DUAL-PHASE COMPUTED TOMOGRAPHIC ANGIOGRAPHY IN THREE DOGS WITH PANCREATIC INSULINOMA

DUAL-PHASE COMPUTED TOMOGRAPHIC ANGIOGRAPHY IN THREE

DOGS WITH PANCREATIC INSULINOMA

WILFRIED MAI, ANA V. CACERES

This article describes the findings in three dogs with histopathologically confirmed pancreatic insulinoma using

dual-phase computed tomographic angiography (CTA). In all three dogs, dual-phase CTA findings identified

lesions not seen on ultrasonography, including the actual identification of the primary pancreatic neoplasm in

two dogs. CTA findings were in agreement with the surgical and histopathological findings. In two dogs, the

insulinomas were found to have a strong enhancement during the arterial phase of the study but not at the other

phases, which stresses the importance of dual-phase computed tomography for the diagnosis of this type of

pancreatic neoplasia, in agreement with current knowledge in humans. Veterinary Radiology & Ultrasound,

Vol. 49, No. 2, 2008, pp 141–148.

Key words: computed, dog, dual-phase, insulinoma, pancreatic, tomography.

Introduction

INSULINOMA IS AN insulin-secreting tumor of the pancre-

atic b cells. Carcinomas account for 60% of pancreatic

b cells tumors, the remainder being adenomas; carcinomas

are regarded to be more frequently endocrinologically ac-

tive.1 Insulinomas are usually diagnosed in middle-age or

older dogs, with no gender predisposition. Insulinomas

are the most common of the three types of canine pancre-

atic endocrine tumor (insulinoma, gastrinoma, and gluca-

gonoma).2,3 Large breed dogs, such as Irish Setters,

Boxers, and German Shepherds are the most commonly

affected breeds, although insulinoma may occur in any

breed.1,2,4–12 The diagnosis of insulinoma is established

based on history and clinical signs, requires confirmation

of hypoglycemia with simultaneous hyperinsulinemia ob-

tained from the same blood sample, and identification of

a pancreatic mass by diagnostic imaging or exploratory

laparotomy. Different laboratory tests exist with various

sensitivities and specificities,1,2,7,9,11,13,14 but a definitive di-

agnosis of b-cell tumor is made only after histopathologic

evaluation of suspected neoplastic tissue.1,2,10,13 Although

medical therapy is an option,1,8 surgery potentially pro-

vides a cure in dogs with a completely resectable mass.10

A large proportion of dogs already have metastases at

the time of diagnosis, with common sites being regional

lymph nodes, the liver, the peripancreatic mesentery, and

omentum.12 Even when metastases are present, surgical

cytoreduction of locally invasive or metastasized tumors

frequently results in an improvement of clinical signs by

decreasing insulin secretion.1,2,9,10,13 Overall, dogs that

have surgery have significantly longer survival than dogs

given only medical therapy.1,10

Presurgical imaging is routinely used in humans with

pancreatic tumors to evaluate surgical respectability, pri-

marily with regard to vessels, lymph node metastasis and

hepatic metastasis. In particular, the location of the lesion

within the pancreas needs to be determined to assess

resectability and surgical prognosis. Computed tomogra-

phy (CT) has excellent reproducibility and overall accu-

racy.15–23 Dual-phase CT and magnetic resonance (MR)

imaging are superior to transabdominal ultrasonography

in the detection of insulinomas (94% for CT and MR

imaging vs. 64% for ultrasonography).24–26

In dogs, several imaging techniques have been used to

evaluate neoplastic and nonneoplastic pancreatic diseases,

including ultrasonography, CT, planar scintigraphy, and

single-photon emission CT (SPECT).3,27–32 Although

ultrasonography is the most widely available and used

technique to evaluate the pancreas in dogs, it is not very

accurate for the diagnosis of pancreatic insulinoma.3,31

There are few studies reporting on the use of CT to eval-

uate the pancreas in dogs.3,27,29,30,33 Only two studies re-

port on the use of CT for the diagnosis of insulinoma and

in the only patient series, 14 dogs, the sensitivity was 71%,

significantly better than ultrasonography and SPECT.3,29

In that series conventional pre- and postcontrast CT was

used.3 Since then, dual-phase CT angiography (CTA) tech-

niques have been developed,27,29 with promising applica-

tions for the diagnosis and differentiation of pancreatic

neuroendocrine tumors and pancreatic adenocarcinoma as

reported in humans.15,20 Recently, use of dynamic CTA for

the presurgical localization of a 34� 16mm pancreatic

insulinoma in a dog was reported.29

Address correspondence and reprint requests to Dr. WilfriedMai, at theabove address. E-mail: [email protected]

Received July 23, 2007; accepted for publication October 2, 2007.doi: 10.1111/j.1740-8261.2008.00340.x

From the Department of Clinical Studies (Section of Radiology), TheUniversity of Pennsylvania School of Veterinary Medicine, 3900 DelanceyStreet, Philadelphia, PA 19104-6010.

141

The purpose of this study was to describe the use of a

previously established dual-phase CTA protocol for the

presurgical diagnosis and staging of pancreatic insulinoma

in three dogs.

Methods

For all three dogs, the following dual-phase CT protocol

was used, in accordance with a previously published pro-

tocol established by our group.27 A third generation single-

slice helical CT unit� was used with 120 kVp and 160mA

settings and a tube rotation speed of 1 s.

Precontrast Series

� Five millimeter thickness with a pitch of 1.4 of theentire abdomen.

� Evaluation of the pancreas for size, shape, location,and attenuation.

Dynamic CT

� Single-slice cine angiography: A slice of interest waslocated on the precontrast series including the aorta,the portal vein, and the body of the pancreas. Thisslice was imaged repeatedly for 60 s at 1 image/s afterinjection of 185mg iodine/kg of nonionic iodinatedcontrast media (Iohexolw) using a power injector setat 5ml/s.

� A time attenuation curve was obtained from this se-ries after manually placing region of interests on theaorta and portal vein, to determine the optimal timewindow for the arterial and venous phase of thestudy. This curve was then used to calculate the timeof appearance, time to peak contrast enhancementand length of respective phases (arterial and venous)in each vessel as previously described.27

Dual-phase CT

� Collimation and pitch varied between animals: dog 1was scanned with 5mm slice thickness and a pitch of1.4, dog 2 was scanned with 2mm slice thickness anda pitch of 1.5, and dog 3 was scanned with 3mm slicethickness and a pitch of 1.0. Contrast media was in-jected using a power injector at 5ml/s at a dosage of814mg iodine/kg. The calculated time delays wereentered in the machine based on the results of the cineseries, with the arterial phase beginning at the calcu-lated aortic time of arrival and scanning in a caudal tocranial direction, covering the entire pancreatic body,

and as much of the pancreatic lobes as the arterialphase length would allow. The venous phase was ob-tained after the arterial phase in a cranial to caudaldirection covering the entire pancreas.

� If abnormal-appearing regions had been identified onthe precontrast series, it was made sure that theywould be included in the arterial phase of the pan-creatic CT angiogram.

Delayed CT Scan

� A delayed scan of the cranial and mid-abdomen wasobtained approximately 2–3min after the dual-phaseCTA using 5mm slice thickness and a pitch of 1.4.

Patient Material

Dog 1

An 8-year-old male intact Chesapeake Bay Retriever

had a 5-month history of weakness, ataxia, and seizures.

After the second episode of seizures, severe hypoglycemia

(35mg/dl, normal range [65–112mg/dl]) and inappropri-

ately elevated insulin levels (50.9mU/ml, normal range

[5–25mU/ml]) were detected. An abdominal ultrasound

was performed and was within normal limits. A dual-phase

CTA of the pancreas was performed (Fig. 1). A

1.3 � 1.5 cm nodule was seen at the caudal aspect of the

right pancreatic lobe on the precontrast series (Fig. 1A).

This nodule was very slightly hypoattenuating to the nor-

mal surrounding pancreas on precontrast series (40 vs.

50Hounsfield Units [HU], respectively), and had marked

contrast enhancement during the arterial phase of the study

where it enhanced more than the surrounding normal

pancreatic tissue (161 vs. 100HU, respectively, Fig. 1B).

At this phase, the nodule was very well defined and had a

regular margin. During the venous phase, the pancreatic

nodule was still enhancing more than the surrounding

pancreas but the difference was less (140 vs. 97HU, re-

spectively, Fig. 1C). During the delayed phase, the pan-

creatic nodule was isoattenuating to the rest of the

pancreas (Fig. 1D). No enlarged regional lymph node

was seen. At exploratory laparotomy a firm pancreatic

mass was found at the caudal extremity of the right lobe of

the pancreas. The mass was removed with a 2-cm surgical

margin. Three 4-mm nodules were found at the surface of

the liver and biopsied. They had not been identified on CT

or ultrasound. No abnormal lymph nodes were observed.

Histopathologic examination of the pancreatic mass con-

firmed the diagnosis of insulinoma with apparent complete

resection. The liver nodules were diagnosed as benign

hyperplastic nodules. The dog recovered uneventfully. Six

months after surgery, and being treated with prednisone,

the dog was clinically normal and normoglycemic.

�GE ProSpeed, General Electric Company, Milwaukee, WI.wOmnipaque 350 or Omnipaque 240, GE Healthcare, Princeton, NJ.

142 MAI and Ca¤ CERES 2008

Dog 2

A 6-year-old female intact Boxer had two episodes of

seizures that occurred after excitement and activity. The

dog was severely hypoglycemic at 12mg/dl. On abdominal

ultrasound, the area of the pancreas could not be fully

assessed due to the presence of intestinal gas, but no nodule

or mass was seen in the area of the pancreas. A 1.5 cm

hypoechoic lymph node was seen at the porta hepatis and

interpreted as an enlarged hepatic lymph node. Based on

these findings and the clinical history, an insulinoma was

strongly suspected and a dual-phase CTA was performed.

A well marginated and irregularly shaped 3.0 � 3.0 mass

was found in the mid-portion of the right pancreatic lobe

which was slightly hypoattenuating to the normal pancreas

on precontrast images (40 vs. 50HU, respectively), was

markedly hyperattenuating to the normal pancreas during

the arterial phase of the study (155 vs. 85HU, respectively)

and was still hyperattenuating (but to a lesser degree) to the

normal pancreas during the venous phase (125 vs. 95HU,

respectively) (Fig. 2A–C). During the delayed phase, the

pancreatic nodule was isoattenuating to the rest of the

pancreas (Fig. 2D). In addition to the pancreatic nodule, a

bilobed mass measuring 1.0 � 1.0 � 2.0 cm was found to

the right of the portal vein near the porta hepatis. It had the

same enhancement pattern as the pancreatic mass and was

believed to represent a metastatic lymph node (likely the

one seen on ultrasonography) (Fig. 3). During laparotomy,

a 3.0 � 3.0 � 1.0 cm mass was found in the midregion

of the right pancreatic lobe and was excised. A 1.0 �1.0 � 2.0 cm nodule was found more cranially within the

mesoduodenum just to the right of the portal vein and was

removed. Wedge biopsies of the liver and mesenteric lymph

nodes (all appearing grossly normal) were obtained. Histo-

pathologic diagnosis was malignant insulinoma, which

effaced much of the submitted portion of the organ and

extended into the adjacent adipose tissue. The nodular le-

sion in the mesoduodenum was a lymph node with almost

complete effacement by the tumor and extension of nests of

neoplastic cells into the adjacent mesentery. Abnormalities

consistent with steroid hepatopathy were seen in the liver

and no evidence of metastasis was seen in the mesenteric

lymph nodes biopsies. The patient was lost to follow-up

thereafter.

Fig. 1. Representative computed tomographic angiography images in dog 1, all at the level of the right pancreatic nodule (Window width: 246, Windowlevel: 101). (A) Precontrast image, (B) arterial phase, (C) venous phase, and (D) delayed phase. The pancreatic nodule is indicated by the arrow. Note the strongenhancement at the arterial phase. �, aorta; þ , caudal vena cava; LK, left kidney; S, spleen.

143CTA IN DOGS WITH PANCREATIC INSULINOMAVol. 49, No. 2

Dog 3

A 10-year-old male castrated Golden Retriever had

difficulty walking. Mild hypoglycemia was noted on the

screening biochemical profile and in a repeat test there was

severe hypoglycemia (19mg/dl) with associated hype-

rinsulinemia (133mU/ml), leading to the suspicion of insu-

linoma. Sonographically, a 1.0 � 1.3 cm hypoechoic oval

to round nodule was found in the left lobe of the pancreas,

while the right lobe could not be visualized well due to the

presence of gas in the intestinal tract. A 2.0 � 3.2 cm struc-

ture of mixed echogenicity was found within the lumen of

the splenic vein close to the abnormal areas of the left

pancreatic lobe. No blood flow could be detected within

the intraluminal structure with Doppler, and normal flow

in the splenic vein distal to that structure could be seen.

These findings were consistent with pancreatic mass and

splenic vein thrombosis most likely secondary to tumor

infiltration of the splenic vein. A dual-phase CTA was

performed to better assess the abdominal lesions. On the

precontrast series, an ill-defined isoattenuating thickening

of the left pancreatic lobe was noted (45HU), close to the

splenic vein, reaching 2.6 cm in thickness (Fig. 4A). This

area enhanced less during the arterial phase than the nor-

mal surrounding pancreatic tissue (80–100 vs. 130HU, re-

spectively, Fig. 4B), although some areas had more

enhancement than others (patchy pattern). During the ve-

nous phase and on the delayed series, this area was iso-

attenuating to the rest of the pancreas (Fig. 4C–D). A later

Fig. 2. Representative computed tomographic angiography images in dog 2, all at the level of the right pancreatic mass (Window width: 251, Window level:100). (A) Precontrast image, (B) arterial phase, (C) venous phase, and (D) delayed phase. The pancreatic mass is indicated by the arrow. Note the strongenhancement at the arterial phase. �, aorta, þ , caudal vena cava: # portal vein; RK, right kidney; S, spleen; L, liver.

Fig. 3. Computed tomographic image at the arterial phase in dog 2(Window width: 255, Window level: 67) demonstrating the mesenteric nod-ule (arrow) cranial to the pancreatic mass and corresponding to a lymphnode invaded by tumor cells with extension into the surrounding mesentery.�, aorta; þ , caudal vena cava; #, portal vein; RK, right kidney; S, spleen.


single-slice dynamic acquisition was repeated after the du-

al-phase and delayed study, with the slice centered on this

abnormal pancreatic area (image not shown) and there was

no evidence of enhancement of that area at the arterial

phase. The structure within the splenic vein was identified

on the precontrast series as a focal dilation of the vessel

which was hypoattenuating to the spleen (40 vs. 60HU

respectively) and isoattenuating to the pancreas (45HU);

some areas of that intraluminal structure did enhance

mildly during the arterial phase (72HU) and more during

the venous phase (129HU), where this structure created a

clear filling defect within the vein. The pancreatic mass was

seen wrapping around the splenic vein and invading the

lumen of the splenic vein through its caudal wall, commu-

nicating with the intraluminal structure (Fig. 5). In addi-

tion, a well-marginated oval-shaped structure measuring

Fig. 4. Representative computed tomographic angiography images in dog 3, all at the level of the left pancreatic mass (Window width: 350, Window level:50). (A) Precontrast image, (B) arterial phase, (C) venous phase, and (D) delayed phase. The pancreatic mass is indicated by the arrow. Dorsal to the pancreaticmass and the splenic artery there is an oval shaped structure corresponding to a metastatic lymph node. �, aorta; þ , caudal vena cava; RK, right kidney;S, spleen; St, stomach; LN, lymph node; SV, splenic vein.

Fig. 5. Close-up view of the splenic vein at the venous phase of the computed tomographic angiography (Window width: 500, Window level: 142) on twocontiguous slices. A large expansile filling defect (M) is seen in the splenic vein (SV). The pancreatic mass (P) is seen invading the splenic vein andcommunicating with the intraluminal filling defect. Dorsal to the splenic vein a metastatic lymph node (LN) is visible. S, spleen; RK, right kidney; �, aorta;þ ,caudal vena cava; #, portal vein.


2.0 � 3.5 � 4.1 cm was identified dorsal to the pancreatic

lesion and was interpreted as an enlarged splenic or pan-

creatic lymph node (Figs. 4 and 5). This lymph node was

hypoattenuating to the pancreas and to the spleen on pre-

contrast series (30HU for the lymph node vs. 60HU for

the spleen and 45HU for the pancreas), enhanced strongly

during the arterial phase (178HU), with mild homoge-

neous enhancement during the venous phase (133HU) and

delayed series (102HU). Several hypoattenuating round

nodules (5mm to 2 cm) were seen within the liver during

the venous phase, that had not been seen on ultrasound.

Based on these findings, an invasive insulinoma in the left

lobe of the pancreas with secondary invasion and throm-

bosis in the adjacent portion of the splenic vein and local

lymph node metastasis was suspected supporting the ul-

trasonographic findings. The liver nodules were felt to cor-

respond to either benign hyperplastic nodules or metastatic

disease. The CTA findings were confirmed at surgery: neo-

plastic tissue was found in the left pancreatic lobe with

local invasion of the splenic vein, and lymph node metas-

tasis. A left pancreatic lobectomy, splenectomy, and lymph

node removal was performed. On histopathologic examin-

ation, insulinoma was diagnosed within the pancreatic tis-

sue with evidence of extension within the adjacent

parenchyma. The lymph node architecture was effaced by

neoplastic cells. Recovery from surgery was uneventful but

the dog still had a few episodes of low blood glucose down

to 38mg/dl, which was suspicious for remaining insulinoma.

Two months after surgery the dog was clinically normal.

Discussion

Detection, classification, and staging of pancreatic neo-

plasms are a challenge for radiologists. In humans, mul-

tislice spiral CT examination with four to 16 detector rows

is now standard.19 In veterinary medicine, CT is not stan-

dard in the diagnosis and staging of pancreatic tumors, and

ultrasonography is the most widely used technique.28,31

Nonetheless, with the increasing availability of CT and the

increasing expertise and experience, CT is becoming more

commonly used for body imaging, and in particular for

pancreatic diseases.27,29,30,33 In comparison to ultrasono-

graphy, CT allows a full and thorough assessment of the

entire pancreas. Presence of gas in the digestive tract fre-

quently prevents assessment of the entire pancreas with

ultrasound, especially the left lobe. In addition, some areas

of the pancreas (left lobe and body in particular) can be

extremely difficult to image in larger dogs especially the

deep-chested dogs. Presence of intestinal gas is not an issue

with CT. With timed acquisition after injection of contrast

medium, CTA can allow delineation of vessels such as the

splenic and portal veins which may act as landmarks for

the pancreas.33 Although the pancreatic gland can be diffi-

cult to clearly delineate on CT images, for it is small and

isoattenuating to the surrounding organs, administration

of dilute barium sulfate might be useful, allowing clear

identification of key anatomic landmarks such as specific

portion of the gastro-intestinal tract. This has not been

investigated yet in veterinary medicine.

Ultrasonography is poorly sensitive for the diagnosis of

insulinomas in dogs: in a series of 16 pancreatic tumors

where 13 were insulinomas, the sensitivity of ultrasono-

graphy in detecting insulinomas was 69% but the sensitiv-

ity for the detection of hepatic or lymphatic metastasis was

only 44%.31 In 14 dogs with insulinomas, the sensitivity of

ultrasonography for the detection of the pancreatic tumor

was 35% and ultrasonography was negative in all five dogs

that had lymph node metastasis at surgery, and half of the

four dogs with liver metastasis.3

Conventional pre- and postcontrast CT is reported to

have a better sensitivity than ultrasonography and SPECT

in the diagnosis and staging of insulinoma in dogs, reach-

ing 71% for the primary and 40% for lymph node metas-

tasis.3 There is evidence in humans that dual-phase CTA is

superior to conventional CT scanning in the detection and

staging of insulinoma.19,20,34 Dual-phase CTA improves

the level of confidence, and improves the conspicuity of

small lesions. Owing to their highly vascular nature, a large

proportion of insulinomas (54–85%) are highly hyperat-

tenuating at the arterial phase of the study while having

only little enhancement at the venous phase.20,21,26 In ad-

dition, some lesions are conspicuous only at the arterial

phase and can be missed if that phase is not imaged.20 This

is a specific feature of insulinomas as opposed to other

types of pancreatic neoplasia which tend to be hypovas-

cular and therefore are hypoattenuating compared with the

normal surrounding pancreas at the parenchymal phase.34

We describe three dogs with confirmed insulinoma for

which we used our previously reported dual-phase CTA

protocol to accurately localize the primary lesion and as-

sess the presence of metastasis.27 In all three dogs there was

agreement between the dual-phase CTA findings and the

surgical findings, and histopathological examination con-

firmed the CTA suspicions in all three dogs with the ar-

terial and portal phases of the dual-phase study being

critical for complete identification of all lesions present.

Interestingly, in two of the three dogs (dogs 1 and 2) the

pancreatic insulinoma did enhance strongly at the arterial

phase of the study but less so at the venous phase. In both

dogs, the tumor was isoattenuating to the rest of the pan-

creas on the delayed series. This is in agreement with pre-

vious reports in humans and one anecdotal report in

animals.19,20,29,34 In dog 3 of our series, the pancreatic in-

sulinoma did not have strong enhancement at the arterial

phase as in dogs 1 and 2, although the metastasized lymph

node was characterized by enhancement patterns compa-

rable to that seen within the primary insulinoma in these

two dogs, with marked enhancement at the arterial phase


(178 vs. 130HU for the normal pancreas). Lack of arterial

enhancement in pancreatic insulinoma has also been re-

ported in people with up to 45% of pancreatic insulinomas

being hypo- to isoattenuating to the rest of the pancreas at

the arterial phase, and occasionally the tumor can be

hyperattenuating at the venous phase only.34 It is also

possible that the advanced stage of the disease in this dog

caused changes in the typical vascular pattern of early,

smaller insulinomas thereby explaining why the primary

tumor did not enhance as much as seen in dogs 1 and 2.

Another explanation would be that the arterial phase was

missed despite careful dynamic acquisition after test bolus

injection of contrast medium to determine the optimal time

windows. It is known that the pure arterial phase within

the pancreas is very short (5–6 s) and due to the length of

the organ, some of the pancreas is commonly not imaged

strictly during the arterial phase with single-slice helical CT

units.27 That being said, a later single slice dynamic acqui-

sition centered on the pancreatic mass was repeated in dog

3 after the dual-phase and delayed study, and did not

reveal enhancement of that area at the arterial phase,

indicating that the pancreatic lesion was truly not hyper-

attenuating at the arterial phase. False negative findings are

possible though, and to prevent this it is recommended to

always include abnormal pancreatic areas in the region that

will be imaged during the arterial phase. With multislice

CT imaging, it would be easier to image the entire pancreas

during the arterial phase as acquisition times are faster.16–18

Some groups have suggested that standardized acquisition

times can be used to image the arterial and parenchymal

(venous) phases in dogs based on determination of average

time-to-peak enhancement.29 We believe that a test bolus

method is preferable as there is normal variation between

dogs as far as the time-to-peak enhancement of various

structures: these values depend on the size of the dog, the

rate of the injection, the site of the injection and hemody-

namic parameters. For example, the time-to-peak enhance-

ment of the aorta in dog 2 was 12 s and it was 30 s in dog 3.

Applying a systematic arterial phase acquisition delay

would not have been adequate in dog 3 to image the pure

arterial phase.29

In all of our three dogs, dual-phase CTA allowed iden-

tification of additional lesions to the ones seen on ultra-

sound. In 2 dogs (dogs 1 and 2) the actual pancreatic

nodule was not seen sonographically, and only partially in

the third dog (dog 3). Lymph node metastasis was only

identified on ultrasound in one of two affected dogs (dog

2), but were seen on CT in both dogs. In dog 3, CT allowed

identification of the structure within the splenic vein seen

on ultrasound as local extension of pancreatic neoplasia as

opposed to thrombosis.

The dosage of contrast medium we used is high (814mg

iodine/kg, in addition to 185mg iodine/kg for the dynamic

part of the study). Although this dosage is still lower than

what is considered to be a dose at risk for causing contrast-

induced renal failure in humans and contrast-induced renal

failure is rare in animals, it is possible that with increased

use of angio-CT, that contrast-induced renal failure may

become a concern in animals.35 It might be possible to

reduce the dose of contrast medium for CTA to what is

more commonly used for CT (approximately 480–600mg

iodine/kg): further studies to determine the effect of

reducing the dosage of contrast media on the quality of

contrast enhancement of the vessels are warranted.

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DUAL-PHASE COMPUTED TOMOGRAPHIC ANGIOGRAPHY IN THREE DOGS WITH PANCREATIC INSULINOMA