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Ultrasonography of the in small animals

Examination techniques Ideally, the patient should be fasted overnight to reduce the interference with gastric contents and intraluminal gas. However, non-fasted dogs may show adequate image quality. The intra-luminal gas causes imaging artifacts, such as reverberation, comet tail and acoustic shadowing. Sedation is not usually necessary, but when needed, xylazine Amalia Agut, DVM, PhD, Dipl. ECVDI should be avoided because it causes gastric stasis The Veterinary Faculty, Department of Medicine leading to massive gaseous distension (1). and Animal Surgery, University of Murcia, Spain In 1981 Dr. Agut graduated from the University of The animal is typically placed in dorsal recumb- Zaragoza in Spain and obtained her PhD in 1984. ency, although the position may depend on the She joined the University of Murcia in 1985 and is patient’s restlessness, discomfort, or on the operat- currently Lecturer in Radiology. She received her Diploma in the European College of Veterinary or’s preferences. The examination with the patient Diagnostic Imaging (ECVD) in 1998. Dr. Agut’s main standing, or via a hole in the supporting table, the interests lie in the fields of ultrasound in small recumbent side is useful. This makes use of the animals. intraluminal fluid gravitating to the dependent wall of the or intestinal tract where it serves as an acoustic window (2).

KEY POINTS Five MHz, 7.5 MHz or higher frequency transducers ± Ultrasound examination of the small intestine has are used, with higher frequency transducers offer- become routine in investigation of the intestinal ing the best resolution of bowel wall layers (1,2). diseases Transducers with small footprint are useful to ± The principal limitation of intestinal tract ultrasound is evaluate the proximal when the probe the presence of luminal gas must be placed below the rib cage or between ribs (2). ± Radiographs should precede the ultrasound examination to evaluate the amount, location and pattern of intestinal gas Ultrasonographic anatomy ± Ultrasound examination can provide information of of the small intestine bowel wall thickness, layering of the wall, , The duodenum is located in the right side of the and luminal contents abdomen, beginning from between the last ribs and then followed distally along the right body wall. The other portions of small bowel are assessed moving the transducer from right to left and left to

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Figure 1. Figure 2. Ultrasonographic layers of the intestinal wall. Ultrasound image of the ileocolic junction of a cat. s (), m (musculature).

right, and then from cranial to caudal to image the Wall thickness entire small intestinal tract. Sections of small The thickness of the bowel wall is measured intestine will be viewed sagittally, transversely and between the outer echogenic serosal surface and in various oblique images, depending on the trans- the mucosal-luminal interface (Figure 1). In dogs, ducer and intestinal tract position (2). The the intestinal wall is between 2-6 mm thick depend- can be identified by its location in the right mid-to ing on the size of the dog and part of the small cranial abdomen and its relationship with the bowel (Table 1 and 2) (5), while in cats a mean and . In the intestinal tract of 2 mm thick has been evaluated (Table 1) (6). wall layers, wall thickness, peristalsis, and luminal contents must be assessed (1). Luminal patterns The ultrasonographic appearance of the small Layers of the bowel wall intestine depends on the type and amount of lumin- Five ultrasonographic layers can be identified al content (Figure 3). When empty, a “mucous in the small bowel, corresponding from the pattern” is present, the bowel lumen appears as a lumen outward, to the luminal/mucosal interface, hyperechoic core ("mucosal stripe") surrounded mucosa, submucosa, muscular, and the serosa layer by a hypoechoic halo of the bowel wall. This (Figure 1). The mucosa and muscular layers are hyperechoic core represents and small air hypoechoic, whereas mucosal surface, submucosa bubbles trapped at the mucosal-luminal interface. and serosa are hyperechoic (3). The mucosal layer When fluid is present in the bowel lumen (“fluid is the thickest layer of the intestinal wall. The ileum pattern”), an anechoic area is seen between the in cats can be identified by a thicker echogenic walls of the bowel that appears tubular in long axis and irregular submucosal layer (Figure 2) (4). views, and circular in short axis views. Gas-filled

Table 1. Table 2. Normal range of wall thickness for different Normal range of wall thickness (mm) for the segments of the intestinal tract in cats (4) and different segments of the intestinal tract in dogs dogs (2) based on body weight (5)

Wall thickness Cats Dogs Body weight Duodenum Body (mm) (kg) weight (kg) Duodenum 2.0 - 2.4 3 - 6 < 20 < 5.1 < 20 < 4.1 Jejunum 2.1 - 2.5 2 - 5 20 - 29.9 < 5.3 20 - 39.9 < 4.4 Ileum 2.5 - 3.2 2 - 4 > 30 < 6 > 40 < 4.7

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A A

B B

Figure 3. Figure 4. Luminal Patterns: A.- Longitudinal sonogram of a normal duo- A.- Transverse and B.- Longitudinal sonogram of a jejunal denum. The mucous (m) and gas (g) patterns can be observed. intussusception in a 5-year old German Shepherd. The hypo- B.- Transverse sonogram of jejunum segments. Fluid pattern is echoic and hyperechoic rings with hyperechoic center (Fat) is noted. consistent with intussusceptions.

small intestinal loops cause a highly echogenic within the jejunum, ileocolic or ileocecal junctions interface with distal acoustic shadowing or reverb- or within the colon (colocolic) and rarely do they eration (“gas pattern”) (7). involve the stomach or duodenum. They often occur in puppies and kittens secondary to primary Peristalsis intestinal disease such as enteritis from intestinal The mean number of peristaltic contractions parasites, bacterial or viral infections. In older observed in the proximal duodenum is four to patients, the intussusceptions can occur close to five per minute and two contractions per minute pseudocysts, enlarged lymph nodes, foreign bodies in the jejunum and ileum (7). or tumoral mass (2).

Ultrasonographic patterns of Intussusceptions have a characteristic ultrasound small intestinal diseases appearance that in most cases allows a definitive Intussusception diagnosis to be made with confidence (8). Intussusception is the invagination of a portion of the intestine, called intussusceptum, into the The most common sonographic pattern observed in lumen of an adjacent segment of intestine, called transverse sections of the bowel is a target-like mass intussuscipiens. Intussusceptions usually occur consisting of multiple hyperechoic and hypoechoic

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ULTRASONOGRAPHY OF THE SMALL INTESTINE IN SMALL ANIMALS

A

Figure 6. The linear foreign body appears as a bright linear interface in the bowel lumen (arrow).

with irreducible intussusceptions (10). However, the recognition of blood flow in the intussuscepted bowel using color flow Doppler ultrasonography appears to be the most valuable factor for predict- B ing bowel reducibility (10).

Figure 5. Foreign bodies Intestinal foreign bodies. A.- A rubber teat is in the lumen of a In small animals, foreign bodies are the main cause bowel loop as two ovoid echogenic lines (arrows). B.- A peach pit of mechanical obstruction. A distension of the small is in the lumen of the bowel, as curved interface with small intestine with fluid, gas, or a combination of both, is protuberances associated with strong acoustic shadowing. an indicator of mechanical ileus (obstruction). The degree of bowel distension depends on whether the obstruction is partial or complete, on the duration and the location of the obstruction. When the entire concentric rings around a hyperechoic center that small intestine is dilated, it is important to different- represents the entrapped (Figures 4A iate diffuse intestinal disease (e.g., parvovirus and 4B). In longitudinal sections, multiple hyper- infection) from a distal small bowel obstruction. echoic and hypoechoic parallel lines are usually Visualizing a small portion of normal, non-distend- visible. Ultrasonographic patterns may vary with ed small bowel (distal to the obstruction) is a clue the length of bowel involved, the duration of the that a distal obstruction is present (1). process, and the orientation of the scan plane in relation to the axis of the intussusception (9). So, Some foreign bodies like balls or rocks are easily in some instances the concentric or layered appear- identified by ultrasonography because of their ance is distorted and not as easily recognized characteristic shape and the presence of acoustic because of inflammation and edema. The presence shadowing. However, the balls may vary in echo- of a thin, external hypoechoic ring of the target-like genicity, depending on their physical properties mass is usually associated with reducible intus- (Figure 5A). Most of foreign bodies produce a susceptions. The appearance of fluid within the bright interface associated with strong shadowing. apex of the intussusceptions, absence of peristaltic Occasionally, the contour of the interface can activity of the bowel, and enlarged lymph nodes help identifying the type of foreign body in the in the intussuscepted intestine are compatible intestine (Figure 5B) (2).

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The ultrasonographic appearance of the perforated The presence of gastrointestinal parasites can mimic bowel wall by foreign bodies, such as sticks, is a the appearance of a linear foreign body (7,12). local thickening and focal loss of layers. Moreover, The ultrasonographic pattern of a gastrointestinal bright mesenteric fat, peritoneal effusion, free roundworm is a hyperechoic linear nonshadowing gas in the abdomen, fluid-filled intestines and structure with a hypoechoic center (13). reduced motility may be present, associated with perforation (11). Inflammatory bowel diseases (IBD) IBD has clinically been defined as a spectrum of Linear foreign bodies are commonly seen in cats gastrointestinal disorders associated with chronic but may also be seen in dogs. The type of foreign inflammation of the stomach, intestine and/or material ingested included string, cellophane, colon of unknown pathogenesis and etiology. pieces of cloth and pantyhose. This type of mech- Histologically, IBD is characterized by diffuse anical obstruction has an accordion-like pleating inflammatory cell infiltration of the mucosal layer. or plication appearance of the small intestine on These cell populations are typically dominated by radiographs. They may be diagnosed with ultra- lymphocytes and plasma cells but may also include sonography by recognizing the characteristic eosinophils, neutrophils and macrophages (14). plicated appearance of the small bowel. The sono- graphic signs are abnormal undulating path of the Intestinal wall thickness has been a criterion for bowel and presence of a bright linear interface determining activity (clinical manifestation of the within the lumen (Figure 6). The affected bowel disease) in humans with inflammatory bowel may be fluid and gas dilated or just appears disease. However, intestinal wall thickness has not thickened and bunched. In the gastroduodenal been found to be specific or sensitive for diagnosis linear foreign body, the foreign material may be of inflammatory bowel disease in dogs (Figures 7 observed in the stomach (12). The presence of and 8) (15,16). Therefore, measurements of wall secondary problems associated with a linear foreign thickness alone may lead to false-negative results body, such as peritonitis, is suggested if free gas or for dogs with intestinal wall inflammation (16). In fluid in the abdomen is detected or the mesentery addition to thickness, altered wall layering appears is hyperechoic with poor sonographic detail, and to be an important finding which differentiates lymphadenopathy is present. An aspirate of any inflammatory from neoplastic and granulomatous free peritoneal fluid may be useful to assess the infiltration (17). However, loss of layering has also presence of peritonitis (12). been reported in severe enteritis or in the case of hemorrhagic, necrotizing, or granulomatous infiltr- ation (17).

Figure 7. Figure 8. Transverse ultrasonographic image of intestine segments filled Longitudinal ultrasonographic image of a jejunal segment of a with fluid. The wall thickness and appearance are normal. This dog with lymphocytic-plasmocytic enteritis. The intestinal wall dog had parvovirus enteritis. is slightly thickened, although, other than that it appears normal. A small amount of fluid is observed in the lumen of the bowel.

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ULTRASONOGRAPHY OF THE SMALL INTESTINE IN SMALL ANIMALS

Figure 9. Figure 10. Longitudinal sonogram of a jejunal segment of a dog with mucosal Longitudinal sonogram of a corrugated bowel caused by peritonitis. striations and abdominal effusion. This dog had a protein losing enteropathy.

Nowadays, it appears that the most important ultra- in association with enteritis (parvovirus, lympho- sound parameters that may allow differentiation of cytic-plasmocytic enteritis and hemorrhagic duo- dogs with IBD are the echogenicity of the small denitis), pancreatitis, peritonitis and bowel wall intestinal mucosa and the presence of secondary ischemia (19). abnormalities of the bowel and contiguous organs (16). Two patterns of increased mucosal echo- Intestinal tumors genicity have been reported, hyperechoic speckles Lymphomas, adenocarcinomas, and mast cell tumors and hyperechoic striations (16). Hyperechoic are the most common intestinal tumors in cats, striations are associated with a histopathologic whereas adenocarcinomas and leiomyomas are finding of dilated mucosal and are highly more common in dogs. Intestinal fibrosarcomas, specific for protein-losing enteropathy (Figure 9) hemangiosarcomas, carcinoids, and plasma cell (16,18). Hyperechoic speckles are a sensitive tumors are rare. Clinical signs usually include weight parameter for determining the presence of inflam- loss and anorexia. Diarrhea, melena, vomiting, matory disease, but they are non-specific for abdominal discomfort, abdominal effusion and differentiating disease category and activity. The anemia may also occur. Intussusception and intest- speckles within the mucosa may represent chronic inal perforation may occur as a consequence of changes that may require a longer period of time intestinal tumors (20). to resolve (16). A normal, hypoechoic intestinal mucosa in dogs with chronic diarrhea is a sensitive The most common ultrasonographic features of and specificity finding for the diagnosis of food- intestinal neoplasia are thickening of the bowel responsive disease (16). The presence of secondary wall, loss of its normal layered appearance, and abnormalities of the bowel, such as free abdominal alterations in the contour of the mucosal and/or fluid, edema of the pancreas, or thickening of the serosal surfaces (17). Changes associated with gallbladder wall, as well as distended bowel seg- intestinal neoplasia are most often focal as a mass- ments are observed in dogs with protein-losing like lesion but can also be diffuse, especially in the enteropathy (Figure 9), although it is uncommon case of canine gastrointestinal lymphoma. The in dogs with inflammatory bowel disease (16). mass may be quite variable in appearance. Focal, concentric thickening of the bowel may be present, Corrugation of the small bowel appears as regular or the thickening may be eccentric in location. waves of undulated bowel segments (Figure 10). Larger lesions are usually complex, with mixed This pattern is a sensitive, but nonspecific indicator echogenicity. While it is not difficult to identify of intestinal or abdominal disorders. It can be seen large mass lesions, it may be more of a challenge to

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associate the mass with the bowel. Metastasis to regional lymph nodes and occasionally to the liver or other organs can occur (17).

Lymphoma Alimentary lymphoma (involving the gastrointest- inal tract and/or the mesenteric lymph nodes) is one of the most common sites of occurrence for feline lymphoma (20).

In dogs and cats, the most common ultrasono- graphic findings are a transmural thickening associated with the diffuse loss of normal wall layering, reduced wall echogenicity, decreased A localized motility and regional lymph node enlargement (Figures 11A-11C) (21). In cats, alimentary lymphoma can affect the intestinal tract without fully disrupting the wall layering (2).

Adenocarcinomas Adenocarcinomas are considered the most com- mon gastrointestinal tumor in dogs. The most common ultrasonographic findings are trans- mural thickening with complete loss of layering, and often with associated lymphadenopathy (Figures 12A-12C). In the majority of these cases, there was evidence of fluid accumulation proximal to the intestinal thickening associated with localized ileus (22). B

Intestinal carcinoma has similar ultrasonographic appearance to intestinal lymphoma, (20) but the length of the lesion tends to be shorter in carcinoma than lymphoma, and mechanical ileus is more common in carcinoma than in lymphoma. So, these lesions must be biopsied with ultrasonic guidance to provide a definitive diagnosis (2).

Smooth muscle tumors tumors include leiomyomas, which are the most common benign tumors of the canine , and leiomyosarcomas, which are the most common sarcoma of the gastro- intestinal tract (2). C

Leiomyomas Figure 11. Leiomyoma are typically found within the stomach A.- Longitudinal, B.- Transverse sonograms of a jejunal segment of older dogs, although they can occasionally be of a cat with lymphoma. Marked thickening of the wall and loss found in the bowel (20). This tumor is small and of layering is observed. C.- The mesenteric lymph nodes were has a uniform echogenicity (Figure 13). enlarged, lobulated and hypoechoic.

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ULTRASONOGRAPHY OF THE SMALL INTESTINE IN SMALL ANIMALS

A Figure 13. Longitudinal sonogram of duodenum of a dog with smooth- muscle tumor. The mass is echogenic and homogeneous.

Leiomyosarcomas Leiomyosarcomas are usually seen as large, complex masses. These tumors are originated intramurally and grow out of the serosa as large eccentric, extraluminal masses, or less commonly grow into the bowel lumen. Due to their distrib- ution and large size, it is difficult to assess the anatomic origin of the mass (23). Internally, these masses may have anechoic and hypoechoic foci B which may correlate with the areas of necrosis and hemorrhage, accounting for their complex ultrasound appearance (23). Anemia is the most frequent hematological abnormality.

Percutaneous ultrasound-guided aspiration or tissue-core biopsy can be performed to confirm the mesenchymal nature of these lesions. However, careful choice of the biopsy path should be made to avoid anechoic cavities and subsequent leakage or hemorrhage (20).

Others tumors Fibrosarcomas, mast cell tumors, hemangio- sarcoma, adenomatous polyps and nonfunctional C carcinoid tumors tend to be focally invasive as poorly echogenic masses or as focal thickening Figure 12. with loss of layering. No specific ultrasonographic appearance helps to differentiate the tumors (2), A.- Longitudinal, B.- Transverse sonograms of a jejunal segment of a dog with carcinoma. In the wall, there are several echogenic so the ultimate diagnosis of the tumor type rounded masses that protrude into the lumen. C.- The mesenteric must be confirmed by histopathology using an lymph nodes were enlarged. endoscopic, surgical or aspiration/biopsy obtained with ultrasound guidance (20).

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ULTRASONOGRAPHY OF THE SMALL INTESTINE IN SMALL ANIMALS

Ultrasound-guided biopsy endoscopic or surgical biopsy. The main rule is Fine-needle aspiration or tissue-core biopsies of to carefully locate and avoid the lumen, since bowel masses under ultrasound guidance are intestinal content leakage can be a serious safe alternative procedures to use instead of complication (2).

REFERENCES

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