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(Radiology. 2001;219:86-90.)
© RSNA, 2001

Nuclear Medicine

Protein-losing Enteropathy: Diagnosis with 99mTc-labeled Human Serum Albumin Scintigraphy1

Nan-Tsing Chiu, MD, Bi-Fang Lee, MD, Shang-Jyh Hwang, MD, Jer-Ming Chang, MD, Gin-Chung Liu, MD and Hsin-Su Yu, MD

1 From the Department of Nuclear Medicine, National Cheng Kung University Hospital, 138 Sheng-Li Rd, Tainan 704, Taiwan (N.T.C., B.F.L.); and the Departments of Internal Medicine (S.J.H., J.M.C.) and Radiology (G.C.L.) and the Institute of Medicine (H.S.Y.), Kaohsiung Medical University Hospital, Kaohsiung, Taiwan. Received March 1, 2000; revision requested April 9; final revision received August 11; accepted September 12. Address correspondence to B.F.L. (e-mail: ntchiu@mail.ncku.edu.tw).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To investigate the diagnostic value of technetium 99m–labeled human serum albumin (HSA) scintigraphy in a group of patients suspected of having protein-losing enteropathy (PLE).

MATERIALS AND METHODS: After intravenous injection of 740 MBq of freshly prepared 99mTc HSA, serial images of the abdomen were obtained from 10 minutes until 24 hours after injection. A 99mTc HSA scan was considered positive for PLE if there was visible tracer exudation in the gut. The diagnosis was established on the basis of standard clinical and biopsy findings.

RESULTS: Thirty-nine scans were obtained: 27 scans in 26 suspected cases of PLE and 12 scans in control subjects with no known gastrointestinal disease. Twenty-five of the 26 studies in patients suspected of having PLE showed 99mTc HSA activity in the bowel. Among the 25 studies with positive findings, seven demonstrated PLE only on images obtained 24 hours after injection. In the control subjects, no activity was seen in the bowel.

CONCLUSION: 99mTc HSA with serial scanning for up to 24 hours is reliable and useful for imaging PLE. Sites of protein loss may also be demonstrated. This imaging method is convenient, easy to perform, and yields results within 24 hours.

Index terms: Gastrointestinal tract, diseases, 70.60, 70.70 • Gastrointestinal tract, radionuclide studies, 70.1217 • Proteins, 70.60, 70.70 • Radionuclide imaging, 70.1217


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Protein-losing enteropathy (PLE) with and without gross anatomic lesions in the bowel has been reported in a heterogeneous group of diseases. It is associated with excessive loss of plasma protein into the gut (1). To detect gastrointestinal protein loss, iodine 131 polyvinylpyrrolidone, iodine 125 polyvinylpyrrolidone (2), chromium 51–labeled albumin (3), 51Cr chromic chloride, 125I albumin (4), indium 111 chloride (5), 111In transferrin (6–8), technetium 99m diethylenetriaminepentaacetic acid human serum albumin (HSA) (9), 99mTc dextran (10,11), 99mTc human immunoglobulin (11,12), and fecal clearance of {alpha}1-antitrypsin (13) have been used.

99mTc–labeled HSA has been used to image PLE since its introduction in 1986 (14). However, our search of the literature (14–25) yielded few series of PLE diagnosed with 99mTc HSA; moreover, none reported more than 18 cases, thus raising the question of the diagnostic value of this radiotracer. The present study was performed in a group of 26 patients suspected of having PLE and 12 control subjects to evaluate and calculate the sensitivity of 99mTc HSA.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Patients
Between December 1993 and October 1999, 26 patients (11 men and 15 women; age range, 30–77 years; mean age, 45.9 years) with hypoalbuminemia (1.75–3.47 g/dL [17.5–34.7 g/L]) and a clinical suspicion of PLE were referred to our hospitals (Cheng Kung University Hospital, Tainan, Taiwan, and Kaohsiung Medical University Hospital, Kaohsiung, Taiwan) to document PLE with abdominal scintigraphy by using 99mTc HSA. PLE was clinically suspected as the result of hypoalbuminemia and the exclusion of urinary loss. Although two patients (patients 18 and 22) had proteinuria, their reduction in the concentration of serum proteins was greater than could be explained by the magnitude of proteinuria. They were included in this study.

The final diagnosis was made with biopsy findings (12 patients and 12 control subjects), culture findings (one patient), or clinical follow-up (13 patients). The underlying diseases in the 26 patients were systemic lupus erythematosus (13 patients—two with nephrotic syndrome), biopsy-proved colon cancer (three patients), biopsy-proved enterocolitis (three patients), biopsy-proved intestinal lymphoma (three patients), culture-proved infectious colitis (one patient), and biopsy-proved lymphangiectasia (three patients). In addition, 12 control subjects (six men and six women; age range, 33–68 years; mean age, 51.2 years) with no known gastrointestinal disease during the study period were referred routinely for cardiac blood-pool imaging with 99mTc HSA with sequential imaging over 24 hours, and they were included in our study.

All studies were performed with the informed consent of all subjects after a full explanation of the examination. Institutional review board approval for the study was obtained. The presence of proteinuria and fecal occult blood was investigated in all patients. Levels of glutamic-oxaloacetic transaminase (GOT) and glutamic-pyruvic transaminase (GPT) were measured in all patients for the assessment of hepatic function; levels of GOT higher than 25 IU/L (0.41 microkatal [µkat] per liter) and of GPT higher than 25 IU/L (0.41 µkat/L) were considered abnormal.

Imaging
Because all patients and control subjects received an intravenous injection of 740 MBq (20 mCi) of freshly prepared 99mTc–labeled HSA (Techne Albumin Kit; Daiichi Radioisotope, Tokyo, Japan), the acquisition time for all studies was the same. Scintigraphic images of the abdomen and pelvis were obtained with a gamma camera (Vertex; ADAC, Milpitas, Calif) equipped with a low-energy general-purpose collimator at intervals of 10 minutes, 30 minutes, 1 hour, 2 hours, 4 hours, and 24 hours. The study was terminated 24 hours after injection or when there was no change in the scan characteristics for at least 1 hour in cases in which radiotracer leakage was detected.

In general, anterior abdominal images were obtained to demonstrate radiotracer leakage from the gut. Images of the thyroid and salivary glands were also obtained at 30 minutes after injection and when we observed abnormal accumulation of radiotracer in the gut to measure the free pertechnetate. A 99mTc HSA scan was considered positive for PLE if there was visible tracer exudation in the gut. Moreover, we compared the luminal transit pattern in each patient’s serial images to identify the source of leakage.

The scans were assessed independently by two nuclear medicine physicians (N.T.C., B.F.L.) who were unaware of any clinical details. The scans in patients suspected of having PLE and the scans in the control subjects were given to the two physicians in a random order. Interobserver variability was recorded, and Cohen’s {kappa} statistic (SPSS for Windows release 7.0; SPSS, Chicago, Ill) was calculated. Interobserver disagreements were resolved by joint discussion between observers. The scans were compared with the final diagnosis based on the biopsy findings, culture findings, and clinical follow-up.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Normal Distribution: Control Subjects
99mTc HSA scintigraphy revealed no radiotracer leakage from the gastrointestinal tract and no tracer accumulation in the thyroid and salivary glands in all 12 control subjects. Scintigraphy with 99mTc HSA (Fig 1) showed normal accumulations of radiotracer in the liver, spleen, kidneys, and large veins.



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  		Figure 1. Anterior scintigram obtained in a control subject 1 hour after injection of 99mTc HSA reveals no radiotracer leakage from the gastrointestinal tract.

 
Localization of Protein Loss: Patients
The clinical details, laboratory data, and 99mTc HSA scintigraphic results in the 26 patients are summarized in the Table. All of the patients had hypoalbuminemia. Tests for occult bleeding were negative in all patients. Patients 18 and 22 had proteinuria. Levels of GOT were elevated in 11 patients, and levels of GPT were elevated in five patients. The site of protein loss was identified on sequential images in 26 examinations: two cases in both the small and large bowels and in the stomach, with biopsy proof for one (Fig 2); seven cases in the small bowel; 10 cases in the large bowel; and seven cases in both the small and large bowels (Fig 3). Patient 18 underwent repeat 99mTc HSA scintigraphy despite the initial negative result because of our strong clinically based suspicions of PLE. The repeat study showed positive findings. Seven of the 26 examinations with positive findings showed no abnormalities until images were obtained 24 hours after injection. One illustrative example (patient 17) is shown in Figure 4. None of the 27 scans showed uptake in the thyroid or salivary glands. No adverse reactions secondary to 99mTc HSA were noted in any of the patients or control subjects.


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  		Clinical Characteristics and Imaging Results in 26 Patients Clinically Suspected of Having Protein-Losing Enteropathy
 


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  		Figure 2a. Patient 1. Anterior scintigrams demonstrate PLE in a patient with systemic lupus erythematosus at (a) 60 minutes and (b) 2 hours after intravenous injection of 99mTc HSA. Involvement of the stomach and distal transverse and descending colon (arrows) is noted and confirmed with biopsy findings. (c) Scintigram obtained 30 minutes after intravenous injection of 99mTc HSA shows that free pertechnetate did not concentrate in the thyroid and salivary glands.

 


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  		Figure 2b. Patient 1. Anterior scintigrams demonstrate PLE in a patient with systemic lupus erythematosus at (a) 60 minutes and (b) 2 hours after intravenous injection of 99mTc HSA. Involvement of the stomach and distal transverse and descending colon (arrows) is noted and confirmed with biopsy findings. (c) Scintigram obtained 30 minutes after intravenous injection of 99mTc HSA shows that free pertechnetate did not concentrate in the thyroid and salivary glands.

 


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  		Figure 2c. Patient 1. Anterior scintigrams demonstrate PLE in a patient with systemic lupus erythematosus at (a) 60 minutes and (b) 2 hours after intravenous injection of 99mTc HSA. Involvement of the stomach and distal transverse and descending colon (arrows) is noted and confirmed with biopsy findings. (c) Scintigram obtained 30 minutes after intravenous injection of 99mTc HSA shows that free pertechnetate did not concentrate in the thyroid and salivary glands.

 


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  		Figure 3a. Patient 12. Anterior abdominal scintigrams obtained after intravenous injection of 99mTc HSA in a patient with PLE complicating intestinal lymphoma. (a) Image of the small intestine obtained 2 hours after injection shows diffuse collection of tracer, which indicates the site of protein loss. (b) Image obtained 4 hours after injection shows leaked 99mTc HSA moving into the ascending and transverse colon (arrows).

 


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  		Figure 3b. Patient 12. Anterior abdominal scintigrams obtained after intravenous injection of 99mTc HSA in a patient with PLE complicating intestinal lymphoma. (a) Image of the small intestine obtained 2 hours after injection shows diffuse collection of tracer, which indicates the site of protein loss. (b) Image obtained 4 hours after injection shows leaked 99mTc HSA moving into the ascending and transverse colon (arrows).

 


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  		Figure 4. Patient 17. Anterior scintigram obtained 24 hours after injection of 99mTc HSA shows high activity (arrows) in the ascending colon. Serial scintigrams (not shown) obtained 10, 30, and 60 minutes and 2 and 6 hours after injection showed no radiotracer in the bowel.

 
The sensitivity of 99mTc HSA was 96% (25 of 26) and the specificity was 100% (12 of 12). The CIs for the specificity and sensitivity were 87%–100% and 74%–100%, respectively. The mean margin of error was 7% for the sensitivity and 13% for the specificity. In terms of image evaluation, there was excellent (25 of 27 [93%] interpretations) interobserver agreement in the 27 examinations in patients suspected of having PLE and excellent (11 of 12 [92%] interpretations) interobserver agreement in the 12 examinations in the control subjects. The {kappa} value for both the control subject and patient groups was 0.83 (95% CI: 0.6, 1.0).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
PLE is defined as a condition in which excess protein loss into the gastrointestinal lumen is severe enough to produce hypoproteinemia. It occurs with diseases such as gastric carcinoma, ulcerative colitis, regional enteritis, Whipple disease, tropical and nontropical sprue, and giant hypertrophy of the gastric mucosa. Furthermore, diseases such as constrictive pericarditis, congestive heart failure, intestinal lymphangiectasia, nephrotic syndrome, and systemic lupus erythematosus may also cause protein loss from the gastrointestinal tract without any observable mucosal lesions in the bowel. The mechanism of the loss of plasma protein into the gastrointestinal tract in these diseases is not yet fully understood. The postulated mechanisms are (a) the increased permeability of capillary walls, which leads to exudation of plasma, or (b) local lymphatic obstruction and stasis secondary to the formation of granulomatous and fibrous tissue (1).

The previously reported materials used for the detection of protein loss have many limitations, such as rapid reabsorption of the radiolabel (2), unstable protein binding both in vivo and in vitro, and limited availability (3,4). The need for measurement of fecal radioactivity over 3–4 days has also been a drawback with some of the methods in which these materials are used. Imaging with other radioisotope-labeled materials such as 111In chloride (5) and 111In transferrin (6–8) has been reported, but 99mTc is more widely available and is simple to use. 99mTc dextran (10,12), however, can occasionally produce an anaphylactic reaction. Also, a variety of adverse reactions, albeit uncommon, have been reported with 99mTc HSA, including nausea, vomiting, erythema, flushing, hypotension, dyspnea, tachycardia, dizziness, and abdominal pain (26).

It is not possible with 99mTc dextran and 99mTc human immunoglobulin (11) to easily differentiate PLE from localized bowel loop inflammation if there is no luminal transit. No published report has shown that 99mTc HSA could accumulate in inflamed intestines. HSA is available in some countries, including Taiwan, but it is not currently available in the United States. A recent alternative approach in which {alpha}1-antitrypsin clearance is used proved to be a sensitive way of detecting PLE, but again, it depends on accurate fecal collection (13). Furthermore, it cannot be used to detect protein loss from the stomach.

99mTc HSA, used to image PLE since 1986, is relatively stable in vivo (14). We did not see any in vivo breakdown of 99mTc HSA, as evidenced by thyroid or salivary gland depiction in the 26 patients and 12 control subjects in our study. Individuals without gastrointestinal protein loss—in this instance, the 12 control subjects—did not show any evidence of radioactivity in the gut, which suggests that the chance of a false-positive finding is minimal. In addition, our results suggest high sensitivity for 99mTc HSA in imaging PLE because 99mTc HSA abdominal scintigraphy demonstrates the site of protein loss.

This result is in contrast to that obtained in one study (15) in which PLE was localized in only four of six patients, and 99mTc HSA scintigraphy was performed at only 30 and 90 minutes after injection. Authors of another study (16) detected PLE in 12 of 18 children but gave no data about the six negative scan results, nor did they state whether 24-hour imaging was being performed. We think the distinct results can be attributed to two possible causes: (a) different amounts of protein loss from the gastrointestinal tract, and (b) the performance of 24-hour imaging to document the sites of protein loss in our study. Seven of the 26 patients with positive findings in our study had evidence of protein loss into the bowel only on the image obtained 24 hours after injection. These results are in agreement with those of two previous reports (17,18) in which images were also obtained 24 hours after injection; the site of protein loss was detected in six of six and three of three patients, respectively.

Serial imaging for up to 24 hours is useful in detecting protein loss from the gut, possibly because of the intermittent nature of this protein loss. We also found 99mTc HSA useful in viewing the entire gastrointestinal tract at one time to permit detection of multiple potential sites of protein loss. Moreover, 24-hour serial imaging studies with 99mTc HSA in the 12 control subjects produced 12 true-negative studies.

Active bleeding in the gastrointestinal tract may result in a false-positive 99mTc HSA scintigram (19) because radiotracer is lost into the bowel lumen along with blood. Because none of the patients in our study (Table) had any occult or fresh blood in their stool, gastrointestinal bleeding did not affect the scintigraphic interpretation in this study. Two of the patients in our study had proteinuria. Kluthe et al (27) suggested that gastrointestinal protein loss possibly plays an important role in the development of hypoproteinemia in the presence of proteinuria. PLE was detected with 99mTc HSA in these two patients. The initial scan in patient 18 was normal, but because of our strong clinically based suspicions of PLE, repeat scanning was performed, and the site of protein loss from the gut was located. The initial study may have given a false-negative result because of the intermittent nature of protein loss from the gut.

Nineteen of the patients in our study had chronic hepatitis B. Among these patients, two had normal levels of GOT and GPT, six had elevated levels of GPT, and 12 had elevated levels of GOT. The hepatic dysfunction, however, appeared to be mild, judging from the diagnostic images and serum biochemistry results. Thus, the hepatic disease in these patients did not seem to play a role in the development of their hypoproteinemia, and 99mTc HSA successfully depicted PLE in all of these patients.

We attempted 99mTc HSA for scintigraphy, and this technique was successful in localizing the protein loss in the gut. We found 99mTc HSA to be an ideal tracer for scintigraphy because there is no need to prepare patients beforehand and because of its in vivo stability, lack of serious side effects, high sensitivity, rapid results, wide availability, allowance of monitoring of the entire gastrointestinal tract continuously over several hours, and lower cost than other radiotracers. In addition, 24-hour imaging can increase the detection rate for PLE. We believe that 99mTc HSA with serial imaging for up to 24 hours is an ideal procedure for localization of protein loss in the gut, and we recommend that it be used in suspected cases of PLE.


   ACKNOWLEDGMENTS
 
The authors thank Shan-Tair Wang, PhD, for his statistical analysis, Rei-Seng Sheu, MD, and Ying-Fong Huang, MD, for their useful comments, and Kuei-Lan Chang, MSc, Show-Lan Ju, BS, Jin-Ya Chen, BS, Fan-Ping Liu, BS, Su-Min Chang, BS, and Chuan-Hsiao Li, BS, for their technical assistance. We thank Bill Franke, MA, for proofreading and revising the English.


   FOOTNOTES
 
Abbreviations: GOT = glutamic-oxaloacetic transaminase, GPT = glutamic-pyruvic transaminase, HSA = human serum albumin, PLE = protein-losing enteropathy

Author contributions: Guarantors of integrity of entire study, N.T.C., B.F.L.; study concepts, N.T.C., B.F.L.; study design, S.J.H., J.M.C., G.C.L., H.S.Y.; literature research, N.T.C.; clinical studies, S.J.H., J.M.C.; data acquisition and analysis/interpretation, N.T.C., B.F.L.; statistical analysis, N.T.C., B.F.L.; manuscript preparation, N.T.C., B.F.L.; manuscript definition of intellectual content, S.J.H., J.M.C., G.C.L., H.S.Y.; manuscript editing, N.T.C., B.F.L.; manuscript revision/review, all authors; manuscript final version approval, B.F.L.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 

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