ULTRASONOGRAPHIC AND CLINICOPATHOLOGIC FINDINGS IN 21 DOGS WITH INTESTINAL ADENOCARCINOMA

ULTRASONOGRAPHIC AND CLINICOPATHOLOGIC FINDINGS IN 2 1 DOGS WITH INTESTINAL ADENOCARCINOMA

MELISSA C. PAOLONI, DVM, DOMINIQUE G. PENNINCK, DVM, DVSc, ANTONY S. MOORE, BVSc, MVSc

In a retrospective study of 21 dogs with intestinal adenocarcinoma, the signalment, clinical presentation, laboratory findings, ultrasonographic features, treatment, and outcome were reviewed. Anorexia (n = 16), vomiting (n = 15), diarrhea (n = lo), and weight loss (n = 9) were the most common clinical signs reported. Ultrasonographic features that were evaluated included location, length, wall thickness, echogenicity, regional motility, layering, regional lymphadenopathy, and fluid accumulation proximal to the lesion site. All lesions were transmural and associated with complete loss of wall layering. Maximum wall thickening at the lesion site ranged from 7 to 17 mm (median 12 mm, mean 11.9 mm). Most of the dogs had a lesion measuring from 23 to 63 mm in length, (median 40 mm, mean 42 mm). Most intestinal lesions were poorly echogenic and had an irregular lumen. Fluid accumulation proximal to the lesion site was identified in 17 of 21 dogs, and in 13 of 17 dogs the fluid accumulation was considered moderate to severe. Regional lymphadenopathy and/or nodular mesentery/omentum were noted in 12 of 21 dogs. The tumor was located in small intestine for 15 dogs and in the colon for the remaining 6 dogs. Fifteen dogs were treated by surgical resection of the intestinal mass. Their median survival time was 233 days. Only gender appeared to influence survival. Female dogs lived a median of 28 days, whereas male dogs lived a median of 272 days. Veterinav Radiology & Ultrasound, Vol. 43, No. 6, 2002, p p 562-567.

Introduction

Primary intestinal neoplasms are uncommon in dogs,’-3 and intestinal adenocarcinoma represents approximately 0.3% of all canine neoplasms.’ Adenocarcinoma and lymphoma are the most common primary gastrointestinal malignancies in the dog, although lymphoma is most often associated with systemic di~ease.’,~ Other malignancies described in the canine intestinal tract include leiomyosarco- ma, fibrosarcoma, poorly differentiated sarcoma, mast cell tumors, carcinoid, and osteosar~oma.”~ Benign tumors reported to occur in the canine intestinal tract include polyps and leiomyomas.

The large intestine is believed to be the most common location of primary intestinal neoplasia in the dog,’.* and adenocarcinoma has been reported in both the small and large in t e~ t ine .~” -~

There is no confirmed breed predisposition for intestinal adenocarcinoma in the dog, even though the collie and Ger- man Shepherd have been reported to be predisposed.’ Males are reported to be more frequently affected by intestinal adenocarcinoma than females.’-s Older dogs appear to be

From the Department of Clinical Sciences Tufts University School of Veterinary Medicine.

Address correspondence and reprint requests to Dominique Penninck, Tufts University School of Veterinary Medicine, 200 Westboro Road North, Grafton, MA 01536.

Received November 13, 2001; accepted for publication February 27, 2002

most commonly affected, although the ages of affected dogs range from 1 to 14 years of age.637

Common clinical signs in dogs with intestinal carcinoma include anorexia, weight loss, vomiting, diarrhea, hematochezia, and tenesmus.’,’-s The clinical signs are often correlated with tumor l ~ c a t i o n . ~ For example, vomiting is usually associated with proximal intestinal lesions, weight loss with jejunal lesions, whereas tenesmus, hematochezia and constipation are often associated with distal large bowel or rectal tumors. ‘A’ Anemia associated both with chronic disease and gastrointestinal tract bleeding is a common finding in dogs with adenocarcinoma. ”’ Intestinal masses can be difficult to palpate in the dog, and the detection rate depends on the size and location of the lesion and the experience of the examiner. Rectal examination has been reported to be useful in detecting a mass or stricture in 60% of dogs with colorectal adenoca r~ inomas .~~’~~

Because clinical signs are often nonspecific and diagnosis is often made late in the course of the disease, more than 40% of dogs have clinically detectable metastases at the time of diagnosis.’ The most common site for metastasis is regional lymph nodes, although metastases also occur in the mesentery and omentum.’-s Metastases to the lungs, spleen, kidneys, pancreas, bladder, testis, and urethra are are.^,','^) Metastases from colorectal adenocarcinomas are suspected to be less common than from small intestinal adenocarci- noma9

Little information on prognostic indicators for dogs with

562

VOL. 43, No. 6 INTESTINAL ADENOCARCINOMA 563

intestinal adenocarcinoma is available. In one study, median survival time for dogs with histologic evidence of metastasis at diagnosis was approximately 3 months, and the 1-year survival rate was 20%.' For dogs without evidence of metastasis, the median survival time was 10 months, and the 1-year survival rate was 40.9%.' Local excision had a positive effect on survival in dogs with colorectal adenocarcinoma, with an average survival time of 22 months, although local recurrence was seen in 50% of the dogs.'

Radiography, contrast studies, and ultrasonography are common diagnostic imaging methods used to evaluate canine intestinal Survey radiographs can be suggestive of obstruction, showing dilatation of the bowel proximal to the annular, stenotic lesions, which often char- acterize intestinal car~inornas.'~' Contrast radiography pro- vides additional information in the detection of annular or intraluminal lesions within the intestinal tract, because they more precisely outline the narrowing of the lumen at the tumor site. I ' Ultrasonography is presently considered to be the most effective means of diagnosing intestinal tumors in dogs and appears to be useful in evaluating mural lesions, gastrointestinal motility, and associated abdominal changes such as lymphadenopathy. I 2 - l 6 Ultrasonographic features of gastrointestinal tumors often include transmural wall thickening with complete loss of the normal wall layering. Re- ports on specific ultrasonographic features of most commonly encountered gastrointestinal tumors in small ani- m a l ~ ~ ~ - ~ ~ and in are available.

The main goal of this retrospective study was to review the signalment, clinical presentation, laboratory findings, ultrasonographic features, treatment, and outcome in 2 1 dogs with histologically proven intestinal adenocarcinoma.

Materials and Methods

The medical records of 21 dogs admitted to Tufts Uni- versity School of Veterinary Medicine (TUSVM) between January 1990 and January 2000 were reviewed. All dogs with histopathologic diagnosis of intestinal adenocarcinoma, and having been ultrasonographically evaluated, were included in this study. Signalment, history, physical examination findings, laboratory data, radiographic findings, and histopathologic diagnosis were evaluated along with ultrasonographic findings. Metastatic sites, treatment, and response to treatment were also recorded. Clinical follow-up data were available for all patients. Local veterinar- ians or owners were contacted for follow-up information when necessary.

Abdominal ultrasonographic examination was performed in all dogs by using a real-time scanner with a 5-, 7 . 5 , and/or 1 0-MHz sectorial transducer.* All videotapes and hard copies (printed with use of multiformat camera) were

*Advanced Technology Laboratories, Inc., Bothell, WA 9804 I

reviewed retrospectively. Each intestinal lesion was evaluated for location, length, maximum wall thickness, wall layering, echogenicity, lymph node size and appearance, regional intestinal motility, and the presence of fluid proximal to the lesion. In this study, wall thickness was considered abnormal if exceeding 4 mm for jejunum, ileum, and large bowel segment, and exceeding 5 mm for the duode- num. Wall echogenicity was considered as diffusely decreased (hypoechoic), diffusely increased (hyperechoic), or mixed (not uniform echotexture). Motility was subjectively assessed as normal, decreased or increased. The degree of fluid accumulation proximal to and/or at the lesion site was subjectively classified as mild, moderate, or severe. Other abdominal abnormalities suggestive of metastases were also noted. Ultrasonographic findings were then correlated to the histopathologic results obtained by ultrasound-guided fine- needle aspiration or biopsy, or by surgical biopsy. The ultrasound-guided fine-needle aspirates were performed by using a 22- or a 20-gauge spinal needle. The ultrasound- guided core biopsies were obtained by using a automated biopsy gun with an 18-gauge Tru-Cut biopsy needle. The ultrasound-guided aspirate and/or biopsies were performed on the intestinal lesion and/or the enlarged lymph nodes. In most dogs, two samples were obtained at each target site.

Of the 21 dogs, 2 dogs were euthanized at the time of surgery because of the presence of an unresectable tumor. Four other dogs were not treated and were euthanized at the time of diagnosis. Fifteen dogs were treated with curative intent by resection of the intestinal tumor. Kaplan-Meier survival statistics? were used to estimate the survival period from surgery to death for any reason in these 15 dogs. Dogs were censored from survival analysis if they were still alive at the end of the study period. Cox forward conditional regression analysis? was used to estimate the effect of the following variables on survival: laboratory values before surgery measured as dichotomous outcomes (normal vs. low or high) including hematocrit (<37% vs. >37%; normal range 37-55%), serum K (normal range 3.8-5.4 mEq/L), Na (normal range 140-151 mEq/L), C1 (normal range 105-120 mEq/L), Ca (normal range 8.8-11 mg/dL), bilirubin (normal range 0.1-0.5 mg/dL), albumin (normal range 3 4 . 2 g/dL), creatinine (normal range (0.5-1.5 mgldL), blood urea nitrogen (normal range 8-33 mg/dL), and amylase (normal range 400-1200 U/L); gender, lesion length, and thickness as measured by ultrasonography, small vs. large intestinal location; clinical signs reported by the owner before surgery of vomiting, diarrhea, weight loss, lethargy, melena, pain, or anorexia; physical findings of abdominal distension or presence of a palpable abdominal mass; presence of regional lymphadenopathy on abdominal ultrasonography; presence of metastases or presence of tumor at surgical margins.

1-SPSS statistics: SPSS Tnc., Chicago, Illinois.

5 64 PAOLONI ET AL. 2002

Results

The age of the 21 dogs ranged from 6 to 14 years with a median of 1 1 years (mean of 10 years). Sixteen dogs were male (9 of 16 neutered), and five were neutered females. Dogs of 14 breeds were included. Four dogs were Golden retrievers; the other breeds represented by more than one dog were mixed breed (n = 3), Lhasa Apso (n = 2), and cocker spaniel (n = 2).

Fifteen dogs had small intestinal neoplasms, and six had large intestinal neoplasms. Six dogs had confirmed jejunal lesions. Of the six dogs with adenocarcinoma of the large intestine, two were confirmed as colonic in origin and two as colorectal. Anorexia fn = 16), vomiting (n = 1 3 , diarrhea (n = lo), and weight loss (n = 9) were the most common clinical signs reported. Of those 15 dogs presented with vomiting, 12 had a small intestinal lesion. Of nine dogs experiencing weight loss, seven had a small intestinal neo- plasm. Six dogs were lethargic. Tenesmus or constipation was reported in two dogs, one of which had a large intestinal lesion. Melena was reported in one dog that had a duodenal tumor. Change in fecal size was seen in one dog with a colonic adenocarcinoma, whereas ascites was reported in one dog with a duodenal carcinoma. On physical examination, all dogs were alert and responsive. A palpable abdominal mass was detected in four dogs, whereas rectal examination revealed a palpable mass in two dogs with colonic or colorectal adenocarcinoma, both of which had rectal bleeding. All dogs had a CBC and a serum biochemical profile performed. Anemia was detected in seven dogs with a median PCV of35% (mean 33%). One of these seven dogs had melena. Hypoalbuminemia (normal range 3-4.2 g/dL) was noted in six dogs. Liver enzyme elevations including alka- line phosphatase (ALP; normal range 20-320 U/L) (7 dogs), alanine transferase (ALT; normal range 10-95 U/L) (3 dogs), or aspartate transferase (AST; normal range 15-52 U/L) ( 5 dogs) were detected in 10 dogs. Two dogs were azotemic (normal creatinine range 0.5-1 .5 mg/dL). Electro- lyte disturbances attributable to gastrointestinal losses (decreased Na, C1, K) were observed in five dogs. Hypocalce- mia was evident in eight dogs but corrected to normal in five hypoalbuminemic dogs. Amylase elevations (normal range 400-1200 U/L) were documented in six dogs.

Thoracic radiographs were obtained for 9 of 21 dogs. No pulmonary metastases were seen on thoracic radiographs made at presentation in any of the dogs. One dog had evidence of mild bilateral pleural effusion. Abdominal radiographs were obtained for 9 of 21 dogs, and abdominal masses were detected in 3 dogs; the radiographic findings were supportive of intestinal obstruction in 6 dogs. Dilated bowel segments proximal to the obstruction site and the accumulation of mineralized ingested fragments at the lesion site were radiographic features suggestive of intestinal obstruction. In six of nine dogs, there was evidence of mod-

erate to severe fluid accumulation in the intestinal tract. One dog with duodenal adenocarcinoma had delayed gastric emptying, and one dog with colorectal tumor had no significant abnormalities on survey radiographs.

Histopathologic diagnosis was obtained by surgical (n =

18) or ultrasound-guided fine-needle aspirate or biopsy (n = 5) of the bowel lesion and/or the enlarged adjacent lymph nodes. The ultrasound-guided procedures were performed in 6 of the 21 dogs but was diagnostic in 5 of the 6 dogs. For each dog, a combination of two fine-needle aspirate and/or core biopsy of the bowel lesion and/or enlarged lymph node provided a positive diagnosis. In one dog with cecal mass, a single sample was obtained from the lesion by using a 22-gauge spinal needle. This sample was considered nondiagnostic.

Of the 21 dogs, 6 dogs were euthanized. Surgery was performed with curative intent in the remaining 15 dogs. One dog with a concurrent pheochromocytoma died imme- diately after surgery.

Chemotherapy was combined with surgical excision in 2 of the 15 dogs. One dog received three treatments of doxorubicin every 3 weeks and one dose of carboplatin. This patient experienced neutropenia after doxorubicin, as well as vomiting and lethargy after carboplatin. The second dog was treated with multiple chemotherapeutic protocols over a 26-month period. Chemotherapeutic agents included doxorubicin, methoxymorpholino-doxorubicin, carboplatin, and 9-aminocamptothecin. This dog had confirmed lymph node metastases that regressed with doxorubicin treatment. Both dogs survived more than 17 months from surgical resection.

In one dog, the intestinal lesion was not observed in the initial ultrasonography but was noted on retrospective review of the videotape (dog #17). Length of lesion was estimated as accurately as possible (Fig. 1 ). Twenty dogs had

FIG. 1. Longitudinal sonogram of a jejunal tubular secreting adenocarcinoma. On this picture. the lesion measured 2.85 cm in length (between calipers). The maximum length measured wa5 3.5 cm. During the real-time examination, the identification of normal wall layering (D) adjacent to the lesion assisted placement of calipers to assess the length of the lesion.


a lesion measuring from 23 to 63 mm in length (median of 40 mm, mean 42 mm); in one dog (dog # I ) the lesion length was underestimated because of interference with the pelvis. Wall thickness ranged from 7 to 17 mm, with a median wall thickness of 12 mm (mean 11.9 mm). The observed ultrasonographic pattern of the intestinal wall was considered hypoechoic in 14 of 21 dogs and mixed in 7 of 21 dogs. In these seven dogs, the background echogenicity was considered decreased, but the presence of inhomogeneous echoes prevented classification of them as hypoechoic. Regional lymphadenopathy (10 of 21) and/or mesenteric nodules (4 of 2 1 ) were found by ultrasonography in a total of 12 of 2 1 dogs (Fig. 2). Lymph node size ranged from 8 to 48 mm in thickness, with a mean size of 27 mm (median 30 mm). Lymph nodes identified were mesenteric, hypogastric, and medial iliac. Four dogs had a hypoechoic, nodular appearance to the mesentery of omentum, which was suggestive of local metastasis.

Intestinal motility could be assessed in seventeen of the 21 dogs. Motility was reduced locally in 14 of 17 dogs and increased in 3 of 17 dogs. Normal peristaltic activity was observed in one dog, and in four dogs motility could not be adequately assessed. The bowel in 15 of 21 dogs had an irregular lumen. Fluid accumulation proximal to the tumor was recognized in 17 of 21 dogs (Fig. 3). Fluid accumulation was described as mild (4 of 2 I ), moderate (8 of 2 I ), or severe ( 5 of 21). There was no evidence of fluid accumulation proximal to the lesion in four dogs.

Evidence of regional lymphatic metastasis, including ei- ther metastases to lymph nodes (n = 9) or evidence of mucosal angiolymphatic invasion (n = 5 ) or both, was found in 1 1 of 21 dogs at histopathologic review. Of these 11 dogs, 7 had recorded lymphadenopathy on abdominal ultrasound. A total of eight dogs had visceral metastases. One dog had liver metastases, one had splenic metastases,

FIG. 2. Transverse sonogram of an intestinal adenocarcinoma (GI). Transmural thickening ( I cm) with complete loss of layering can be seen. An adjacent enlarged and poorly echogenic mesenteric lymph node (4 cm in thickness) is also present (LN). The lumen of the thickened bowel segment is seen as a bright interface.

FIG. 3. Longitudinal sonogram of an intestinal adenocarcinoma. Marked fluid accumulation (F) was noted proximal to the lesion. The lesion length was estimated at 4.2 cm (black arrows). Transmural thickening (1.4 cm) with complete loss of layering was present. On this static image, the thickened wall is difficult to distinguish from the echogenic intraluminal fluid. The demarcation was better assessed during real-time evaluation.

and four had metastases to the mesentery or omentum. One dog had abdominal carcinomatosis at necropsy.

Of the 15 dogs treated with surgery, 2 dogs were alive 300 and 365 days after surgery. These latter two dogs were censored in survival analysis. Median survival time for all 15 dogs was 233 days (range 5-784 days, mean 267 days). Gender was the only variable having a significant relation- ship with survival ( P = 0.012). Three female dogs lived a median of 28 days after surgery (range 5-55, mean 29 days), whereas 12 male dogs lived a median of 272 days (range 14-784, mean 326 days).

Discussion

In our study, as in other reported there were more male dogs with intestinal adenocarcinoma. Reasons for this gender predilection are unknown. It is of interest that male dogs were more likely to live longer after surgery than were female dogs; however, numbers are small and the meaning of this finding should be investigated in future studies.

The results of our study are also consistent with the lit- erature in correlating the location of the primary lesion with the patient’s presenting clinical signs. According to our study, vomiting and weight loss were common in dogs with small intestinal neoplasms. Rectal bleeding and hematochezia were seen in dogs with large bowel adenocarcinoma.

Fifteen dogs in our study had small intestinal adenocarcinoma, and 6 of these had a confirmed jejunal lesion. This finding is most likely the result of our patient selection because only the dogs with confirmed intestinal carcinoma, which had been ultrasonographically evaluated, were included. Many dogs with rectal or distal colonic tumors may

566 PAOLONI ET AL. 2002

not have an ultrasound examination, because the lesion is too distal to be imaged fully.

Abdominal radiographs provided useful information in eight of nine dogs; however, they provided very little mor- phologic information on the intestinal lesion. The radiographs yielded no information on the likelihood of the spread of disease within the abdomen. Even though thoracic radiographs are included as part of a general health screen, it is very uncommon to detect pulmonary metastases associated with intestinal adenocarcinoma, as was observed in our study.

Ultrasonography has been described as the most effective and least invasive diagnostic modality available in small animals to detect gastrointestinal tumors. 172’8,20 Several in- vestigators have been studying the ultrasonographic features of specific tumor types and have indicated that some of these features may be indicative of particular tumor type. Canine gastric carcinomas have been reported to appear as a transmural thickening of the stomach associated with a distinctive pattern of p~eudolayering.’~ In latter study, regional lymphadenopathy was characterized in 25% of patients by a “target”-like appearance with a poorly echogenic rim and a highly echogenic center.I7 Similarly, leiomyosar- comas have been reported to have a distinctive ultrasonographic appearance of eccentric growth and lack of regional lymphadenopathy.” When the lesion exceeds 4 cm in over- all diameter, the presence of poorly echogenic cavities is common. Transmural circumferential thickening with complete loss of layering, associated with moderate to severe regional lymphadenopathy, has been reported in feline and canine lymphoma.”~20 Transmural thickening with the loss of normal gastrointestinal wall layering and local lymphadenopathy has also been described in both feline and canine intestinal adenocarcinomas.2”22 In a study of five cats with intestinal carcinoma, the ultrasonographic features of the intestinal lesion were reported as transmural thickening of the wall with complete loss of layering in all cats.” In that series, the thickening was considered circumferentially symmetric and hypoechoic in one cat, whereas it was described as being asymmetric and of mixed echogenicity in three cats and symmetric with mixed echogenicity in the last cat. Hepatic metastases were noted, but there was no men-

tion of detected regional lymphadenopathy.21 In all dogs of our study, the lesion appeared as transmural, marked thickening of the intestinal wall with complete loss of layering. Unlike the reported pseudolayered sign in canine gastric carcinoma, the intestinal carcinomas in our study had a diffusely poorly echogenic appearance in most dogs.

Acinar, solid, and mucinous adenocarcinomas have been reported to average 4 cm in length.* It is interesting that in our study, most of the intestinal carcinoma (17 of 21) were less than 6 cm in length, and the maximum length was 7 cm. Most of the articles describing the ultrasonographic appearance of intestinal carcinomas have not reported the length of the lesion. The main reason may be the difficulty in measuring the length of a tubular lesion by using a sectorial probe. However, because the length of some tumors may vary significantly (i.e., carcinoma vs. lymphoma), this additional feature could contribute in distinguishing between different tumor types.

In addition, moderate to severe fluid accumulation in bowel proximal to the lesion site was noted on ultrasound in 13 dogs, and mild fluid accumulation was present in 4 dogs. Moderate to severe (localized) fluid accumulation is highly suggestive of intestinal obstruction (as confirmed radio- graphically in six of nine dogs with abdominal radiographs available). This finding supports the annular constrictive nature of some intestinal adenocarcinomas. In two reports on ultrasonographic features of feline alimentary lymphoma in cats (total of 33 cats), there was no mention of ultrasonographic features suggestive of obstruction at the lesion(s)

Ultrasonography identified regional lymphadenopathy and/or nodules in the mesentery/omentum in 12 dogs. The identification of regional lymphadenopathy or omental/ mesenteric nodules is very helpful in staging intestinal tumors that may provide prognostic information before interventional procedures.

Ultrasonography is also a valuable tool to safely guide biopsy of intestinal masses, as well as enlarged lymph nodes and other visceral sites for tumor diagnosis and clinical ~ t a g i n g . ~ ~ - ~ ’ In our study, ultrasound-guided fine-needle aspirate, and/or biopsy was successfully performed in five of six dogs that underwent this procedure.

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ULTRASONOGRAPHIC AND CLINICOPATHOLOGIC FINDINGS IN 21 DOGS WITH INTESTINAL ADENOCARCINOMA

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