestine should also be examined with ultrasound if features indicative of
pancreatitis are identified.
✜ Multiple pancreatic nodules <1 cm diameter are more likely to represent nodular hyperplasia, whereas a solitary
mass >2 cm diameter is more likely to be neoplastic.
✜ Potential consequences of pancreatitis include extrahepatic biliary obstruction and the formation of pancreatic
pseudocysts or abscesses. Pseudocysts and abscesses typically have thick walls and may contain echogenic
contents and, as such, it may not be possible to distinguish between them ultrasonographically. Differentiation
may be possible through aspiration of contents and determination of amylase and lipase levels.
✜ Since pancreatitis can appear mass-like on ultrasound and neoplasia can produce diffuse pancreatic
changes, FNA of the pancreas may be warranted and is considered to be a safe and minimally
invasive technique.

JFMS CLINICAL PRACTICE 257


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 258

R E V I E W / Feline abdominal ultrasonography – the pancreas

References feline trypsin-like immunoreactivity for the diagnosis of pancre-


atitis in cats. J Am Vet Med Assoc 2000; 217: 37–42.
1 Nyland TG and Mattoon JS. Pancreas. In: Nyland TG and Mattoon 25 Saunders HM, VanWinkle TJ, Drobatz K, et al. Ultrasonographic
JS (eds). Small animal diagnostic ultrasound. 3rd ed. St Louis, MO: findings in cats with clinical, gross pathologic, and histologic
Elsevier Saunders, 2015, pp 438–467. evidence of acute pancreatic necrosis: 20 cases (1994–2001). J Am Vet
2 Lamb CR. Abdominal ultrasonography in small animals: examination Med Assoc 2002; 221: 1724–1730.
of the liver, spleen and pancreas. J Small Anim Pract 1990; 31: 5–14. 26 Forman MA, Marks SL, De Cock HE, et al. Evaluation of serum
3 Penninck D and d’Anjou MA. Pancreas. In: Penninck D and d’Anjou feline pancreatic lipase immunoreactivity and helical computed
MA (eds). Atlas of small animal ultrasonography. 2nd ed. Iowa: tomography versus conventional testing for the diagnosis of feline
John Wiley, 2015, pp 309–330. pancreatitis. J Vet Intern Med 2004; 18: 807–815.
4 Barone R. Anatomie comparee des mammiferes domestique. Tome 3, 27 Williams JM, Panciera DL, Larson MM, et al. Ultrasonographic find-
Splanchnologie 1. 3rd ed. Paris: Vigot 1997, p 853. ings of the pancreas in cats with elevated serum pancreatic lipase
5 Hecht S, Penninck DG, Mahony OM, et al. Relationship of pancreatic immunoreactivity. J Vet Intern Med 2013; 27: 913–918.
duct dilation to age and clinical findings in cats. Vet Radiol 28 Oppliger S, Hartnack S, Reusch CE, et al. Agreement of serum feline
Ultrasound 2006; 47: 287–294. pancreas-specific lipase and colorimetric lipase assays with pan-
6 Larson MM, Panciera DL, Ward DL, et al. Age-related changes in creatic ultrasonographic findings in cats with suspicion of pancre-
the ultrasound appearance of the normal feline pancreas. Vet Radiol atitis: 161 cases (2008–2012). J Am Vet Med Assoc 2014; 244: 1060–1065.
Ultrasound 2005; 46: 238–242. 29 Akol KG, Washabau RJ, Saunders HM, et al. Acute pancreatitis in
7 Etue SM, Penninck DG, Labato MA, et al. Ultrasonography of the cats with hepatic lipidosis. J Vet Intern Med 1993; 7: 205–209.
normal feline pancreas and associated anatomic landmarks: 30 Weiss DJ, Gagne JM and Armstrong PJ. Relationship between
a prospective study of 20 cats. Vet Radiol Ultrasound 2001; 42: 330–336. inflammatory hepatic disease and inflammatory bowel disease, pan-
8 Evans H and de Lahunta A. The digestive apparatus and abdomen. creatitis, and nephritis in cats. J Am Vet Med Assoc 1996; 209: 1114–1116.
In: Evans H and de Lahunta A (eds). Miller’s anatomy of the dog. 31 Bailey S, Benigni L, Eastwood J, et al. Comparisons between cats
4th ed. St Louis, MO: Elsevier Saunders, 2013, pp 281–338. with normal and increased fPLI concentrations in cats diagnosed
9 Watson P. Pancreatitis in dogs and cats: definitions and pathophys- with inflammatory bowel disease. J Small Anim Pract 2010; 51: 484–489.
iology. J Small Anim Pract 2015; 56: 3–12. 32 De Cock HE, Forman MA, Farver TB, et al. Prevalence and histopatho-
10 Atri M and Finnegan PW. The pancreas. In: Rumack CM, Wilson SR logic characteristics of pancreatitis in cats. Vet Pathol 2007; 44: 39–49.
and Charboneau JW (eds). Diagnostic ultrasound. St Louis, MO: 33 Mansfield CS and Jones BR. Review of feline pancreatitis part one: the
Mosby, 1998, pp 225–277. normal feline pancreas, the pathophysiology, classification, preva-
11 Leveille R, Biller DS and Shiroma JT. Sonographic evaluation of the lence and aetiologies of pancreatitis. J Feline Med Surg 2001; 3: 117–124.
common bile duct in cats. J Vet Intern Med 1996; 10: 296–299. 34 Armstrong PJ and Williams DA. Pancreatitis in cats. Top Companion
12 Crouch JE. Text-atlas of cat anatomy. Toronto, Canada: Lea & Febiger Anim Med 2012; 27: 140–147.
and Macmillan Co of Canada, 1969, p 340. 35 Simpson KW, Shiroma JT, Biller DS, et al. Ante mortem diagnosis of
13 Center SA. Diseases of the gallbladder and biliary tree. Vet Clin pancreatitis in four cats. J Small Anim Pract 1994; 35: 93–99.
North Am Small Anim Pract 2009; 39: 543–598. 36 Hecht S and Henry G. Sonographic evaluation of the normal and
14 Xenoulis PG. Diagnosis of pancreatitis in dogs and cats. J Small abnormal pancreas. Clin Tech Small Anim Pract 2007; 22: 115–121.
Anim Pract 2015; 56: 13–26. 37 Moser K, Mitze S, Teske E, et al. Evaluation of sonographic para-
15 Bazelle J and Watson P. Pancreatitis in cats: is it acute, is it chronic, meters as prognostic risk factors in cats with pancreatitis – a retro-
is it significant? J Feline Med Surg 2014; 16: 395–406. spective study in 42 cats [article in German]. Tierarztl Prax Ausg K
16 Steiner JM and Williams DA. Feline pancreatitis. Comp Cont Educ Kleintiere Heimtiere 2018; 46: 386–392.
Pract Vet 1997; 19: 590–601. 38 Lamb CR. Pancreatic edema in dogs with hypoalbuminemia or
17 Nivy R, Kaplanov A, Kuzi S, et al. A retrospective study of 157 portal hypertension. J Vet Intern Med 1999; 13: 498–500.
hospitalized cats with pancreatitis in a tertiary care center: clinical, 39 Mayhew PD, Holt DE, McLear RC, et al. Pathogenesis and outcome
imaging and laboratory findings, potential prognostic markers of extrahepatic biliary obstruction in cats. J Small Anim Pract 2002;
and outcome. J Vet Intern Med 2018; 32: 1874–1885. 43: 247–253.
18 Hill RC and Van Winkle TJ. Acute necrotizing pancreatitis and 40 Son TT, Thompson L, Serrano S, et al. Surgical intervention in the
acute suppurative pancreatitis in the cat. A retrospective study management of severe acute pancreatitis in cats: 8 cases
of 40 cases (1976–1989). J Vet Intern Med 1993; 7: 25–33. (2003–2007). J Vet Emerg Crit Care (San Antonio) 2010; 20: 426–435.
19 Mansfield CS and Jones BR. Review of feline pancreatitis part two: clin- 41 Moon ML, Biller DS and Armbrust LJ. Ultrasonographic appearance
ical signs, diagnosis and treatment. J Feline Med Surg 2001; 3: 125–132. and etiology of corrugated small intestine. Vet Radiol Ultrasound
20 Ferreri JA, Hardam E, Kimmel SE, et al. Clinical differentiation of 2003; 44: 199–203.
acute necrotizing from chronic nonsuppurative pancreatitis in cats: 42 Morita Y, Takiguchi M, Yasuda J, et al. Endoscopic ultrasonographic
63 cases (1996–2001). J Am Vet Med Assoc 2003; 223: 469–474. findings of the pancreas after pancreatic duct ligation in the dog.
21 Steiner JM. Diagnosis of pancreatitis. Vet Clin North Am Small Anim Vet Radiol Ultrasound 1998; 39: 557–562.
Pract 2003; 33: 1181–1195. 43 Watson PJ, Archer J, Roulois AJ, et al. Observational study of 14
22 Gerhardt A, Steiner JM, Williams DA, et al. Comparison of the cases of chronic pancreatitis in dogs. Vet Rec 2010; 167: 968–976.
sensitivity of different diagnostic tests for pancreatitis in cats. 44 Saunders HM. Ultrasonography of the pancreas. Probl Vet Med 1991;
J Vet Intern Med 2001; 15: 329–333. 3: 583–603.
23 Williams D. The pancreas. In: Guilford WG, Center SA, Strombeck 45 Wall M, Biller DS, Schoning P, et al. Pancreatitis in a cat demonstrat-
DR, et al (eds). Strombeck’s small animal gastroenterology. 3rd ed. ing pancreatic duct dilatation ultrasonographically. J Am Anim
Philadelphia: WB Saunders, 1996, pp 381–410. Hosp Assoc 2001; 37: 49–53.
24 Swift NC, Marks SL, MacLachlan NJ, et al. Evaluation of serum 46 Glaser J, Esser W and Holtmannspotter K. Sonographic visualiza-

258 JFMS CLINICAL PRACTICE


241_259_Griffin_pancreas2.qxp_FAB 03/02/2020 12:53 Page 259

R E V I E W / Feline abdominal ultrasonography – the pancreas

tion of the pancreatic duct before and after secretin stimulation: of domestic animals. San Diego: Academic Press, 1993, pp 407–424.
an aid in the diagnosis of chronic pancreatitis [article in German]. 72 Hecht S, Penninck DG and Keating JH. Imaging findings in pancre-
Ultraschall Med 1985; 6: 106–109. atic neoplasia and nodular hyperplasia in 19 cats. Vet Radiol
47 Bolondi L, Gaiani S, Gullo L, et al. Secretin administration induces Ultrasound 2007; 48: 45–50.
a dilatation of main pancreatic duct. Dig Dis Sci 1984; 29: 802–808. 73 Seaman RL. Exocrine pancreatic neoplasia in the cat: a case series.
48 Glaser J, Mann O and Pausch J. Diagnosis of chronic pancreatitis by J Am Anim Hosp Assoc 2004; 40: 238–245.
means of a sonographic secretin test. Int J Pancreatol 1994; 15: 195–200. 74 Prister WA. Data from eleven United States and Canadian colleges
49 Baron ML, Hecht S, Matthews AR, et al. Ultrasonographic observa- of veterinary medicine on pancreatic carcinoma in domestic ani-
tion of secretin-induced pancreatic duct dilation in healthy cats. mals. Cancer Res 1974; 34: 1372–1375.
Vet Radiol Ultrasound 2010; 51: 86–89. 75 Linderman MJ, Brodsky EM, de Lorimier LP, et al. Feline exocrine
50 Garvey MS and Zawie DA. Feline pancreatic disease. Vet Clin North pancreatic carcinoma: a retrospective study of 34 cases. Vet Comp
Am Small Anim Pract 1984; 14: 1231–1246. Oncol 2013; 11: 208–218.
51 Howard JM. Cystic neoplasms and true cysts of the pancreas. Surg 76 Pascal-Tenorio A, Olivry T, Gross TL, et al. Paraneoplastic alopecia asso-
Clin North Am 1989; 69: 651–665. ciated with internal malignancies in the cat. Vet Dermatol 1997; 8: 47–52.
52 Bergin D, Ho LM, Jowell PS, et al. Simple pancreatic cysts: CT and 77 Godfrey DR. A case of feline paraneoplastic alopecia with secondary
endosonographic appearances. AJR Am J Roentgenol 2002; 178: 837–840. Malassezia-associated dermatitis. J Small Anim Pract 1998; 39: 394–396.
53 Coleman MG, Robson MC and Harvey C. Pancreatic cyst in a cat. 78 Tasker S, Griffon DJ, Nuttall TJ, et al. Resolution of paraneoplastic
N Z Vet J 2005; 53: 157–159. alopecia following surgical removal of a pancreatic carcinoma in a
54 Branter EM and Viviano KR. Multiple recurrent pancreatic cysts cat. J Small Anim Pract 1999; 40: 16–19.
with associated pancreatic inflammation and atrophy in a cat. 79 Bennett PF, Hahn KA, Toal RL, et al. Ultrasonographic and
J Feline Med Surg 2010; 12: 822–827. cytopathological diagnosis of exocrine pancreatic carcinoma in the
55 Bruckner M. Laparoscopic omentalization of a pancreatic cyst in dog and cat. J Am Anim Hosp Assoc 2001; 37: 466–473.
a cat. J Am Vet Med Assoc 2019; 255: 213–218. 80 Schaub S and Wigger A. Ultrasound-aided diagnosis of an insulino-
56 Jones DR, Vaughan RA and Timberlake GA. Pancreatic pseudocyst: ma in a cat. Tierarztl Prax Ausg K Kleintiere Heimtiere 2013; 41: 338–342.
diagnosis and management. South Med J 1992; 85: 729–734. 81 Hawks D, Peterson ME, Hawkins KL, et al. Insulin-secreting pancre-
57 Reber HA and Way LW. Pancreatic pseudocyst. In: Way LW (ed). atic (islet cell) carcinoma in a cat. J Vet Intern Med 1992; 6: 193–196.
Current surgical diagnosis and treatment. Norwalk: CT: Appleton 82 Lamb CR, Simpson KW, Boswood A, et al. Ultrasonography of
& Lange, 1944, pp 577–580. pancreatic neoplasia in the dog: a retrospective review of 16 cases.
58 Karoumpalis I and Christodoulou DK. Cystic lesions of the pan- Vet Rec 1995; 137: 65–68.
creas. Ann Gastroenterol 2016; 29: 155–161. 83 Cervone M, Harel M, Segard-Weisse E, et al. Use of contrast-
59 VanEnkevort BA, O’Brien RT and Young KM. Pancreatic pseudo- enhanced ultrasonography for the detection of a feline insulino-
cysts in 4 dogs and 2 cats: ultrasonographic and clinicopathologic ma. JFMS Open Rep 2019; 5. DOI: 10.1177/2055116919876140.
findings. J Vet Intern Med 1999; 13: 309–313. 84 Culp WT, Drobatz KJ, Glassman MM, et al. Feline visceral heman-
60 Hines BL, Salisbury SK, Jakovljevic S, et al. Pancreatic pseudocyst giosarcoma. J Vet Intern Med 2008; 22: 148–152.
associated with chronic-active necrotizing pancreatitis in a cat. 85 Hubbard BS, Vulgamott JC and Liska WD. Prostatic adenocarcino-
J Am Anim Hosp Assoc 1996; 32: 147–152. ma in a cat. J Am Vet Med Assoc 1990; 197: 1493–1494.
61 Laing FC, Gooding GA, Brown T, et al. Atypical pseudocysts of the pan- 86 Liehmann LM, Dorner J, Hittmair KM, et al. Pancreatic rupture in four
creas: an ultrasonographic evaluation. J Clin Ultrasound 1979; 7: 27–33. cats with high-rise syndrome. J Feline Med Surg 2012; 14: 131–137.
62 Skellenger ME, Patterson D, Foley NT, et al. Cholestasis due to 87 Zimmermann E, Hittmair KM, Suchodolski JS, et al. Serum feline-
compression of the common bile duct by pancreatic pseudocysts. specific pancreatic lipase immunoreactivity concentrations and
Am J Surg 1983; 145: 343–348. abdominal ultrasonographic findings in cats with trauma resulting
63 Rocha R, Marinho R, Gomes A, et al. Spontaneous rupture of from high-rise syndrome. J Am Vet Med Assoc 2013; 242: 1238–1243.
pancreatic pseudocyst: report of two cases. Case Rep Surg 2016; 88 Hocke M and Dietrich CF. Vascularisation pattern of chronic
2016. DOI: 10.1155/2016/7056567. pancreatitis compared with pancreatic carcinoma: results from
64 Sarti DA. Rapid development and spontaneous regression of pancreat- contrast-enhanced endoscopic ultrasound. Int J Inflam 2012; 2012.
ic pseudocysts documented by ultrasound. Radiology 1977; 125: 789–793. DOI: 10.1155/2012/420787.
65 Sand JA, Hyoty MK, Mattila J, et al. Clinical assessment compared 89 Rickes S, Monkemuller K and Malfertheiner P. Acute severe pancreati-
with cyst fluid analysis in the differential diagnosis of cystic tis: contrast-enhanced sonography. Abdom Imaging 2007; 32: 362–364.
lesions in the pancreas. Surgery 1996; 119: 275–280. 90 De Robertis R, D’Onofrio M, Crosara S, et al. Contrast-enhanced
66 Bosje JT, van den Ingh TS and van der Linde-Sipman JS. Polycystic ultrasound of pancreatic tumours. Australas J Ultrasound Med 2014;
kidney and liver disease in cats. Vet Q 1998; 20: 136–139. 17: 96–109.
67 Nemoto Y, Haraguchi T, Shimokawa Miyama T, et al. Pancreatic 91 Rademacher N, Ohlerth S, Scharf G, et al. Contrast-enhanced power
abscess in a cat due to Staphylococcus aureus infection. J Vet Med and color Doppler ultrasonography of the pancreas in healthy and
Sci 2017; 79: 1146–1150. diseased cats. J Vet Intern Med 2008; 22: 1310–1316.
68 Lee M, Kang JH, Chang D, et al. Pancreatic abscess in a cat with 92 Diana A, Linta N, Cipone M, et al. Contrast-enhanced ultrasonogra-
diabetes mellitus. J Am Anim Hosp Assoc 2015; 51: 180–184. phy of the pancreas in healthy cats. BMC Vet Res 2015; 11: 64.
69 Boyden EA. The problem of the pancreatic bladder. Am J Anat 1925; DOI: 10.1186/s12917-015-0380-2.
36: 151–183. 93 Crain SK, Sharkey LC, Cordner AP, et al. Safety of ultrasound-guid-
70 Bailiff NL, Norris CR, Seguin B, et al. Pancreatolithiasis and pancre- ed fine-needle aspiration of the feline pancreas: a case-control
atic pseudobladder associated with pancreatitis in a cat. J Am Anim study. J Feline Med Surg 2015; 17: 858–863.
Hosp Assoc 2004; 40: 69–74. 94 Bjorneby JM and Kari S. Cytology of the pancreas. Vet Clin North Am
71 Jubb K. The pancreas. In: Jubb K, Kennedy P and NP (eds). Pathology Small Anim Pract 2002; 32: 1293–1312, vi.

Available online at jfms.com


Article reuse guidelines: sagepub.co.uk/journals-permissions
For reuse of images only, contact the author
JFMS CLINICAL PRACTICE 259

You might also like