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Clinical Research

Metabolic interactions between organs in overweight and obesity using total-body positron emission tomography

Subjects

Abstract

Background and Objectives

Overweight and obesity is a complex condition resulting from unbalanced energy homeostasis among various organs. However, systemic abnormalities in overweight and obese people are seldom explored in vivo by metabolic imaging techniques. The aim of this study was to determine metabolic abnormities throughout the body in overweight and obese adults using total-body positron emission tomography (PET) glucose uptake imaging.

Methods

Thirty normal weight subjects [body mass index (BMI) < 25 kg/m2, 55.47 ± 13.94 years, 16 men and 14 women], and 26 overweight and obese subjects [BMI ≥ 25 kg/m2, 52.38 ± 9.52 years, 21 men and 5 women] received whole-body 18F-fluorodeoxyglucose PET imaging using the uEXPLORER. Whole-body standardized uptake value normalized by lean body mass (SUL) images were calculated. Metabolic networks were constructed based on the whole-body SUL images using covariance network approach. Both group-level and individual-level network differences between normal weight and overweight/obese subjects were evaluated. Correlation analysis was conducted between network properties and BMI for the overweight/obese subjects.

Results

Compared with normal weight subjects, overweight/obese subjects exhibited altered network connectivity strength in four network nodes, namely the pancreas (p = 0.033), spleen (p = 0.021), visceral adipose tissue (VAT) (p = 1.12 × 10−5) and bone (p = 0.021). Network deviations of overweight/obese subjects from the normal weight were positively correlated with BMI (r = 0.718, p = 3.64 × 10−5). In addition, overweight/obese subjects experienced altered connections between organs, and some of the altered connections, including pancreas-right lung and VAT-bilateral lung connections were significantly correlated with BMI.

Conclusion

Overweight/obese individuals exhibit metabolic alterations in organ level, and altered metabolic interactions at the systemic level. The proposed approach using total-body PET imaging can reveal individual metabolic variability and metabolic deviations between organs, which would open up a new path for understanding metabolic alterations in overweight and obesity.

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Fig. 1: Visualization of the 22 ROIs.
Fig. 2: Flow chart of network construction using SUL values from the 22 ROIs.
Fig. 3: Scatter plot between BMI and contribution of each overweight subjects to the network deviation.
Fig. 4: Connectivity maps for normal weight and overweight groups.
Fig. 5: Comparisons of NCS and SUL values between the two groups.
Fig. 6: Differences in edges between the two groups.
Fig. 7: Associations between edges and BMI in the overweight group.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Funding

This work was supported by the Science and Technology Funding from Jinan (grant number: 2020GXRC018), Academic Promotion Program of Shandong First Medical University (grant number: 2019QL009), Natural Science Foundation of Shandong Province (Grant number: ZR2023QH109), and Taishan Scholars Program of Shandong Province (grant number: TS201712065).

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Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection were performed by YD, KL and ZC data processing and analysis were performed by WL and JQ The first draft of the manuscript was written by WL. All authors commented on previous versions of the manuscript and all authors read and approved the final manuscript.

Corresponding authors

Correspondence to Zhaoping Cheng or Jianfeng Qiu.

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Competing interests

The authors have no conflicts of interest to declare that are relevant to the content of this article. All authors commented on previous versions of the manuscript and all authors read and approved the final manuscript.

Ethics approval

This study received approval from the Institutional Review Board of Shandong First Medical University in accordance with the Declaration of Helsinki.

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Prior to PET/CT scan, all subjects gave their written informed consent.

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All authors commented on previous versions of the manuscript and all authors read and approved the final manuscript.

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Lu, W., Duan, Y., Li, K. et al. Metabolic interactions between organs in overweight and obesity using total-body positron emission tomography. Int J Obes 48, 94–102 (2024). https://doi.org/10.1038/s41366-023-01394-2

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