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Metabolomics profiling of visceral and abdominal subcutaneous adipose tissue in colorectal cancer patients: results from the ColoCare study

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Abstract

Purpose

Underlying mechanisms of the relationship between body fatness and colorectal cancer remain unclear. This study investigated associations of circulating metabolites with visceral (VFA), abdominal subcutaneous (SFA), and total fat area (TFA) in colorectal cancer patients.

Methods

Pre-surgery plasma samples from 212 patients (stage I–IV) from the ColoCare Study were used to perform targeted metabolomics. VFA, SFA, and TFA were quantified by computed tomography scans. Partial correlation and linear regression analyses of VFA, SFA, and TFA with metabolites were computed and corrected for multiple testing. Cox proportional hazards were used to assess 2-year survival.

Results

In patients with metastatic tumors, SFA and TFA were statistically significantly inversely associated with 16 glycerophospholipids (SFA: pFDR range 0.017–0.049; TFA: pFDR range 0.029–0.048), while VFA was not. Doubling of ten of the aforementioned glycerophospholipids was associated with increased risk of death in patients with metastatic tumors, but not in patients with non-metastatic tumors (phet range: 0.00044–0.049). Doubling of PC ae C34:0 was associated with ninefold increased risk of death in metastatic tumors (Hazard Ratio [HR], 9.05; 95% confidence interval [CI] 2.17–37.80); an inverse association was observed in non-metastatic tumors (HR 0.17; 95% CI 0.04–0.87; phet = 0.00044).

Conclusion

These data provide initial evidence that glycerophospholipids in metastatic colorectal cancer are uniquely associated with subcutaneous adiposity, and may impact overall survival.

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Abbreviations

BMI:

Body Mass Index

CALS:

Concentration levels of standard mixes for amino acids and biogenic amines calibration

CI:

Confidence interval

CRC:

Colorectal cancer

CT:

Computed tomography

CV:

Coefficient of variation

DXA:

Dual-energy x-ray absorptiometry

FDR:

False discovery rate

FIA:

Flow injection analysis

HR:

Hazard ratio

HU:

Hounsfield units

IARC:

International Agency for Research on Cancer

LC:

Liquid chromatography

LLOQ:

Lower limit of quantification

LOD:

Limit of detection

MS:

Mass spectrometry

NSAID:

Non-steroidal anti-inflammatory drugs

OS:

Overall survival

PBS:

Phosphate buffer saline

QC:

Quality control

SAT:

Subcutaneous adipose tissue

SFA:

Subcutaneous fat area

SATI:

Subcutaneous adiposity index

TAT:

Total adipose tissue

TFA:

Total fat area

UHPLC:

Ultrahigh-performance liquid chromatography

ULOQ:

Upper limit of quantification

VAT:

Visceral adipose tissue

VEGF:

Vascular endothelial growth factor VFA: Visceral fat area

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Acknowledgments

The authors would like to acknowledge the contribution of all ColoCare participants. ColoCare samples were stored by the liquid biobank of the National Center for Tumor Diseases according to the SOPs of the Biomaterialbank Heidelberg. Lin Zielske, Anett Brendel, Renate Skatula, and Marita Wenzel supported biobanking at the National Center for Tumor Diseases. In addition, we would like to thank Rifraz Farook and Werner Diehl for their data management support and the ColoCare team, specifically Torsten Kölsch, Clare Abbenhardt-Martin, Susanne Jakob, and Judith Kammer for patient recruitment and follow-up.

Funding

Researchers involved in this work were funded by the ERA-NET, TRANSCAN project 01KT1503, the National Cancer Institute project R01 CA189184, R01 CA207371, U01 CA206110, and P30 CA042014, the Huntsman Cancer Foundation, as well as the National Institutes of Health under Ruth L. Kirschstein National Research Service Award T32 HG008962 from the National Human Genome Research Institute. This study was further supported by the Austrian Science Fund (FWF, Austria; project no. 1578-B19), the Federal Ministry of Education and Research (BMBF, Germany; project no. 01KT1512), the National Cancer Institute (INCa, France; project no. 2014-007), The Research Council of Norway (RCN, Norway; project no. 236564/H10), the Dutch Cancer Society (KWF Kankerbestrijding), and the Netherlands Organization for Health Research and Development (ZonMw, the Netherlands; project no. UW2013-6397) coordinated by the ERA-NET, JTC 2012 call on Translational Cancer Research (TRANSCAN).

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Authors and Affiliations

  1. Huntsman Cancer Institute, Salt Lake City, UT, USA

    Jennifer Ose, Andreana N. Holowatyj, Tengda Lin, Caroline Himbert, Jürgen Böhm & Cornelia M. Ulrich

  2. Department of Population Health Sciences, University of Utah, Salt Lake City, UT, USA

    Jennifer Ose, Andreana N. Holowatyj, Caroline Himbert & Cornelia M. Ulrich

  3. Diagnostic and Interventional Radiology, University Hospital of Heidelberg, Heidelberg, Germany

    Johanna Nattenmüller & Hans-Ulrich Kauczor

  4. Department of General, Visceral and Transplantation Surgery, University Hospital of Heidelberg, Heidelberg, Germany

    Biljana Gigic, Martin Schneider & Alexis Ulrich

  5. Genome Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany

    Nina Habermann

  6. International Agency Research on Cancer (IARC), Lyon, France

    David Achaintre, Augustin Scalbert & Pekka Keski-Rahkonen

  7. Division of Preventive Oncology, German Cancer Research Center (DKFZ), National Center for Tumor Diseases (NCT), Heidelberg, Germany

    Petra Schrotz-King

  8. Division of Human Nutrition, Wageningen University, Wageningen, The Netherlands

    Ellen Kampman

  9. Department of Epidemiology, GROW – School of Oncology and Developmental Biology, Maastricht University, Maastricht, The Netherlands

    Matty Weijenberg

  10. Institute of Cancer Research, Department of Medicine I, Medical University of Vienna, Vienna, Austria

    Andrea Gsur

  11. BEVITAL, Bergen, Norway

    Per-Magne Ueland

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  1. Jennifer Ose
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Correspondence to Jennifer Ose or Cornelia M. Ulrich.

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C.M.U. has served as cancer center director oversight over research funded by several pharmaceutical companies, but has not received funding directly herself. The remaining authors declare no conflict of interest.

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Ose, J., Holowatyj, A.N., Nattenmüller, J. et al. Metabolomics profiling of visceral and abdominal subcutaneous adipose tissue in colorectal cancer patients: results from the ColoCare study. Cancer Causes Control 31, 723–735 (2020). https://doi.org/10.1007/s10552-020-01312-1

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