INTESTINAL INVAGINATION IN ADULTS: SPECTRUM OF IMAGES AND FREQUENT CAUSES

Silva H. Jorge, MD1, Jurado D. Mireya, MD2, Avalos G. Carmen, MD3

1Médico Radiólogo Intervencionista. Radiólogos Asociados, Quito - Ecuador 2Médica Radióloga. Hospital San Francisco IESS, Quito – Ecuador 3Médica Radióloga. Hospital San Francisco IESS, Quito – Ecuador

REVISTA DE LA FEDERACION ECUATORIANA DE RADIOLOGIA E IMAGEN. VOL 10 No 1 pag 13-18

ABSTRACT: The most frequent use of computed tomography as a diagnostic tool in different clinical Comité de Ética situations has increased the incidental findings of intestinal intussusception. Este artículo fue The diagnostic challenges consist in differentiating between the cases who require an urgent care and aprobado por el comité identifying the potential cause of the intussusception. de ética del Instituto This paper describes the types of intestinal intussusception, the differential diagnosis and the main Radiólogos Asociados diagnostic tools, useful to differentiate between the transient condition and the intussusception that requires surgical management. In addition, an updated review about basic concepts, etiology and

imaging features are presented along with representative clinical cases to depict the variety of Recibido en: octubre 20 de 2017 presentations of this condition.

Aceptado en: noviembre Key words: intussusception, , intestinal obstruction, computed tomography 30 de 2017 RESUMEN: Con el mayor uso de la tomografía computada como método diagnóstico en diferentes Correo para situaciones clínicas, el hallazgo incidental de invaginación intestinal en adultos ha aumentado. correspondencia a: El verdadero reto diagnóstico consiste en diferenciar aquellos casos que necesiten un tratamiento Dr. Jorge Silva Hidalgo urgente e identificar las posibles causas de la invaginación. jorgebolivar.silva@gmail. En este artículo se describen los diferentes tipos de invaginación intestinal, su diagnóstico diferencial y com las principales herramientas diagnosticas útiles para diferenciar la invaginación transitoria de la quirúrgica. Además, se presenta una revisión bibliográfica actualizada de los conceptos básicos, etiopatogenia y hallazgos de imagen junto con casos clínicos que ilustran la variedad de presentación de la invaginación intestinal. Palabras clave: invaginación intestinal, intususcepción, dolor abdominal, obstrucción intestinal, tomografía computada

INTRODUCTION produced in the majority of cases (70- 90%) by a serious underlying illness. he broad and increasing use of

computed tomography (CT) scan, as a T Currently it is recognized that this diagnostic method in different clinical information is not accurate, because it was situations, has increased the incidental obtained from a series of and finding of intestinal invagination in adults, histology in which all cases were surgical, especially one that has no invagination leaving aside those intestinal invaginations head and tends to be transient.1 causing no clinic, generating an

unintentional bias of this pathology. In most cases, the radiologist makes a

certainty diagnosis of intussusception with Therefore, these results are not applicable the CT scan, by observing the to intussusception diagnosed by any typical image of an intestine loop into the imaging method and mainly those subsequent portion of the digestive tract, diagnosed by CT scan.2-4 generating the classic “target sign”. Faced

with this, the true diagnostic challenge is By the above, differentiating between an to differentiate those cases that need intestinal intussusception with invagination urgent treatment and identify possible head of a transient is essential to causes for the invagination.1 determine the appropriate treatment and

to reduce any unnecessary surgical Until the 1990s, intestinal invagination in interventions.1 adults was considered to be an uncommon cause of intestinal obstruction,

representing only 5% of all invaginations and 1% of intestinal obstructions; the OBJETIVE average age of presentation varies The main objective of this article is to between the sixth and seventh decades of present a brief review of the topic through life.5,6 exemplifying cases of the methods of conventional images and images obtained by Multi-slice Computed Tomography (MSCT) scan where there are different variants of intestinal invagination. Finally, we list some useful features that allow a better diagnostic-therapeutic approach in each of the cases.

GENERALITIES AND PHYSIOLOGY Intussusception occurs when one segment of the (invaginated loop) enters into the following portion of the digestive tract (invaginating loop), partially or completely occluding the intestinal lumen.4 (Graphic 1)

In infants, intussusception is the second cause of acute abdomen after ; it is idiopathic in 95% of the cases and in the majority is resolved with GRAPHIC 1: Diagram illustrating a typical transient 4 intussusception seen longitudinally (a) and transversely to non-surgical reduction. Invagination in the axis of the digestive tract (b). The invaginating adults is reported as a rare entity, segments are highlighted (White arrow), invaginated (Black arrow) and also the invagination of the fat and the mesenteric vessels (Arrow’s head)

On the occasions that the invagination is symptomatic, the clinic and the time of evolution are variable, depending on the When there is a partially-mobile endo- location and cause. It can be acute, luminal organic injury ( or foreign chronic or recurrent and in all series, body), this is propelled with the peristaltic abdominal pain is the most common wave, and enters into the subsequent symptom (70-100%), followed by portion of the intestine and, therefore, and in 40-60% of cases and causes the invagination. This is known as only in 4-13% of the “invagination head”.5,9 These types of cases.7 Acute abdominal pain with invaginations following , defense is present in 50% of patients.12 adhesions, or external bodies, are those The presentation as a palpable mass is associated with intestinal obstruction.10 5 visible in less than 10% of the cases.

In situations where there is no invagination IMAGING STUDIES head, the intussusception-generator Intestinal invagination can be diagnosed mechanism is not completely known and with several imaging methods that include presumed that it occurs as a result of the barium-contrast studies, ultrasound (US) inappropriate increase of and magnetic resonance imaging (MRI); conceived by a functional disorder that however, the CT scan is clearly better prevents that the anterograde movement since it is unaffected by the presence of 14 wave takes its normal course. gas in the (which makes the ultrasound difficult) and also provides

important information about its possible In other cases, the image can be seen in cause. the classic target sign or “doughnut Disadvantages are the use of radiation sign”.11 and its reduced availability compared with ultrasound; still, assessing the risk-benefit, In contrasting studies, when the contrast the CT scan has been proposed as the material has an anterograde passage, it test of choice.1,3,7,15 displays a filiform passage through the lumen of the invaginated loop, which Plain x-ray often shows signs of intestinal acquires the shape of a spring (coiled- obstruction and allows discarding spring sign). On the other hand, when the . Rarely, if the lesion is contrast is injected through retrograde ileo-colic or colo-colic, the crescent-moon route, as in the colon by enema, it shows sign (crescent sign) can be observed, an intestinal invagination when it finds a which consists of a radiolucent image in filling-defect in the shape of a cup (cup- the shape of a half-moon generated by the shaped sign), which consists of the invaginated loop inside a distended colon invagination head, surrounded by full of air. contrast.10 (Figure 1) Ultrasound is not routinely used for the initial evaluation of the intestine, but it is the mostly-often-used method in the initial assessment of the adult patient with acute abdomen and therefore it can occasionally get images compatible with intestinal invagination, which consist of hyper and hypo-echogenic alternating multiple layers due to the presence of two superimposed mucous and muscular layers of the invaginating and invaginated segments. It is common to find external intestinal wall thickening (greater than 5 mm in thickness), represented in the cross- section of the intestinal loop as the “doughnut sign”.8,12 (Figure 2)

The -flow decrease detected by ECO Doppler predicts the possibility of necrosis and anticipates the need for .13

FINDINGS ON MULTI-SLICE COMPUTED TOMOGRAPHY (MSCT) CT scan can diagnose invagination with certainty due to its virtually-pathognomonic appearance. It is presented as a soft- tissue mass consisting in outside/inward: the external invaginating loop, a halo of mesenteric fat (with vascular structures), FIGURE 1 and 2: (1) Barium study (colon by enema), the internal invaginated loop and the 14 filling-defect in the shape of a cup (cup-shaped sign). lumen of the latter. (Graphic 1) The use of this method to increase the intraluminal pressure and press the invagination head into the proximal is known as non-surgical dis-invagination, widely used in Pediatrics but not very useful for adults. (2) Ultrasound, “target sign”, note the small volume of liquid (black arrow) between the invaginating (arrow’s head) and the invaginated (white arrow) loop.

A

B

FIGURE 3: A 61-year-old woman, admitted due to complicated duodenal ; a control CT scan was performed after the placement of naso-jejunal probe, no abdominal discomfort. As incidental finding there was a jejuno-jejunal invagination associated with the tube. (A) The axial CT scan shows image in horseshoe-shape corresponding to the invaginating loop containing the invaginated loop and the mesenteric fat. The punctiform-hypodense image corresponds to the probe (arrow). (B) Sagittal reconstruction where the unfolded probe can be observed.

This phenomenon is represented in In some cases, you can see a hyper- images as a mass in the shape of a dense halo surrounding the mesenteric fat sausage or sandwich (bowel-within-bowel) layer, which represents an opacification by when the tomographic cross-section oral contrast of the virtual space lying passes parallel to the longitudinal axis of between the outer and inner wall of the that portion of the intestine, or the classic invaginating loop.15 target sign when the cross-section passes perpendicularly to the longitudinal axis of While the image of invagination is the intestine.1,14 (Figure 3-4) characteristic, not in all cases it allows determining the origin of the TABLE 1: Classification of the Intestinal intussusception by CT scans. Invagination in the Adult DISCUSSION LOCATION ENTERO-ENTERIC ILEOCECAL There are various classifications according ILEOCOLIC (Figure 5) to the location, cause, duration and if they COLO-COLIC do or don’t present invagination head. DURATION PERSISTENT (Table 1) TRANSIENT RECURRENT CAUSE TUMOR (BENIGN OR SMALL INTESTINE MALIGNANT) NO TUMOR The invagination that involves the small intestine may be due to benign or INVAGINATION YES RESOLVES idiopathic causes and less frequent to a HEAD SPONTANEOUSLY . (Table 2) (No intestinal obstruction) The transient invagination is more frequent in the proximal intestine since the NO PERSISTENT peristaltic activity of the is more (Associated with intense and, therefore, the propulsive intestinal effect of the invaginated loop is greater.2,15 obstruction) Often, these types of invaginations are irrelevant and incidental, becoming Prepared by: Silva et al. (2017) findings that should not change the therapeutic approach of the patient.4,9

FIGURE 4: A 59-year-old woman who underwent a CT scan with endovenous contrast for study of intermittent hematuria, not referring any abdominal symptoms. (A) In axial CT scan we observed a mass of soft tissue with hypo-dense linear images inside (Arrows) that correspond to the mesenteric fat of an intussusception seen in longitudinal cross-section. (B) Coronal reconstruction showing the classic image of “target” from the invagination in a transversal cross-section of the compromised intestinal loop.

On the other hand, several malignant processes can cause invagination; the TABLE 2: Causes of Small Intestine most common are metastases (especially Invagination in Adults melanoma or carcinoid tumor); another Non-tumor Motility disorder important cause is the lymphoma.16,18 Systemic Lymphatoid diseases hyperplasia Several signs help distinguish between Adenitis permanent and transitory invagination; the Celiac disease most important are the signs of Crohn’s disease complication that predict a likely surgical- Henoch-Schonlein resolution; the most important are the Purpura presence of intestinal occlusion, free Focal Meckel's lesions diverticulum liquid, pneumoperitoneum, 9,10 Intestinal intestinalis, among others. (Table 3). duplication Other Jejunal-ileal In addition, there are signs directly related intubation to the invaginated segment which are the Foreign body presence of edema of the wall, Postoperative invagination head and the length of the adhesions portion of the intestine that is invaginated, Tumor Benign Lipoma which when being greater than 35 mm is Leiomyoma considered as a predictor of permanent Inflammatory invagination.9 (Figure 6). fibrous polyp Hemangioma Neurofibroma Malignant Metastasis COLON (Melanoma) The colonic invagination usually manifests Lymphoma as abdominal pain since it causes Adenocarcinoma intestinal obstruction.17 (Figure 7) More Prepared by: Silva et al. (2017) than half of the intussusceptions in the colon are associated with malignant lesions, including primary tumors (adenocarcinoma, lymphoma) and metastasis.(5)

TABLE 3: Signs that help Distinguishing Between Transient and Permanent Invagination SIGNS TRANSIENT PERMANENT * INVAGINATION HEAD No Yes INVAGINATED SEGMENT < 35 mm > 35 mm DILATION OF LOOPS No, mild Mild to Severe ONSET OF OCCLUSION Not evident Site of invagination SWELLING OF THE INTESTINAL WALL No, Mild Wall thickness > 5 mm SIGNS OF FREE LIQUID No Yes COMPLICATION PNEUMOPERITONEUM No Yes INTESTINAL IN No Yes THE PROXIMAL SEGMENT *Not all signs must be present to identify a permanent invagination. Prepared by: Silva et al. (2017)

FIGURE 5: A 52-year-old man who was admitted into ER due to intermittent, moderate abdominal pain, located on his right flank with 1 month of evolution. (A) CT scan with oral contrast that did not reach the colon; there is nodular image with soft-tissue density surrounded by a hypo- dense halo, located in the cecum. (B) Coronal reconstruction shows invagination of a short portion of the terminal in the cecum. (C) CT scan with EV contrast performed 1 hour later, in which the oral contrast reached the colon. We do not observe the previously-described image, compatible with intermittent intussusception.

FIGURE 6: A 57-year-old woman who presented pain and bloating associated with vomiting of intestinal contents, interpreted as intestinal obstruction. A MSCT scan (A) is performed with coronal reconstruction (B), showing that there are loops of small intestine dilated with hydro-air levels (white arrows), collapsed colon (black arrow), free liquid and extensive ileocecal invagination where it did not properly-displayed the hypo-dense halo by alteration of the mesenteric fat by reactive inflammation and edema of the wall of the invaginated loop (arrow’s head).

FIGURE 7: A 62-year-old patient who is admitted into ER due to pain and bloating. A MSCT scan is performed with EV contrast where we observe thickening of the wall of the invaginating loop (arrows’ head), a large portion of invaginated loop (black arrows) and intensive enhancement of congestive mesenteric vessels (white arrow). (B) Parietal thickening of the invaginated loop corresponding to invagination head (black arrows); the histopathological examination showed Adenocarcinoma of the Colon.

CONCLUSIONS with the great use of computed tomography scan for the diagnosis of Computed tomography scan is the many diseases, it will be increasingly diagnostic-imaging technique that more frequent to observe benign allows making an accurate diagnosis of invaginations that do not require intestinal invagination in almost all treatment. cases. There are direct and indirect signs that are useful to differentiate an invagination that will require surgical CONFLICTS OF INTEREST: treatment from a transient or benign. No one to declare. Finally, it is important to recognize that

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