Association between technetium-99m albumin scintigraphy-based severity of protein-losing enteropathy and patient characteristics and laboratory data

doi:10.21203/rs.3.rs-7088989/v1

Objective

This study aimed to demonstrate the differences in Technetium-99m albumin scintigraphy findings for patients with protein-losing enteropathy (PLE) associated with their characteristics and laboratory data.

Methods

Eighteen patients with PLE were grouped into two based on two mechanisms: direct mucosal damage and failed lymph drainage. Scintigraphy images were divided based on the timing of acquisition: dynamic images obtained within the first hour; and images obtained at 2, 4, 6, and 24 h after starting the examination. The intensity of tracer uptake was graded as follows: 3 (marked uptake equal to or greater than the liver level), 2 (moderate uptake less than liver and greater than kidney levels), 1 (mild uptake less than kidney level), and 0 (negative). The grades at each timepoint for the two groups were compared using the Mann-Whitney U test. The associations between the grades and fecal alfa-1-antitrypsin and serum total protein concentrations were evaluated using Pearson correlation coefficients.

Results

Of 18 patients, 7 had PLE due to failed lymph drainage. The direct mucosal damage and failed lymph drainage groups had significantly different fecal alfa-1-antitrypsin concentrations (43.5 ± 29.6 [range, 11–115] vs. 208.7 ± 66.0 [range, 124–311], respectively; P < 0.001) and scintigraphy-based severity at 24 h (1.2 ± 0.8 [range, 1–3] vs. 2.8 ± 0.4 [range, 2–3], respectively; P = 0.007). The fecal alpha-1-antitrypsin concentration was positively correlated with the scintigraphy-based severity at 6 h (r = 0.499, P = 0.049) and 24 h (r = 0.747, P = 0.002). However, the serum protein concentration was negatively correlated with the scintigraphy-based severity at 6 h (r = -0.587, P = 0.017).

Conclusions

The scintigraphy-based severity at 6 and 24 h and the fecal alpha-1 antitrypsin concentrations were higher for patients with PLE due to failed lymph drainage mechanisms than for those with PLE due to direct mucosal damage. Scintigraphy can help localize the leakage point and determine disease severity to guide PLE management.

Protein losing enteropathy

Fontan

nuclear medicine

scintigraphy

Technetium-99m Albumin scintigraphy

Protein-losing enteropathy (PLE) is rare condition characterized by protein loss into the gastrointestinal tract [1–3]. The two principal underlying pathophysiological mechanisms are direct mucosal damage (either erosive or nonerosive) and failed lymph drainage, causing backflow through the epithelium into the lumen [3]. Patient outcomes and treatment vary based on these mechanisms [4–7]. In addition, the severity of laboratory findings of the patients is associated with PLE recurrence after treatment [4].

The fecal alpha-1-antitrypsin concentration and technetium-99m albumin scintigraphy findings are important for diagnosing this PLE [8–14]. Fecal alpha-1-antitrypsin is usually the first examination for patients with suspected PLE, and it can predict the amount of protein lost into the intestine [3, 15, 16]. Technetium-99m albumin scintigraphy is also useful for diagnosing PLE, as it helps visualize the tracer in the gastrointestinal tract and detect the leakage point [8–10, 12, 15, 17]. However, systematic studies on the associations of the severity of patient conditions and laboratory data are lacking. Furthermore, few studies have discussed the severity of scintigraphy findings [10].

The purpose of this study was to demonstrate the differences in Technetium-99m albumin scintigraphy findings for PLE cases secondary to direct mucosal damage and failed lymph drainage. The study also aimed to describe the association between the scintigraphy-based severity of PLE and laboratory data of patients.

Ethical considerations

This retrospective study was conducted in accordance with the principles of the Declaration of Helsinki. The ethics committee of our institution approved this study and waived the requirement for informed consent due to its retrospective design.

Study population

We reviewed the medical database of our hospital and included patients with suspected PLE who underwent Technetium-99m albumin scintigraphy between April 2000 and May 2025. Twenty patients were enrolled in this study. Only the results of the first examination were evaluated for patients who underwent this examination multiple times.

The exclusion criteria were as follows: unreviewed medical records (n = 2).

Patient data

Suspected PLE

PLE has various symptoms, including hypoproteinemia, edema, nutritional deficiency, and recurrent infection [2, 3, 10] The fecal alpha-1-antitrypsin concentrations were determined for these cases, and a spot value greater than 10 mg/dl indicated PLE positivity or warranted its suspicion. The clearance was better for evaluating the amount of protein lost. However, it was difficult to calculate the protein loss for patients in our hospital using the amount of feces in one day.

Patient characteristics and laboratory data

Following data were recorded; sex, age of scintigraphy examination, underlying disease associated with PLE and spot value of alfa-1 antitrypsin. In addition, serum albumin and serum protein levels obtained on the same day of scintigraphy examination were recorded.

Patient classification

Patients were classified into two groups based on the mechanism: direct mucosal damage or failed lymph drainage. Direct mucosal damage includes inflammatory and ulcerative diseases, infections, malignancy, hypertrophic gastropathies, eosinophilic gastroenteropathies, vasculitic disorders. Failed lymph drainage includes primary lymphangiectasia and secondary lymphangiectasia such as obstructive or elevated lymph pressure caused by congenital heart disease or syndrome [1–3].

Technetium-99m albumin scintigraphy

Equipment and examination protocol: Technetium-99m Albumin scintigraphy was performed in patients with suspected PLE, who had symptoms such as diarrhea, generalized edema, low serum protein, low serum albumin, or/and high fecal α-1-antitrypsin. Doses of 50 MBq of Technetium-99m labeled human serum albumin-DTPA (99mTc-HSAD) were determined based on the Japanese Society of Nuclear Medicine guidelines (administration dose range 73.1–740 MBq)[18]. A gamma camera (Siemens Symbia E or T16; Siemens Medical Systems Inc., Hoffmann Estates, IL, USA) equipped with a fan beam collimator was used. A 60-min anterior dynamic sequence captured the dynamic phase (Figs. 3, 4, 5), followed by the acquisition of static anterior, posterior, and both right and left lateral images at 2, 4, 6, or 24 h post-injection. Previous images could not be obtained in some cases due to those general conditions. For cases with difficulty assessing bowel activity in static images, single-photon emission computerized tomography (SPECT) scans were obtained. The dynamic sequence was obtained with a 64 × 64 matrix size and at sampling times of 30 s. All static images were obtained with a 512 × 512 matrix size and at varying sampling times (300 s at 3 h, 300 s at 6 h, and 900 s at 24 h).

Evaluation of scintigraphy results: The examination results were evaluated based on previous studies [10, 14, 16]. The timing of image evaluations varied across studies, which may lead to confusion when comparing the studies [10, 14, 16]. Therefore, we classified the timing of imaging evaluations based on the time of acquisition as follows: dynamic images acquired within the first hour; images obtained at 2 h; images obtained at 4 h; images obtained at 6 h; and images obtained at 24 h after the commencement of the examination. The intensity of tracer uptake in the intestinal tract was graded as follows: 3, marked uptake equal to or greater than that in the liver (Fig. 1); 2, moderate uptake less than that in the liver and greater than that in the kidney (Figs. 1, 2); 1, mild uptake less than that in the kidney (Figs. 2, 3); and 0, negative uptake (Figs. 1–3)[10]). For cases with greater uptake in the kidney than in the liver, marked uptake was defined as equal to or greater than that in the kidney, moderate uptake as less than that in the kidney and greater than that in the liver, and mild uptake as less than that in the liver. The main leakage points of PLE were classified into the small intestine (Figs. 1, 3) and large intestine (Fig. 2). The presence (Figs. 1, 2) or absence (Fig. 3) of tracer movement to the distal large intestine was evaluated.

Review process: Two pediatric radiologists with 25 and 10 years of clinical experience in pediatric nuclear medicine independently reviewed all images of technetium-99m albumin scintigraphy using a 1600 × 1200 picture archiving and communication system (PACS; GE Healthcare). Discrepancies in interpretation between the radiologists were resolved by consensus.

Statistical analysis

The data are presented as the mean ± standard deviation. Statistical significance was set at P < 0.05 (two-sided) for all tests. All analyses were performed using IBM SPSS Statistics for Windows version 24 (IBM Corp., Armonk, NY, USA).

The characteristics of the patients with PLE caused by direct mucosal damage and those with PLE caused failed lymph drainage, including sex, age, and scintigraphy findings such as main leakage point of PLE and presence or absence of tracer movement to distal large intestine, were compared using Fisher’s exact test and the Mann-Whitney U test. The uptake intensities for each timing were compared for the two groups using the Mann-Whitney U test.

The associations between those grades and age and serum albumin, serum protein, and fecal alpha-1-antitrypsin concentrations were evaluated using Pearson correlation coefficients.

Patient characteristics

The patient characteristics are summarized in Table 1. Eighteen patients were enrolled in this study. Of these, 11 had direct mucosal damage, and seven had failed lymph drainage. The underlying diseases or final diagnoses of the 11 patients with direct mucosal damage were enteritis due to infection by unknown pathogens in eight patients, cytomegalovirus infection in one patient, and systemic lupus erythematosus or juvenile idiopathic arthritis in one patient each. Of the seven patients with failed lymph drainage, five had undergone the Fontan operation, and two had right-sided hypertension due to congenital heart disease before the Fontan operation. Nine patients were male and nine were female. Their average age was 6.3 ± 6.7 [range, 0.3–25.5] years. Their average serum total protein, serum albumin, and fecal alpha-1-antitrypsin concentrations were 4.9 ± 1.1 [range, 3.5–7.1] g/dl, 2.6 ± 0.7 [range, 1.6–4.1] g/dl, and 107.8 ± 94.4 [range, 11–311] mg/dl, respectively.

Table 1. Patient characteristics

No	sex	Age (years)	Serum Albumin (g/dl)	Serum protein (g/dl)	Fecal alfa-1-antitrypsin (mg/dl)	Underlying disease/diagnosis	Mechanism of PLE	Leakage point	Grade of tracer intensity in each timing*					Tracer movement into distal large intestine	Fig
No	sex	Age (years)	Serum Albumin (g/dl)	Serum protein (g/dl)	Fecal alfa-1-antitrypsin (mg/dl)	Underlying disease/diagnosis	Mechanism of PLE	Leakage point	-1 h	2 h	4 h	6 h	24 h	Tracer movement into distal large intestine	Fig
1	M	7.5	2.6	4.8	311	After Fontan operation	failed lymph drainage	Small intestine	0	2	3	3	3	Present	Fig 1
2	M	1.2	3	5.2	269	Right side hypertension before Fontan operation	failed lymph drainage	Small intestine	0	1	2	**	**	Present
3	M	10.7	2.4	4.6	220	After Fontan operation	failed lymph drainage	Small intestine	0	０	2	3	3	Present
4	F	3.0	2.2	3.8	210	After Fontan operation	failed lymph drainage	Small intestine	0	0	０	2	3	Present
5	M	4.3	2.5	4.3	182	Right side hypertension before Fontan operation	failed lymph drainage	Large intestine	0	**	２	2	**	Absent
6	M	3.6	1.9	3.6	145	After Fontan operation	failed lymph drainage	Small intestine	2	2	２	2	3	Present
7	M	4.3	2.1	4.3	124	After Fontan operation	failed lymph drainage	Small intestine	2	２	３	3	2	Present
8	M	3.7	1.6	3.5	115	Enteritis due to infection	direct mucosal damage	Small intestine	0	2	2	3	1	Absent
9	M	3.4	3.5	6.2	60	Enteritis due to infection	direct mucosal damage	Small intestine	0	0	0	1	2	Present
10	F	25.5	2.3	4.8	57	Enteritis due to infection	direct mucosal damage	Small intestine	0	0	１	1	1	Present
11	F	16.2	3.5	5.6	56	Juvenile idiopathic arthritis	direct mucosal damage	Large intestine	0	０	２	2	1	Present	Fig 2
12	F	14.8	2.4	4.4	53	Systematic lupus arthropathy	direct mucosal damage	Small intestine	2	2	３	3	3	Present
13	F	0.3	2.5	4	35	Cytomegalovirus infection	direct mucosal damage	Small intestine	3	３	３	3	**	Present
14	F	9.1	4.1	7.1	33	Enteritis due to infection	direct mucosal damage	Small intestine	0	０	１	1	1	Present
15	F	2.6	3.3	7	21	Enteritis due to infection	direct mucosal damage	Small intestine	0	0	１	1	1	Absent	Fig 3
16	M	2.5	3.1	6	21	Enteritis due to infection	direct mucosal damage	Small intestine	1	2	**	**	**	Present
17	F	0.6	2.1	4.3	17	Enteritis due to infection	direct mucosal damage	Small intestine	0	0	１	1	1	Absent
18	F	1.0	1.7	3.8	11	Enteritis due to infection	direct mucosal damage	Small intestine	0	0	２	2	1	Absent

F; Female, M; male.

*Images were classified into dynamic, 2 h, 4 h, 6 h, and 24 h based on the timing of acquisition. For each timing, the intensity of tracer uptake in the intestinal tract was graded as follows: 3, marked uptake equal to or greater than liver level; 2, moderate uptake less than liver and greater than kidney levels; 1, mild uptake less than kidney level; and 0, negative uptake.

**indicates that images were not obtained at this timing due to patient conditions or imaging result obtained before timing.

Scintigraphy

The dynamic phase was obtained for all patients during scintigraphy. However, images obtained at 2 and 24 h for one patient were not obtained due to the condition of the patient. Three patients did not have images obtained at some of the timepoints due to evidence of PLE before the respective timing. One lacked images at 6 and 24 h; one lacked images at 24 h; and another lacked images at 4, 6, and 24 h.

The main leakage points of PLE were the small intestine for 16 patients and the large intestine for 2 patients. Tracer movement to the distal large intestine was detected in 12 patients.

The grades of severity for scintigraphy at 2, 4, 6, and 24 h were 0.8 ± 1.2 [range, 0–3], 1.3 ± 1.0 [range, 0–3], 1.8 ± 1.0 [range, 0–3], 2.0 ± 0.9 [range, 1–3], and 1.8 ± 1.0 [range, 1–3], respectively.

Comparison of patient characteristics and scintigraphy-based severity

Table 2 summarizes the comparison of the characteristics of the patients and scintigraphy severity for the two etiological groups PLE. Significant differences were observed in the fecal alpha-1-antitrypsin concentration and scintigraphy severity during the delayed and super-delayed phases (alpha-1-antitrypsin in patients with direct mucosal damage vs those with failed lymph drainage: 43.5 ± 29.6 [range, 11–115] vs. 208.7 ± 66.0 [range, 124–311], P < 0.001; severity in 6-h image for direct mucosal damage vs failed lymph drainage : 1.6 ± 0.8 [range, 1–3] vs. 2.6 ± 0.5 [range, 2–3], P = 0.031; severity in 24-h image for direct mucosal damage vs failed lymph drainage =: 1.2 ± 0.8 [range, 1–3] vs. 2.8 ± 0.4 [range, 2–3], P = 0.007). No significant differences were observed in sex, age, serum protein concentration, albumin concentration, location of the main leakage point, tracer movement into the distal large intestine, and scintigraphy-based severity obtained at other times.

Table 2
Comparison of the severity of scintigraphy findings between patients’ characteristics and scintigraphy results
		Mechanism of PLE
		direct mucosal damage	failed lymph drainage	P
		11	7
Sex female/male		8/3	1/6	0.050
Age		7.2 ± 8.2 [range, 0.3–25.5]	4.9 ± 3.2 [range, 1.2–10.7]	0.724
Total protein		5.2 ± 1.3 [range, 3.8–7.1]	4.4 ± 0.6 [range, 3.6–5.2]	0.285
Total albumin		2.7 ± 0.8 [range, 1.6–4.1]	2.4 ± 0.4 [range, 1.9–2.5]	0.425
Fecal alfa-1 antitrypsin		43.5 ± 29.6 [range, 11–115]	208.7 ± 66.0 [range, 124–311]	< 0.001
Technetium-99m labeled human serum albumin-DTPA
Main location of leakage point (small intestine/large intestine)		10/1	6/1	> 0.999
Severity of scintigraphy*	− 1 h	0.5 ± 1.0 [range, 0–3]	0.6 ± 1.0 [range, 0–2]	> 0.999
	2 h	0.8 ± 1.2 [range, 0–3]	1.2 ± 1.0 [range, 0–2]	0.525
	4 h	1.8 ± 0.8 [range, 1–3]	2.0 ± 1.0 [range, 0–3]	0.536
	6 h	1.8 ± 0.9 [range, 1–3]	2.5 ± 0.5 [range, 2–3]	0.147
	24 h	1.2 ± 0.8 [range, 1–3]	2.8 ± 0.4 [range, 2–3]	0.007
Movement of tracer into distal large intestine (present/absent)		7/4	6/1	0.316
*Images were classified into dynamic, 2 h, 4 h, 6 h, and 24 h based on obtaining timing. In each timing, the intensity of tracer uptake in the intestinal tract was classified into the following grades: 3, marked uptake as equal to or greater than the liver; 2, moderate uptake as less than the liver and greater than the kidney; 1, mild uptake as less than the kidney; and 0, negative uptake.

Correlation between scintigraphy-based severity and laboratory data

Table 3 summarizes the correlations between the scintigraphy-based severity and laboratory data. The fecal alpha-1-antitrypsin concentration had moderate positive correlations with scintigraphy-based severity at 6 h (r = 0.499, P = 0.049) and 24 h (r = 0.747, P = 0.002). The serum protein concentration had a significant negative correlation with scintigraphy-based severity at 6 h (r = -0.587, P = 0.017), but no significant correlations were observed at other time points. Albumin concentration did not also have a significant correlation with scintigraphy-based severity.

Table 3
Associations between scintigraphy-based severity and laboratory findings
		Severity of scintigraphy in each timing*
		-1 h	2 h	4 h	6 h	24 h
Age		-0.132 (0.601)	-0.239 (0.356)	-0.039 (0.811)	-0.077 (0.778)	0.026(0.929)
Laboratory data	Serum protein concentration	-0.317 (0.199)	-0.390 (0.122)	-0.246 (0.341)	-0.587 (0.017)**	-0.256 (0.378)
	Serum albumin concentration	-0.288 (0.363)	-0.310 (0.226)	-0.154 (0.556)	-0.470 (0.066)	-0.111 (0.705)
	Fecalα-1-antitrypsin concentration	-0.195 (0.438)	0.155 (0.553)	0.254 (0.554)	0.499 (0.049)**	0.747 (0.002)**
*Images were classified into dynamic, 2 h, 4 h, 6 h, and 24 h based on the timing of acquisition. For each timing, the intensity of tracer uptake in the intestinal tract was graded as follows: 3, marked uptake equal to or greater than liver level; 2, moderate uptake less than liver and greater than kidney levels; 1, mild uptake less than kidney level; and 0, negative uptake.
** indicates significant association between laboratory data and severity of scintigraphy findings

In our limited cohort, scintigraphy-based severity obtained at 24 h and fecal alpha-1 antitrypsin concentrations were higher for patients with PLE due to failed lymph drainage than for those with PLE due to direct mucosal damage. The scintigraphy-based severity obtained at 6 and 24 h tended to correlate with spot fecal alpha-1-antitrypsin concentration. Technetium-99m albumin scintigraphy provided information on the location of leakage and the severity of protein loss in the gastrointestinal tract. This information would be useful for managing patients with PLE.

The failed lymph drainage mechanisms of PLE are classified into primary (intestinal lymphangiectasia due to defects intrinsic to the lymphatic system) and secondary (external obstruction to lymph vessels or cardiovascular disease that impairs lymphatic flow)[1–3]. All patients with PLE due to failed lymph drainage in our cohort had congenital heart disease with Fontan operation or right-sided hypertension [1, 3, 5, 19]. These conditions impair lymphatic flow and extend to the entire intestine. Moreover, follow-up for such patients tends to be prolonged from birth, during which they are exposed to impaired lymphatic flow [5, 20, 21]. Therefore, these cases had severe scintigraphy results and fecal alpha-1 antitrypsin concentrations compared to those with mucosal damage that may be due to segmental lesions and are usually acquired conditions and not congenital conditions [4, 6, 7, 22–24]. PLE is one of the most important complications in patients with Fontan operation due to its high mortality rate of 50%[25], and its severity may be associated with the scintigraphy-based severity.

Takeda et al. reported three cases of PLE associated with fecal alpha-1 antitrypsin concentration and scintigraphy-based severity. Their images demonstrated the correspondence between the scintigraphy-based severity and concentration of fecal alpha-1 antitrypsin [14]. Halaby et al. reported that images obtained more than 2 h after the dynamic phase had higher tracer accumulation within the gastrointestinal tract [10]. These findings are consistent with our results. However, the findings of a few cases in our cohort did not match the severity based on laboratory data and scintigraphy results. Protein-losing enteropathy is characterized by nonselective depletion of all plasma proteins, and the condition of the patients is affected by the turnover rates of various types of proteins, such as albumin and immunoglobulin [2, 3]. Technetium-99m albumin scintigraphy visualizes only the depletion of albumin, not all plasma protein [9, 10, 12, 14, 17]. This may explain the differences in our results.

The timing of scintigraphy is important. The dynamic phase obtained within 1 h represents both intestinal perfusion and tracer leakage into the intestinal tract. Images obtained after 2 h indicate the amount of tracer in the intestinal tract, while those obtained at 6 and 24 h tend to help visualize its accumulation. The amount of leakage into the intestinal tract may be associated with protein loss and laboratory abnormalities. Fecal alpha-1-antitrypsin concentrations directly reflect protein leakage into the stool, whereas albumin and protein concentrations reflect various patient conditions, such as prolonged inflammation and malnutrition. Therefore, it was understandable to note a significant positive correlation only between fecal alpha-1-antitrypsin concentrations and severity of 24-h scintigraphy and not between serum albumin and protein concentrations. Only the negative correlation between 6-h scintigraphy and serum protein concentration was not explained.

Bhatgar et al. reported that scintigraphy-based severity was higher for patients with direct mucosal damage than for those with failed lymph drainage [8]. Three patients with failed lymph drainage were included in this study: one had congenital heart disease, and two had lymphangiectasia without cardiac anomalies. These results suggest that patients with failed lymph drainage and localized lesions may not have severe scintigraphy findings.

The movement of the tracer into the distal large intestine is an important finding for the diagnosis of PLE via technetium-99m albumin scintigraphy. Tracer movement is usually easily detected in cases with marked tracer uptake in the intestine.

Scintigraphy was useful in our study, but it had some limitations. First, we included only 18 patients with PLE. We did not include patients with congenital intestinal lymphangiectasia. We only included patients with congenital heart disease in the failed lymph drainage group. Studies involving more patients with various underlying diseases are needed. Second, we used spot fecal alpha-1-antitrypsin tests instead of calculating its clearance. It was difficult to correct the total fecal alpha-1-antitrypsin concentrations in our patients at the children's hospital for one day. Third, we did not include patients who had not undergone fecal alpha-1-antitrypsin testing or had negative results. Fecal alpha-1-antitrypsin testing is an important screening examination for PLE [2, 3]. However, Chau et al reported the diagnostic performance of scintigraphy for PLE was superior to that of fecal alpha-1-antitrypthin concentration [16]. Therefore, we could not evaluate the scintigraphy-based severity for patients with negative fecal alpha-1-antitrypsin results. Further studies should include these patients.

Funding

None.

Acknowledgement

We would like to thank Editage [http://www.editage.com] for editing and reviewing this manuscript for English language

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Association between technetium-99m albumin scintigraphy-based severity of protein-losing enteropathy and patient characteristics and laboratory data

Status:

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Abstract

Objective

Methods

Results

Conclusions

Figures

INTRODUCTION

MATERIAL AND METHODS

Statistical analysis

RESULTS

DISCUSSION

Declarations

Funding

Acknowledgement

References

Status:

Journal Publication

Version 1