(Radiographics. 2000;20:1153-1159.)
© RSNA, 2000
Radionuclide Imaging in the Evaluation of Acute Gastrointestinal Bleeding1
Lawrence E. Holder, MD
1 From the Department of Diagnostic Imaging, Division of Nuclear Medicine, University of Maryland Medical System, 22 S Greene St, Baltimore, MD 21201-1595. From the Plenary Session, Friday Imaging Symposium: Algorithmic Controversies, at the 1999 RSNA scientific assembly. Received March 14, 2000; revision requested March 27 and received April 12; accepted April 14. Address correspondence to the author (e-mail: lhold002@umaryland.edu).
Index Terms: Gastrointestinal tract, hemorrhage, 70.12178 Gastrointestinal tract, radionuclide studies, 70.12178
Introduction
Most reports available in the surgery and radiology literature base their conclusions and recommendations on results obtained with older techniques that have significant inherent limitations (1,2), and many do not describe the imaging technique or criteria used for localization (1,3,4). The primary technical weakness in the older techniques was the collection of data with insufficient temporal resolution. Images obtained every hour, 30 minutes, 15 minutes, or even 5 minutes cannot depict physiologic events that often occur during 10- or 15-second periods. Rapid antegrade bowel transit of intraluminal blood, retrograde transit of blood, and intraluminal dilution of minimal, often intermittent bleeding must be recognized for detection and correct localization of bleeding sites.
Even when more dynamic imaging protocols were used, the small-, standard-, or original large-field-of-view gamma cameras that were available prior to the introduction of the extra large field-of-view detectors in 1990 limited the ability to simultaneously visualize all of the upper and lower gastrointestinal tract (5). Most often this resulted in the inability to detect gastric, duodenal, or jejunal sources of bleeding that manifested as suspected acute lower gastrointestinal bleeding (6,7).
It was not until 1992 that emphasis was placed on the concept of rapid diagnostic imaging with cine scintigraphy or movie mode display (8,9). One currently accepted protocol used in our department is shown in Table 1. It includes the highly efficient in vitro red blood cell labeling technique, which eliminates the diagnostic challenges created by incomplete labeling (eg, free pertechnetate being secreted into the gastrointestinal tract) (10). The historical debate about the relative merits of Tc-99m sulfur colloid versus Tc-99mlabeled red blood cells, which has generally been resolved in favor of the latter, was not discussed during the symposium (11,12). The technical advances that permit rapid dynamic imaging with extra large field-of-view cameras and movie mode display on improved monitors have also allowed more specific localization criteria to be established (Table 2).
Both the imaging protocol and the criteria used for localization require and emphasize dynamic data acquisition and movie mode analysis. Only movie mode display was used in the presentation of this material at the Friday Imaging Symposium; for the print version, selected frames are used for illustrative purposes only; they are not adequate for clinical diagnosis.
The goal of this presentation was to illustrate the current state-of-the-art technique for scintigraphic localization of the source of acute gastrointestinal bleeding. Among the controversies that were not considered were the capacity of scintigraphy to help direct surgical intervention (3,4,13,14), angiographic diagnosis, or treatment or to improve the positive yield of angiographic studies (15,16). Furthermore, the question of which patients have acute, "significant," or "life-threatening" bleeding and should undergo emergent imaging and which should undergo upper gastrointestinal endoscopy or other studies instead of urgent scintigraphy was left to the referring clinician and the institution (10,17).
This article discusses and illustrates the impact of a variety of factors on the evaluation of acute gastrointestinal bleeding with radionuclide imaging. These factors are related to blood flow (rapid antegrade transit, retrograde transit, intermittent or minimal bleeding), surgical procedures (postsurgical bowel), and timing of imaging (delayed imaging).
Blood Flow
Rapid Antegrade Transit
Blood is an irritant and cathartic and can move rapidly through both the small and large bowel. Care must be taken to detect the site of the initial appearance of radiotracer, especially when bleeding is intermittent (Fig 1; see also Movie 1 at http://radiographics.rsnajnls.org/cgi/content/full/20/4/1153/DC1/index.htm). Ten 10-second-per-frame images, which yield optimal temporal resolution, are most helpful in this situation.

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Figure 1a. Rapid antegrade transit from a bleeding site at the hepatic flexure. (a) Selected anterior images from a dynamic 10-second-per-image acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint abnormal increased activity in the distal ascending colon (arrow). (b) Selected anterior images from the same acquisition that were obtained 24 minutes 41 seconds to 24 minutes 50 seconds (left), 24 minutes 51 seconds to 25 minutes (middle), and 25 minutes 1 second to 25 minutes 10 seconds (right) after injection demonstrate rapid transit from the hepatic flexure (short arrow) to the splenic flexure and descending colon (long arrow). This movement occurred in less than 30 seconds.
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Figure 1b. Rapid antegrade transit from a bleeding site at the hepatic flexure. (a) Selected anterior images from a dynamic 10-second-per-image acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint abnormal increased activity in the distal ascending colon (arrow). (b) Selected anterior images from the same acquisition that were obtained 24 minutes 41 seconds to 24 minutes 50 seconds (left), 24 minutes 51 seconds to 25 minutes (middle), and 25 minutes 1 second to 25 minutes 10 seconds (right) after injection demonstrate rapid transit from the hepatic flexure (short arrow) to the splenic flexure and descending colon (long arrow). This movement occurred in less than 30 seconds.
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Retrograde Transit
There is considerable variation in the peristaltic patterns encountered in patients who have intraluminal blood. Rapid dynamic imaging detects such movements, with movie mode display further increasing diagnostic certainty (Fig 2; see also Movie 2 at same URL as above).

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Figure 2a. Retrograde transit from a bleeding site in the proximal sigmoid or distal descending colon. Each image represents the summation of six 10-second frames into a 1-minute frame for increased spatial resolution. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 1-2 minutes (left), 2-3 minutes (middle), and 3-4 minutes (right) after injection demonstrate a focus of increased activity just lateral to the left common iliac vein (arrow). This area of increased activity represents the site of bleeding. (b) Selected images from the same acquisition that were obtained 45-46 minutes (left), 46-47 minutes (middle), and 47-48 minutes (right) after injection demonstrate antegrade movement across the midline (thick arrow) as well as retrograde movement to the splenic flexure (thin arrow).
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Figure 2b. Retrograde transit from a bleeding site in the proximal sigmoid or distal descending colon. Each image represents the summation of six 10-second frames into a 1-minute frame for increased spatial resolution. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 1-2 minutes (left), 2-3 minutes (middle), and 3-4 minutes (right) after injection demonstrate a focus of increased activity just lateral to the left common iliac vein (arrow). This area of increased activity represents the site of bleeding. (b) Selected images from the same acquisition that were obtained 45-46 minutes (left), 46-47 minutes (middle), and 47-48 minutes (right) after injection demonstrate antegrade movement across the midline (thick arrow) as well as retrograde movement to the splenic flexure (thin arrow).
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Intermittent Bleeding
The intermittent nature of even massive bleeding is well established (18,19). The length of a standard imaging session is determined by each individual department's patient load, intensive care unit nursing logistics, and the patient's condition. At our institution, if the site of active bleeding is not detected within 60 minutes, we will often extend the imaging session to 120 minutes or longer in patients who have received multiple transfusions and demonstrate significant hemodynamic instability (Fig 3; see also Movie 3 at same URL as above).

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Figure 3a. Intermittent bleeding from a hepatic flexure site. Each image represents the summation of six 10-second frames into a 1-minute frame (cf Fig 2). (a) No focus of bleeding is seen on selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-1 minute (left), 1-2 minutes (middle), and 2-3 minutes (right) after injection. Note that the aorta and the inferior vena cava overlap (arrow). (b) Selected images from the same acquisition that were obtained 45-46 minutes (left), 46-47 minutes (middle), and 47-48 minutes (right) after injection demonstrate activity that originates in the hepatic flexure and moves antegrade through the transverse colon to the splenic flexure.
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Figure 3b. Intermittent bleeding from a hepatic flexure site. Each image represents the summation of six 10-second frames into a 1-minute frame (cf Fig 2). (a) No focus of bleeding is seen on selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-1 minute (left), 1-2 minutes (middle), and 2-3 minutes (right) after injection. Note that the aorta and the inferior vena cava overlap (arrow). (b) Selected images from the same acquisition that were obtained 45-46 minutes (left), 46-47 minutes (middle), and 47-48 minutes (right) after injection demonstrate activity that originates in the hepatic flexure and moves antegrade through the transverse colon to the splenic flexure.
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Minimal Bleeding
The less bleeding that is present, the more difficult it can be to localize the site to a specific bowel segment, particularly in the jejunum and ileum. However, demonstrating that the bleeding is minimal is valuable in itself in that it obviates urgent intervention. Small amounts of blood also move slowly, so that without the urgent need to transport the patient to the operating room or angiography suite, imaging can be continued until the visualization of more distal bowel allows more certain localization (Fig 4; see also Movie 4 at same URL as above). Summing the 10-second images into a 1-minute-per-frame imaging sequence is often a necessary compromise between achieving optimal temporal resolution and having enough counts per image for adequate spatial resolution.

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Figure 4a. Minimal bleeding from a proximal ileal focus. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint activity in the lower pelvis medial to the iliac vein (arrow), a finding that represents the bleeding site. The area of photon deficiency inferior to the focus of abnormal activity represents the bladder (arrowhead). (b) Selected images from the same acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 26-27 minutes (left), 27-28 minutes (middle), and 28-29 minutes (right) after injection demonstrate increasing intensity without significant movement (arrow). (c) Selected images from the same acquisition (each image represents a 1-minute summation) obtained 79-80 minutes (left), 80-81 minutes (middle), and 81-82 minutes (right) after injection demonstrate movement of radiotracer superiorly and to the right (arrowheads). Bladder filling is more prominent than on the previously acquired images (cf a and b). (d) On selected images from the same acquisition (each image represents a 1-minute summation) obtained 162-163 minutes (left), 163-164 minutes (middle), and 164-165 minutes (right) after injection, the bladder is full and the leading edge of the labeled red blood cells has reached the ascending colon (arrow), which helps confirm localization of the initial bleeding site. Note that there is no longer any activity at the site of initial bleeding.
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Figure 4b. Minimal bleeding from a proximal ileal focus. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint activity in the lower pelvis medial to the iliac vein (arrow), a finding that represents the bleeding site. The area of photon deficiency inferior to the focus of abnormal activity represents the bladder (arrowhead). (b) Selected images from the same acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 26-27 minutes (left), 27-28 minutes (middle), and 28-29 minutes (right) after injection demonstrate increasing intensity without significant movement (arrow). (c) Selected images from the same acquisition (each image represents a 1-minute summation) obtained 79-80 minutes (left), 80-81 minutes (middle), and 81-82 minutes (right) after injection demonstrate movement of radiotracer superiorly and to the right (arrowheads). Bladder filling is more prominent than on the previously acquired images (cf a and b). (d) On selected images from the same acquisition (each image represents a 1-minute summation) obtained 162-163 minutes (left), 163-164 minutes (middle), and 164-165 minutes (right) after injection, the bladder is full and the leading edge of the labeled red blood cells has reached the ascending colon (arrow), which helps confirm localization of the initial bleeding site. Note that there is no longer any activity at the site of initial bleeding.
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Figure 4c. Minimal bleeding from a proximal ileal focus. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint activity in the lower pelvis medial to the iliac vein (arrow), a finding that represents the bleeding site. The area of photon deficiency inferior to the focus of abnormal activity represents the bladder (arrowhead). (b) Selected images from the same acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 26-27 minutes (left), 27-28 minutes (middle), and 28-29 minutes (right) after injection demonstrate increasing intensity without significant movement (arrow). (c) Selected images from the same acquisition (each image represents a 1-minute summation) obtained 79-80 minutes (left), 80-81 minutes (middle), and 81-82 minutes (right) after injection demonstrate movement of radiotracer superiorly and to the right (arrowheads). Bladder filling is more prominent than on the previously acquired images (cf a and b). (d) On selected images from the same acquisition (each image represents a 1-minute summation) obtained 162-163 minutes (left), 163-164 minutes (middle), and 164-165 minutes (right) after injection, the bladder is full and the leading edge of the labeled red blood cells has reached the ascending colon (arrow), which helps confirm localization of the initial bleeding site. Note that there is no longer any activity at the site of initial bleeding.
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Figure 4d. Minimal bleeding from a proximal ileal focus. (a) Selected images from a dynamic 10-second-per-frame acquisition that were obtained 0-10 seconds (left), 11-20 seconds (middle), and 21-30 seconds (right) after injection demonstrate faint activity in the lower pelvis medial to the iliac vein (arrow), a finding that represents the bleeding site. The area of photon deficiency inferior to the focus of abnormal activity represents the bladder (arrowhead). (b) Selected images from the same acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 26-27 minutes (left), 27-28 minutes (middle), and 28-29 minutes (right) after injection demonstrate increasing intensity without significant movement (arrow). (c) Selected images from the same acquisition (each image represents a 1-minute summation) obtained 79-80 minutes (left), 80-81 minutes (middle), and 81-82 minutes (right) after injection demonstrate movement of radiotracer superiorly and to the right (arrowheads). Bladder filling is more prominent than on the previously acquired images (cf a and b). (d) On selected images from the same acquisition (each image represents a 1-minute summation) obtained 162-163 minutes (left), 163-164 minutes (middle), and 164-165 minutes (right) after injection, the bladder is full and the leading edge of the labeled red blood cells has reached the ascending colon (arrow), which helps confirm localization of the initial bleeding site. Note that there is no longer any activity at the site of initial bleeding.
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Postsurgical Bowel
Resection, anastomosis, and mobilization of normal bowel all create difficulties in bleeding site localization (Fig 5; see also Movie 5 at same URL as above). An understanding of what has already been donewith a surgical drawing available if possibleis helpful, but localization in the postoperative patient should be performed with extra caution. As with all localization, any uncertainty must be clearly communicated to the referring surgeon or angiographer.

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Figure 5a. Blood from a bleeding transplanted pancreas entering the ileum via a donor cuff duodenostomy. The patient had undergone combined kidney-pancreas transplantation. (a) Selected images from a dynamic 10-second-per-frame acquisition (each image represents the summation of six 10-second frames into a 1-minute frame for increased spatial resolution) that were obtained 0-1 minute (left), 1-2 minutes (middle), and 2-3 minutes (right) after injection demonstrate increased activity in the right lower quadrant (thick arrow) without definite luminal increases in intensity. Note the movement of the area of increased activity medially, superiorly, and laterally. The renal transplant is seen in the left side of the pelvis (thin arrow). (b) Selected frames from the same acquisition that were obtained 32 minutes 31 seconds to 32 minutes 40 seconds (left), 32 minutes 41 seconds to 32 minutes 50 seconds (middle), and 33 minutes 51 seconds to 34 minutes (right) after injection demonstrate medial movement of a focus of increased activity (arrow). Such a course is not typical for antegrade movement from the cecum up through the ascending colon, which is usually visualized laterally.
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Figure 5b. Blood from a bleeding transplanted pancreas entering the ileum via a donor cuff duodenostomy. The patient had undergone combined kidney-pancreas transplantation. (a) Selected images from a dynamic 10-second-per-frame acquisition (each image represents the summation of six 10-second frames into a 1-minute frame for increased spatial resolution) that were obtained 0-1 minute (left), 1-2 minutes (middle), and 2-3 minutes (right) after injection demonstrate increased activity in the right lower quadrant (thick arrow) without definite luminal increases in intensity. Note the movement of the area of increased activity medially, superiorly, and laterally. The renal transplant is seen in the left side of the pelvis (thin arrow). (b) Selected frames from the same acquisition that were obtained 32 minutes 31 seconds to 32 minutes 40 seconds (left), 32 minutes 41 seconds to 32 minutes 50 seconds (middle), and 33 minutes 51 seconds to 34 minutes (right) after injection demonstrate medial movement of a focus of increased activity (arrow). Such a course is not typical for antegrade movement from the cecum up through the ascending colon, which is usually visualized laterally.
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Delayed Imaging
Because Tc-99m has a physical half-life of 6 hours and the labeled red blood cells are stable for many hours, it is theoretically possible to perform delayed imaging up to 1824 hours after labeling and injection. It is important to remember that intraluminal activity seen on a delayed image after initial dynamic acquisition that did not demonstrate bleeding simply indicates that the labeled red blood cells entered the bowel between the end of the first imaging session and the start of the delayed session (Fig 6a). Subsequent dynamic acquisition performed with standard acquisition protocol and interpreted with standard diagnostic criteria is required for localization. A second injection of labeled red blood cells is often required after 12 hours and occasionally earlier (Fig 6b; see also Movie 6b at same URL as above) (20).

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Figure 6a. Delayed bleeding from a midjejunal site. Findings at initial imaging performed 0-60 minutes after injection were normal. (a) Anterior 5-minute static image obtained 22 hours after injection demonstrates activity throughout the large bowel and in a few small bowel loops in the pelvis (arrow). (b) Selected frames from a dynamic 10-second-per-image acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 60-61 minutes (left), 61-62 minutes (middle), and 62-63 minutes (right) after a second injection of labeled red blood cells demonstrate activity in the small bowel (long arrow) and movement across the midline in the midabdomen. Some residual activity from the first injection (cf a) is seen in the splenic flexure in the left upper quadrant (short arrow).
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Figure 6b. Delayed bleeding from a midjejunal site. Findings at initial imaging performed 0-60 minutes after injection were normal. (a) Anterior 5-minute static image obtained 22 hours after injection demonstrates activity throughout the large bowel and in a few small bowel loops in the pelvis (arrow). (b) Selected frames from a dynamic 10-second-per-image acquisition (each image represents the summation of six 10-second frames into a 1-minute frame) obtained 60-61 minutes (left), 61-62 minutes (middle), and 62-63 minutes (right) after a second injection of labeled red blood cells demonstrate activity in the small bowel (long arrow) and movement across the midline in the midabdomen. Some residual activity from the first injection (cf a) is seen in the splenic flexure in the left upper quadrant (short arrow).
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Conclusions
In most patients, significant bleeding in the stomach, small bowel, or colon can be localized with a high degree of certainty. Colonic bleeding can be more precisely localized than jejunal or ileal bleeding, and the bleeding site in patients who have not undergone prior surgery can be localized with more confidence than in those patients who have undergone prior surgery. Extending the dynamic imaging session to allow visualization of more distal transit is often required to localize minimal bleeding, increase anatomic certainty, and localize small bowel bleeding sites.
Footnotes
Editor's note.Supplemental material (see the editorial by Honeyman and Olmsted in this issue [pp 905906
]) for this article in the form of movie mode display images is available at http://radiographics.rsnajnls.org/cgi/content/full/20/4/1153/DC1/index.htm
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