Incidence and characteristics of 18F-FDG uptake in brown adipose tissue induced by β3-adrenergic receptor agonist treatment in 18F-FDG PET/CT images in elderly patients over 50 years of age

doi:10.21203/rs.3.rs-3326786/v1

Objective

The incidence of ¹⁸F-fluorodeoxyglucose (FDG) uptake in brown adipose tissue (BAT) in elderly patients and the characteristics of ¹⁸F-FDG uptake in BAT induced by β3-adrenergic receptor (β3-AR) agonist treatment remain unclear. The purpose of this study was to clarify the incidence of radiotracer uptake during ¹⁸F-FDG positron emission tomography (PET)/computed tomography (CT) in patients over 50 years of age in daily clinical practice, and to explore the characteristics of ¹⁸F-FDG uptake in BAT induced by β3-AR agonist treatment.

Methods

We retrospectively reviewed the ¹⁸F-FDG-PET images of 29 patients over 50 years of age who showed ¹⁸F-FDG uptake in BAT. We analyzed the association between β3-AR agonist treatment and ¹⁸F-FDG uptake in BAT by focusing on the following 8 regions - the cervical, periclavicular, axillary, mediastinal, paraspinal, para-abdominal aortic, perirenal, and perisplenic regions.

Results

The results revealed a significant difference in the FDG uptake in the BAT of the perirenal region between patients who were under and not under β3-AR agonist treatment at the time of the PET examination. Comparison of the standardized uptake value maximum (SUVmax) also showed a significant difference in ¹⁸F-FDG uptake in the BAT of the perirenal region between patients who were under and not under β3-AR agonist treatment at the time of the PET examination (p = 0.001).

Conclusion

In patients over 50 years of age who show ¹⁸F-FDG uptake in BAT, increased ¹⁸F-FDG uptake due to the influence of β3-AR agonists should be considered. Presence of ¹⁸F-FDG uptake in the BAT of the perirenal region may serve as a clue to considering β3-AR agonist-induced uptake.

18F-FDG-PET

brown adipose tissue

overactive bladder

vibegron

mirabegron

One of the tissues of the body that shows physiological ¹⁸F-fluorodeoxyglucose (FDG) uptake is the hypermetabolic brown adipose tissue (BAT), which expresses the heat-producing protein uncoupling protein 1 (UCP1) and breaks down fat to produce heat and contribute to maintenance of the body temperature [1]. BAT UCP1-mediated heat production is associated not only with increased fat utilization, but also with increased glucose utilization [2]. Owing to enhanced glucose metabolism, BAT shows increased ¹⁸F-FDG uptake on ¹⁸F-FDG positron emission tomography (PET)/computed tomography (CT) [3]. BAT cells, which are abundant in the adipose tissue of newborns and children under 1 year of age are reported to be replaced by white adipocytes with advancing age [4–7]. Therefore, it is assumed that BAT is only present in very small amounts in adults, and that its physiological role in adults is negligible.

In daily clinical practice, increased physiologic uptake of FDG is occasionally encountered in¹⁸F-FDG PET/CT scans of elderly patients. This has been reported to be primarily due to enhanced glucose metabolism in BAT occurring for the purpose of heat production in response to cold stimuli [8–11]. In addition, recently, there have been reports of increased radiotracer uptake on ¹⁸F-FDG PET images in elderly patients under treatment with β3-adrenergic receptor (β3-AR) agonists, which are known to enhance glucose metabolism in the BAT [12–14]. β3-AR agonists are widely used as first-line agents for patients with overactive bladder (OAB) because they have fewer side effects than anticholinergic agents. However, there are few reports on the ¹⁸F-FDG PET/CT findings of β3-AR agonist-induced BAT uptake. It is important for nuclear medicine physicians and radiologists interpreting ¹⁸F-FDG PET/CT images to be aware that increased FDG uptake in BAT could be induced by β3-AR agonists. β3-AR agonists are also promising anti-obesity and anti-diabetes drugs, which may underscore the importance of elucidating the effects of β3-AR agonists on the glucose uptake in BAT in FDG-PET images [15].

The purpose of this study was to clarify the incidence of increased glucose uptake in BAT in ¹⁸F-FDG PET/CT images of patients over 50 years of age in daily clinical practice and to explore the characteristics of increased ¹⁸F-FDG uptake in BAT induced by β3-AR agonists.

We retrospectively selected FDG-PET/CT images of patients over 50 years of age which showed increased FDG uptake in BAT from among ¹⁸F-FDG PET/CT scans performed at the National Cancer Center Hospital, Japan. We then checked the drug history of the patients from the clinical records to determine if they were receiving vibegron (Beova®) or mirabegron (Betanis®) as β3-AR agonists at the time of their FDG-PET examinations. Patients with missing data on the drug history were excluded from this study. We also excluded patients in whom the increased ¹⁸F-FDG uptake in the BAT was attributable to excessive catecholamine release from pheochromocytoma or other causes [16, 17]. If a single patient had undergone FDG-PET multiple times, only data from the scanning examination in which increased FDG uptake in the BAT was observed for the first time were adopted. For the patients whose images were finally included in the analysis, information on the age, BMI, and outdoor temperature in Chuo-ku Tokyo, all of which have been reported from previous studies as possible confounding factors, was also collected from the patient records. For outpatients, the outside temperature considered for the study was the outside temperature recorded one hour before the ¹⁸F-FDG injection in the database of the Japan Meteorological Agency [18]. For inpatients, the temperature was considered as 24°C, the temperature of the air-conditioned room in the inpatient wing of the hospital. Since this was a retrospective single-center study, the need to obtain informed consent from the patients was waived by the institutional review board (research proposal number 2018–049).

¹⁸ F-FDG PET/CT image acquisition

For ¹⁸F-FDG PET/CT examination at our hospital, patients are instructed to fast for at least 4 hours prior to the injection of ¹⁸F-FDG. Then, 3–4 MBq/kg of the radiotracer is administered by intravenous injection, depending on the patient height and body weight. After the injection, the patients are asked to rest for 50–70 min prior to acquisition of the images. ¹⁸F-FDG PET/CT imaging is performed using one of two PET/CT scanners, the main one being Discovery 600. Patients are positioned in the supine head-first position. The image acquisition is started from the pelvic region and moved toward the head. The axial field of view contains the body volume from the head to the thigh. Both whole-body CT and the adaptive PET/CT images are reconstructed using time-of-fight ordered-subsets expectation maximization (TOF-OSEM) with two iterations and 16 subsets and point spread function modeling at a dedicated workstation. The voxel size for whole-body PET is 3.125 × 3.125 × 2.780 mm³ (matrix size, 192 × 192). After ensuring correct positioning of the spatial acquisition windows, the whole-body PET/CT image acquisition is initiated at a 2-min acquisition time per bed position. For attenuation correction of the PET data from the PET/CT scanner, the reconstruction software provided by the manufacturer uses attenuation maps generated based on the 3D CT images obtained for every bed position. The procedure for CT-based attenuation correction is implemented in the post-processing software of the scanner and operated automatically. During the PET/CT examination, the room temperature is set at 24℃ to avoid cold stimulation. In addition, thermal insulation measures, such as use of blankets, are adopted according to the wishes of the patient.

Assessments by visual analysis and determination of the SUVmax

One board-certified radiologist-cum-nuclear medicine physician (K.I.) and one board-certified nuclear medicine physician (K.O.) assessed the images for FDG uptake in BAT, by focusing their observation on eight anatomic regions, namely, the cervical, periclavicular, axillary, mediastinal, para-abdominal aortic, paraspinal, perirenal, and perisplenic regions, based on previous reports [6,19]. The ¹⁸F-FDG uptake in BAT was determined by comparing it with the uptake level in the subcutaneous fat of the lumbar region. ¹⁸F-FDG uptake in BAT was distinguished from that by malignant tumors by referring to attenuation-corrected CT images and determined only when the ¹⁸F-FDG uptake was within the fat concentration range (CT value − 100 to 0 HU) on CT. In this study, FDG uptake was determined to be present when FDG uptake was detected in any of these regions. The BAT areas where uptake was observed were visually set as regions of interest (ROI), and the standardized uptake values maximum (SUVmax) in these regions were determined.

Statistical analysis

All the statistical analyses were performed using IBM SPSS Version.22 (IBM Corp., Armonk, NY, USA). For each of the eight BAT regions, Fisher's exact probability test was performed after confirming that more than 20% of all cells had an expected frequency of less than 5 in the cross-tabulation table, considering a positive or negative history of treatment with β3-AR agonists and FDG uptake in BAT as the non-corresponding nominal variables. P values of 0.05 or lower were set as denoting statistical significance.

The SUVmax of ¹⁸F-FDG uptake in each of the eight BAT regions was used as a continuous variable to check for normality by the Shapiro-Wilk test. When normality could not be confirmed, the median value was calculated, and a Mann-Whitney test was performed to compare between the two groups with a positive and negative history of β3-AR agonist treatment.

Patient characteristics

A flow diagram summarizing the selection of patients for the study is shown in Fig. 1. A There was a total of 29 patients whose FDG-PET images showed ¹⁸F-FDG uptake in BAT, after excluding one patient who was diagnosed as having pheochromocytoma. Of the 29 patients, 7 (24.1%) wereβ3-AR agonist (+) group at the time of the ¹⁸F-FDG PET/CT examination (hereinafter, simply PET examination). The clinical parameters are summarized in Table 1. The mean ages of the β3-AR agonist (+) and β3-AR agonist (-) groups were 72.4 years and 66.0 years, respectively (p = 0.173). The mean BMI values of theβ3-AR agonist (+) and β3-AR agonist (-) groups were 20.9 kg/m² and 20.1 kg/m² , respectively (p = 0.543). The outdoor temperature at the time of the PET examination tended to be lower in theβ3-AR agonist (-) group (14.8 ± 8.2°C) than that in theβ3-AR agonist (+) group (21.9 ± 6.3°C), although the difference was not statistically significant (p = 0.052). The difference in the room temperature from the outside temperature at the time of the PET examination was postulated as being the main cause of FDG uptake in BAT in the β3-AR agonist (+) group, although this remains speculative.

Assessments by visual analysis and determination of the SUVmax

Table 2 shows the results of visual evaluation of the presence or absence of ¹⁸F-FDG uptake in the BAT of the eight regions of observation listed above. A significant association between β3-AR agonist treatment and ¹⁸F-FDG uptake was observed only in the BAT of the perirenal region, with no such association observed in any of the other seven regions. Table 3 shows the characteristics of the β3-AR agonist (+) group. ¹⁸F-FDG uptake in the BAT of the paraspinal region was observed in all the patients of the β3-AR agonist (+) group. ¹⁸F-FDG uptake in the BAT of the perirenal region was observed in 6 of the 7 patients of the β3-AR agonist (+) group. On the other hand, none of the patients of this group showed ¹⁸F-FDG uptake in the BAT of the perisplenic region. Typical cases of FDG uptake in BAT among patients who were receiving β3-AR agonist treatment at the time of the PET examination are presented in Fig. 2 and Fig. 3.

The results of the semi-quantitative analysis using SUVmax are shown in Table 2, together with the results of the visual evaluation. A significant difference in the FDG uptake betweenthe β3-AR agonist (+) group and β3-AR agonist (-) group was observed only in the BAT of the perirenal region, with no significant differences observed in any of the other seven regions. These results were consistent with the results of the visual evaluation.

In this study, ¹⁸F-FDG PET/CT images of 29 patients who were older than 50 years of age that showed FDG uptake in the BAT were retrospectively reviewed to evaluate the associations between FDG uptake in the BAT in eight anatomic regions and the history of β3-AR agonist treatment. Our results showed that in the seven cases who were under β3-AR agonist treatment, the pharmacological effects of β3-AR agonists may have led to the FDG uptake in the BAT. FDG uptake was particularly high in the paraspinal and perirenal regions, but only the uptake in the BAT of the perirenal region was statistically significantly different between the patients who were and were not receiving β3-AR agonist treatment at the time of the PET examination.

Among the patients whose images showed ¹⁸F-FDG uptake in BAT, patients who were under β3-AR agonist treatment at the time of the PET examination showed significantly higher FDG uptake in the BAT of the perirenal regions. This finding suggests that the observation of ¹⁸F-FDG uptake in the BAT of the perirenal regions in daily practice may reflect hypermetabolism induced by β3-AR agonist treatment. However, before determining that the ¹⁸F-FDG uptake in the BAT of the perirenal regions may be drug-induced, it is necessary to exclude physiologic uptake by the adrenal glands and pathologic uptake by conditions such as adrenal metastases. It is necessary to refer to the attenuation-corrected CT images to differentiate the BAT uptake from adrenal gland uptake.

On the other hand, while FDG uptake was observed in the BAT of the other regions, including the cervical, periclavicular, axillary, mediastinal, and paraspinal regions in both the patients groups that were and were not receiving β3-AR agonist treatment at the time of the PET examination, no significant differences in the ¹⁸F-FDG uptakes in these regions were observed between the two groups. This finding is consistent with previous reports [20, 21] suggesting that factors such as cold stimulation, besides β3-AR agonist treatment, could enhance FDG uptake by BAT, as described above. The mean outside temperature recorded in the patient group that was receiving β3-AR agonist treatment at the time of the PET examination was 7 degrees Celsius lower as compared with that in the group that was not receiving β3-AR agonist treatment at the time of the PET examination, although the difference was not statistically significant (p = 0.052). It is possible that the level of cold stimulation was not significantly different among the patients in this study, because factors (e.g., clothing and climate) other than the difference between the outdoor temperature and room temperature are also considered to influence the degree of cold stimulation. Increased glucose metabolism of BAT in the six regions other than the perirenal and perisplenic regions appeared to be a common finding in both patients who were and were not receiving β3-AR agonist treatment at the time of the PET examination. On the other hand, it would appear that the BAT in the perirenal and perisplenic regions may be activated to a lesser degree at the room temperatures prevailing in 18F-FDG PET scanning facilities [22].

In a previous study, Cypess AM et al. demonstrated FDG uptake in many BAT areas throughout the body, from the neck and mediastinum, including the perirenal region, to the perirenal, paraspinal, and perihepatic areas, in patients under β3-AR agonist treatment [19]. Our results were consistent with the finding of FDG uptake in the BAT of the perirenal region, but not with the finding of significant FDG uptake observed in the BAT of the spleen and liver areas. This discrepancy could be attributable to differences in the β3-AR agonist doses used between our two studies: 200 mg mirabegron was the mean reported dose from the previous study, which is four times the dose of 50 mg used in clinical practice. The 200-mg dose appears to be sufficient to stimulate BAT in various regions of the body, while the 50-mg dose used for the treatment of OAB can probably only stimulate the BAT in the cervical, axillary, paraspinal, and perirenal regions, but is insufficient to stimulate the BAT in the perihepatic region. The maximum dose of β3-AR agonists in daily practice is 50 mg/day. Clinically, BAT uptake is usually low, so that ¹⁸F-FDG uptake in the spleen and liver regions may not pose a problem.

There were some limitations in this study. First, a total of only 29 patients were included in the study, which is a small number. The reason for the small number of cases is that the presence of FDG uptake in BAT is generally considered undesirable in ¹⁸F-FDG PET/CT studies, and care is always taken to avoid cold stimulation. Second, because the present study was based on a retrospective review of cases that showed FDG uptake in the BAT, not all patients taking the β3-AR agonists may have been extracted. There could have been patients who were under β3-AR agonist treatment at the time of the ¹⁸F-FDG PET/CT examination who did not show BAT uptake.

In patients over 50 years of age who show 18F-FDG uptake in BAT, increased 18F-FDG uptake due to the influence of β3-AR agonists should be considered. Presence or absence of perirenal BAT uptake could serve as a clue to the possibility of the FDG uptake by BAT as being attributable to β3-AR agonist treatment.

Ethics declarations

Ethics approval and consent to participate:

The study protocol was approved by the Ethics Committee of National Cancer Center Hospital (Research proposal number 2018-049).

Consent for publication: Not applicable.

Competing interests: The authors certify that they have no competing interests to declare.

Funding: None declared.

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Table 1. Patient characteristics
	N = 29
Age in yr (range)	67.6 (51-87)
Male/female ratio	10/19
Height (cm)	158.8 ± 9.2
Body weight (kg)	51.4 ± 9.2
BMI (kg/m²)	20.3 ± 2.90
Outside temperature prior to the PET scanning (°C)	16.5 ± 8.4
Malignancy (n)
lung cancer	8
malignant lymphoma	5
rectal cancer	2
myelodysplasia	1
anaplastic oligodendroglioma	1
Merkel cell carcinoma	1
nasopharyngeal cancer	1
tongue cancer	1
osteosarcoma	1
malignant mesothelioma	1
esophageal cancer	1
breast cancer	1
pancreatic cancer	1
uterine cervical cancer	1
fallopian tube cancer	1
adult T-cell leukemia	1
myxofibrosarcoma	1

Table 2. Comparison of FDG uptake between patients under and not under treatment with β3-AR agonists at the time of the PET examination
	Number of patients assessed by visual assessment as showing FDG uptake in BAT			SUVmax in BAT (mean ± SD)
BAT location	β3-AR(+) group (N = 7)	β3-AR(-) group (N = 22)	p	β3-AR(+) group (N = 7)	β3-AR(-) group (N = 22)	p
Cervical	4	9	0.667	5.37 ± 6.26	3.96 ± 4.84	0.533
Periclavicular	3	11	1.000	2.76 ± 3.46	2.94 ± 3.09	0.784
Axillary	1	0	0.241	1.54 ± 1.82	0.72 ± 0.24	0.217
Mediastinal	5	8	0.192	6.3 ± 4.91	3.18 ± 2.34	0.070
Para-abdominal aortic	2	0	0.052	3.21 ± 2.86	1.44 ± 0.24	0.135
Paraspinal	7	16	0.289	10.53 ± 4.5	6.35 ± 4.91	0.199
Perirenal	6	0	0.001	7.93 ± 5.68	1.3 ± 0.3	0.001
Perisplenic	0	0		1.21 ± 0.45	0.96 ± 0.26	0.304
β3-AR: β3-adrenergic receptor; BAT: brown adipose tissue; SD: standard deviation

Table 3. Characteristics of the patients who were under treatment with β3-AR agonists at the time of the PET examination
No	Sex	age (yr)	BMI (kg/m²)	outside temperature (℃)	disease	medication	dose (mg/day)	FDG uptake (visual assessment / SUVmax)
No	Sex	age (yr)	BMI (kg/m²)	outside temperature (℃)	disease	medication	dose (mg/day)	cervical		periclavicular		axillary		mediastinal		para-abdominal aorta		paraspinal		perirenal		perisplenic
1	F	55	20.4	22.7	pancreatic ca.	mirabegron	50	－	1.1	○	1.5	－	0.7	○	2.8	－	1.6	○	6.1	○	6.2	－	1.1
2	F	87	18.2	25.0	breast ca.	vibegron	50	○	3.2	－	0.6	－	0.9	－	1.8	－	1.5	○	7.2	－	1.9	－	1.1
3	F	63	13.8	18.1	lung ca.	mirabegron	50	○	18.1	○	9.8	○	5.6	○	12.5	○	7.3	○	12.3	○	4.0	－	1.3
4	M	83	21.4	9.5	ML	mirabegron	25	○	4.1	－	0.8	－	0.5	○	13.6	－	1.7	○	6.5	○	17.4	－	1.2
5	M	81	28.2	27.9	MFS	vibegron	50	○	8.9	－	1.0	－	0.5	○	6.0	○	7.5	○	12.6	○	14.1	－	1.6
6	F	78	24.3	20.7	MCC	vibegron	50	－	0.8	－	0.6	－	1.1	－	1.8	－	1.2	○	10.3	○	5.1	－	0.5
7	F	60	20.3	29.5	lung ca.	vibegron	50	－	1.5	○	5.0	－	1.5	○	5.7	－	1.6	○	18.7	○	6.9	－	0.8
ML: malignant lymphoma; MFS: myxofibrosarcoma; MCC: Merkel cell carcinoma; ○: visual assessment indicates the presence of FDG uptake

Incidence and characteristics of 18F-FDG uptake in brown adipose tissue induced by β3-adrenergic receptor agonist treatment in 18F-FDG PET/CT images in elderly patients over 50 years of age

Status:

Version 1

Abstract

Objective

Methods

Results

Conclusion

Figures

Introduction

Materials and Methods

Assessments by visual analysis and determination of the SUVmax

Statistical analysis

Results

Discussion

Conclusion

Declarations

References

Tables

Status:

Version 1