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Published online before print August 18, 2003, 10.1148/radiol.2291020692
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(Radiology 2003;229:70-74.)
© RSNA, 2003

Nuclear Medicine

Active Inflammatory Bowel Disease: Evaluation with 99mTc (V) DMSA Scintigraphy1

Ioannis E. Koutroubakis, MD, Sophia I. Koukouraki, MD, Philippos D. Dimoulios, MD, Antigoni A. Velidaki, MD, Nikolaos S. Karkavitsas, MD, PhD and Elias A. Kouroumalis, MD, PhD

1 From the Departments of Gastroenterology (I.E.K., P.D.D., E.A.K.) and Nuclear Medicine (S.I.K., A.A.V., N.S.K.), University Hospital Heraklion, Voutes, 71110 Heraklion, Crete, Greece. Received June 10, 2002; revision requested August 8; final revision received February 24, 2003; accepted March 12. Address correspondence to I.E.K. (e-mail: ktjohn@her.forthnet.gr).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the use of pentavalent (V) technetium 99m (99mTc) dimercaptosuccinic acid (DMSA) scintigraphy for the assessment of disease activity in patients with inflammatory bowel disease (IBD).

MATERIALS AND METHODS: 99mTc (V) DMSA scintigraphy was performed in 76 patients. There were 36 patients with active IBD (11 with ulcerative colitis, 25 with Crohn disease), 28 patients with inactive disease (eight with ulcerative colitis, 20 with Crohn disease), and 12 patients with miscellaneous bowel disease. Sensitivity and specificity of 99mTc (V) DMSA scintigraphy in the diagnosis of IBD were calculated. In the group with active IBD, the disease activity and laboratory indices, as well as the endoscopic and histologic activity, were compared with the scanning activity index. Correlation coefficients between them were calculated with the Spearman rank test.

RESULTS: 99mTc (V) DMSA scintigraphy had a 92% (33 of 36) sensitivity and an 86% (24 of 28) specificity in the detection of active IBD. A significant correlation between disease activity indices and scintigraphy score was demonstrated. Endoscopic and histologic activity was significantly correlated (P = .005 and .02, respectively, overall disease activity) with the scanning activity score. Of the group of patients with miscellaneous bowel disease, three with ischemic colitis had negative findings at scintigraphy.

CONCLUSION: 99mTc (V) DMSA scintigraphy provides a noninvasive, practical, and accurate assessment of IBD activity.

© RSNA, 2003

Index terms: Colitis, ulcerative, 75.261 • Crohn disease, 75.262 • Enteritis, 75.262 • Inflammation, radionuclide studies, 75.12161, 75.1217 • Intestines, radionuclide studies, 75.12161, 75.1217


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Several agents have been used for radionuclide imaging of inflammatory bowel disease (IBD), and these agents include radiolabeled autologous leukocytes, polyclonal immunoglobulins, antigranulocyte monoclonal antibodies and, more recently, monoclonal antibodies that recognize activated endothelial adhesion molecules (1–6). The most important and widely used are the leukocytes (white blood cells) labeled with either indium 111 (111In) or technetium 99m (99mTc) because of their high sensitivity and specificity (3,5,7). 99mTc labeling has important advantages over labeling with 111In, and these advantages include shorter image acquisition times and improved image quality (8). For these reasons, 99mTc hexamethyl-propyleneamine oxime, or HMPAO, has replaced 111In as the radiopharmaceutical of choice for imaging IBD. With this noninvasive technique, it is possible to visualize active disease in both the small and the large bowel. However, stenoses, fistulas, and malignancies cannot be detected with 99mTc white blood cell scintigraphy. Moreover, the high cost, the time-consuming in vitro cell labeling procedure, and the concerns about radiation microdosimetry, as well as the handling and the reinjection of blood, are the main disadvantages of this diagnostic tool. To overcome these problems, new agents that are equally effective but do not have these disadvantages are being developed.

Pentavalent (V) 99mTc dimercaptosuccinic acid (DMSA) is a tumor-seeking agent previously reported to be effective in the detection of medullary thyroid cancer and in that of soft tissue, brain, and lung tumors (9–13). Uptake of 99mTc (V) DMSA by inflammatory tissues has also been reported, and it has been proved advantageous in the diagnosis of inflammations such as osteomyelitis, psoas muscle abscess, and bone and joint infections (14,15). It has the advantages of being an ideal 99mTc label that can be prepared with a simple method from commercially available DMSA kits (Ekete Dimokritos, Athens, Greece), and it is relatively inexpensive. The use of 99mTc (V) DMSA scintigraphy recently has been proposed as a useful noninvasive test for the detection and localization of intestinal inflammation (16).

The purpose of this study was to evaluate the use of 99mTc (V) DMSA scintigraphy for the assessment of disease activity in patients with IBD.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
We examined three groups of patients. In the first group, 36 consecutive patients (25 with Crohn disease [CD], 11 with ulcerative colitis [UC]) were included who had an exacerbation of previously proved IBD or who had a first attack of IBD. All these patients were hospitalized in the Department of Gastroenterology of the University Hospital Heraklion, Crete, Greece. An exacerbation was defined as recent deterioration of the symptoms in patients with IBD, with a CD activity index greater than 150 in CD (17) or a simple clinical colitis activity index greater than 3 in UC (18). The second group included 28 consecutive patients (eight with UC, 20 with CD) who were in remission (ie, >3 months) and had a CD activity index of less than 150 and a simple clinical colitis activity index of less than 3. These patients were followed up at the outpatient IBD clinic of our department. A diagnosis of UC and CD in both groups was based on standard criteria (19). The third group included 12 patients with miscellaneous bowel disease. Of these, five patients had segmental colitis associated with diverticulosis, four patients had ischemic colitis, and three patients had infectious colitis. They were also hospitalized in our hospital during the study period. The clinical characteristics of the patients with IBD and miscellaneous bowel disease are presented in Table 1.


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  		TABLE 1. Clinical and Laboratory Data in Three Groups of Patients in the Study

 
Standard laboratory parameters included red and white blood cell counts, hemoglobin level, hematocrit level, platelet count, albumin level, erythrocyte sedimentation rate, and C-reactive protein level and were routinely determined in all the patients of the three groups. Moreover, colonoscopy with biopsy was performed in all patients with active disease, as well as in those with miscellaneous bowel disease during their hospitalization. In the cases with active CD, upper gastrointestinal endoscopy and enteroclysis also were performed. From the endoscopic and histologic findings, a score of inflammatory activity for each bowel segment was determined according to a score evaluation as suggested by Kolkman et al (20). Endoscopic and histologic evaluation was performed by blinded specialists (E.A.K., I.E.K., P.D.D.) who had no knowledge of the diagnosis and the scintigraphic results. Informed consent was obtained from all patients, and the protocol of this study was approved by the review board of the University Hospital Heraklion.

99mTc (V) DMSA Scintigraphy and Interpretation of Findings
Seventy-six examinations with 99mTc (V) DMSA scintigraphy were performed. In all patients with active IBD, scintigraphy was performed within 3 days after colonoscopy. Twenty microcuries (740 MBq) of 99mTc (V) DMSA was injected intravenously in all patients included in this study. A gamma camera (Millennium; GE Medical Systems, Milwaukee, Wis) equipped with a low-energy general-purpose collimator (LEGP; GE Medical Systems) was used for 99mTc (V) DMSA scintigraphy. With the patient in the supine position, planar views of the abdomen were obtained 3 hours after intravenous injection. The time of imaging was chosen on the basis of the experimental data (21,22) and of the data of Lee et al (16). Before scanning, patients were requested to void their bladders to prevent false results. 99mTc (V) DMSA scintigraphy was well tolerated by all patients, and there were no complications.

All scintigrams were visually evaluated by two nuclear medicine physicians (S.I.K., N.S.K.) with 10 and 22 years of experience who had no knowledge of the diagnosis and the endoscopic data. The bowel was divided into the following five segments: small bowel, ascending colon, transverse colon, descending colon, and rectosigmoid. Scintigraphic images were considered positive when an area of increased uptake was observed in any of the five segments of the bowel. To assess the severity of IBD, the intensity of the uptake was evaluated by the same two nuclear medicine physicians with reference to the uptake in the iliac crest, and it was graded as follows: score 0, no uptake in the region of interest; score 1, faint uptake less than that of the iliac crest bone marrow; score 2, moderate uptake similar to that of the iliac crest; and score 3, severe uptake greater than that of the iliac crest. Concerning the disease localization, every part of the bowel was blindly evaluated by the same two nuclear medicine physicians with scores 0–3. Scintigraphic results were compared with endoscopic, radiologic, and clinical data of the patients by three of the authors (I.E.K, S.I.K., P.D.D.). Subanalysis of the scintigraphic results in the first group (with active IBD) according to the medical treatment was also performed. The sensitivity of 99mTc (V) DMSA scintigraphy in the diagnosis of IBD in patients who received steroids (28 cases) and in those who did not (eight cases) was compared.

Statistical Analysis
Results were considered false-negative when there was no uptake of 99mTc (V) DMSA in the bowel but clinical data and other examination findings were positive. In cases with clinical data that suggested inactive disease, any uptake of the bowel was considered as a false-positive scintigraphic finding.

Data were expressed as the mean ± SD or as the mean and range. Sensitivity, specificity, positive predictive value, and negative predictive value were calculated. To take account of possible interdependency between the five analyzed bowel segments, an analysis of principal components was performed with patients who had UC and CD. The data were transformed into a set of uncorrelated variables, and dimensionality was reduced (23). The principal components were calculated by using the covariance matrix, and the Kaiser criterion (24) was applied to ascertain the principal components to be retained. The first two principal components were used for further analysis; the first principal component, principal component 1, explains 48% of the variability in the data and is a contrast of the first three segments with the last two (a possible contrast of UC vs CD), and absolute values of loadings ranged from 0.12 to 0.77. The second principal component, principal component 2, explains 28% of the variability and represents overall disease activity (a weighted average with loadings between 0.23 and 0.52). Correlation coefficients were calculated by using the Spearman rank test. A difference with P < .05 was considered statistically significant. A statistical package (S-Plus 4.5; MathSoft, Seattle, Wash) was used for the analysis of principal components, and another statistical package (InStat, version 3.00 for Windows 95; GraphPad Software, San Diego, Calif) was used for all other tests.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Figures 1–3 show examples of the images obtained in patients with IBD. The overall scanning results in the three study groups are shown in Table 2. Presence of inflammation was revealed in 33 of 36 patients with active disease. False-negative results were found in one of 11 patients with UC and in two of 25 patients with CD. Inflammation was revealed in four of 28 patients with inactive disease. False-positive results were found in one of eight patients with UC and in three of 20 patients with CD. In the detection of active disease, the sensitivity and the specificity of 99mTc (V) DMSA scintigraphy were 92% (33 of 36) and 86% (24 of 28), respectively. The positive predictive value was 91.9%, and the negative predictive value was 85.1%. In nine of 12 patients with miscellaneous bowel disease, inflammation was revealed. Only three patients with ischemic colitis had negative findings at scintigraphy. An absolute correlation between the readings of the two nuclear medicine physicians concerning positivity was found. A disagreement in the grading was found in three cases, and this was resolved after discussion.



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  		Figure 1. Anterior 99mTc (V) DMSA scintigram in a patient with active UC shows intense inflammation (arrows) in transverse and left colon.

 


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  		Figure 2. Anterior 99mTc (V) DMSA scintigram in a patient with active CD shows intense inflammation (arrows) in the small bowel.

 


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  		Figure 3. Anterior 99mTc (V) DMSA scintigram in a patient with inactive CD shows no bowel inflammation.

 

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  		TABLE 2. Overall 99mTc (V) DMSA Scintigraphic Results in Three Groups of Patients

 
The 99mTc (V) DMSA scintigraphic score for overall disease activity (ie, principal component 2) was significantly correlated with the CD activity index score (Spearman rank correlation coefficient r = 0.50, P < .001) for patients with CD and with the simple clinical colitis activity index score (r = 0.53, P = .03) for patients with UC. In the 36 cases with active disease, a significant correlation between the scintigraphic score and endoscopic severity score (r = 0.42, P = .005) was established. A similar correlation with the histologic score (r = 0.34, P = .02) was also found. The correlations with the laboratory parameters are presented in Table 3.


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  		TABLE 3. Correlation between 99mTc (V) DMSA Scintigraphic Scores and Other Measures of Disease Activity

 
As far as disease localization is concerned, an analysis of the concordance of the results between colonoscopy (and enteroclysis when necessary) and 99mTc (V) DMSA scintigraphy was performed for the patients with active disease (n = 36) who had simultaneously undergone both examinations. All 10 patients with UC who had positive findings at 99mTc (V) DMSA scintigraphy had similar localization with colonoscopy. These patients included two with proctitis, five with left-sided colitis, and three with total colitis. In patients with CD, concordant localization was found in 16 of 23 who had positive findings on scans, whereas disagreement between the two methods was found in seven patients. In all seven patients (two with small-bowel disease and five with colonic disease), areas with endoscopic findings of mild disease such as aphthous ulcers, erythema, and edema were not depicted at scintigraphy. Presence of inflammation was revealed in 26 (93%) of 28 patients receiving treatment with steroids and in seven (88%) of eight patients who were not receiving treatment with steroids. There was no statistically significant difference between the two groups. Similarly, no significant association between the scintigraphic results and the use of other medications was found.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
REFERENCES
 
Findings of the present study show that 99mTc (V) DMSA scintigraphy has a high sensitivity and specificity in the detection of active inflammation in IBD. 99mTc (V) DMSA was developed in 1981, and it has been recognized as advantageous for radionuclide imaging of malignant tumors and their metastases (21). Subsequently, it was demonstrated that there is uptake of 99mTc (V) DMSA by inflammatory tissues. Moreover, experimental inflammatory lesions in mice were better visualized with 99mTc (V) DMSA in comparison with trivalent 99mTc DMSA and 99mTc human polyclonal immunoglobulin (22). 99mTc (V) DMSA scintigraphy proved advantageous in the diagnosis of inflammations such as osteomyelitis, psoas muscle abscess, and bone and joint infections in humans (14,15). 99mTc (V) DMSA is a low-molecular-weight complex, and its suggested mechanism of localization of inflammatory lesions is the infiltration into the interstitial space caused by increased capillary permeability (22). The use of 99mTc (V) DMSA scintigraphy recently has been evaluated in the detection and localization of intestinal inflammation in a study from Taiwan (16). In 62 cases with suspected intestinal inflammation and a final diagnosis of UC in 15, of CD in one, and of miscellaneous colitis in 46, 99mTc (V) DMSA scintigraphy had a sensitivity of 95% and a specificity of 94% in the detection of the site of inflammation. On the basis of these data and our data, we could suggest that 99mTc (V) DMSA scintigraphy could be used for the detection and localization of intestinal inflammation. However, in this study with 99mTc (V) DMSA scintigraphy, discrimination between the various causes of intestinal inflammation was not possible. The negative scintigraphic results in three of four patients with ischemic colitis may suggest that a larger series of patients with ischemic colitis is required to answer the question of whether 99mTc (V) DMSA scintigraphy can help to distinguish between IBD and ischemic colitis. It is possible that in some cases of colonic ischemia there is mainly a transient mucosal congestion and not enough chronic inflammation in order for bowel uptake to be depicted.

Scanning with leukocyte labeling has been demonstrated by investigators in several studies as a reliable technique for the diagnosis and assessment of disease activity in IBD (25–27), as well as for the early detection of postoperative asymptomatic recurrence in CD (28). 99mTc hexamethyl-propyleneamine oxime white blood cell single photon emission computed tomographic imaging provides an accurate quantification of IBD activity and has been proposed as an objective method in the assessment of treatment response in IBD (29–31). However, the time-consuming in vitro cell labeling procedure and concerns about radiation microdosimetry are shortcomings of this method, and a simpler alternative technique is desirable.

In the present study, we tried to answer the question that has been raised about whether 99mTc (V) DMSA scintigraphy can be used in the assessment of disease activity in IBD. Our data showed that 99mTc (V) DMSA scintigraphy provides a noninvasive, practical, safe, and accurate assessment of IBD activity. Moreover, there was a high patient acceptability compared with that for endoscopic and radiographic methods, because 99mTc (V) DMSA scintigraphy requires no bowel preparation and causes no discomfort.

A significant correlation between the 99mTc (V) DMSA scintigraphic score and disease activity indices was found in patients with UC and in those with CD. From the examined laboratory parameters, only C-reactive protein levels were also significantly correlated with the scintigraphic score. In cases in which the intestinal segments were studied both endoscopically and histologically, a high correlation of the scintigraphic activity index with endoscopic and histologic inflammatory activity was found. From the statistical analysis of the principal component, however, it appears that the variability in the pattern of uptake of 99mTc (V) DMSA represents differences caused by the underlying condition to a greater extent than it represents extent of overall disease activity in the group of patients that is considered. As for accuracy of 99mTc (V) DMSA scintigraphy related to disease localization, the assessment of IBD extension was somewhat more accurate in patients with UC than it was in those with CD. The inability of 99mTc (V) DMSA scintigraphy to identify mild lesions in patients with CD represents a limitation of the method. Moreover, the liver and bladder uptake could limit bowel visualization in the hepatic flexure and pelvis. This problem could be solved by obtaining images with the patient in the upright position to distinguish liver activity from the hepatic flexure after the bladder is emptied and, when necessary, with additional lateral views.

In conclusion, the results of the present study, undertaken to evaluate the use of 99mTc (V) DMSA scintigraphy in the assessment of active IBD, suggest that scintigraphy with this radionuclide provides a practical and accurate approach to identify patients with active disease and to assess the disease activity. 99mTc (V) DMSA scintigraphy cannot be used for the diagnosis of IBD, which is still based in other methods, but it can be recommended for use at follow-up and for assessment of disease activity in the patients. The response to various treatment schedules, as well as the disease progression, can also be evaluated by using this method. In addition, this technique may be complementary to colonoscopy in the assessment of disease activity and extension when colonoscopy cannot be completed. The direct comparison of 99mTc (V) DMSA scintigraphy with 99mTc hexamethyl-propyleneamine oxime white blood cell scintigraphy in the evaluation of IBD may be necessary in future studies.


   ACKNOWLEDGMENTS
 
We are grateful to Dr Joanna Moschandreas for her assistance in the statistical analysis of the results.


   FOOTNOTES
 
Abbreviations: CD = Crohn disease, DMSA = dimercaptosuccinic acid, IBD = inflammatory bowel disease, UC = ulcerative colitis

Author contributions: Guarantor of integrity of entire study, I.E.K.; study concepts and design, N.S.K.; literature research, I.E.K.; clinical studies, P.D.D., A.A.V., S.I.K.; data acquisition, S.I.K., P.D.D.; data analysis/interpretation, I.E.K.; statistical analysis, I.E.K.; manuscript preparation and editing, I.E.K.; manuscript definition of intellectual content, revision/review, and final version approval, E.A.K.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 

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