Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Clinical Research

Sex-specific association of visceral and subcutaneous adipose tissue volumes with systemic inflammation and innate immune cells in people living with obesity

International Journal of Obesity volume 48, pages 523–532 (2024)Cite this article

Subjects

Abstract

Background and aims

Obesity predisposes to metabolic and cardiovascular diseases. Adipose tissue inflammation and systemic inflammation contribute to these complications. There are strong sex differences in adipose tissue distribution and in systemic inflammation. Women have more subcutaneous adipose tissue (SAT) and less visceral adipose tissue (VAT) than men. We explored the sex differences in the association between the different adipose compartments and inflammatory markers that are important in cardiometabolic disease pathophysiology.

Methods

Single-center observational cohort study with 302 individuals with a BMI ≥ 27 kg/m2. We were unable to acquire MRI data from seven individuals and from another 18 the MRI data were not usable, resulting in 277 people (155 men, 122 women), aged 55–81 years.

Intervention

We performed the following measurements: abdominal magnetic resonance imaging to measure VAT, and SAT (deep and superficial) volumes; circulating leukocyte counts and cytokine production capacity of peripheral blood mononuclear cells (PBMCs), circulating cytokines, adipokines, and targeted proteomics; abdominal sSAT biopsies for histology and gene expression.

Results

Only in women, (s)SAT volume was associated with circulating leukocytes, monocytes, and neutrophils. Circulating IL-6 and IL-18BP were associated with SAT volume in women and VAT in men. Several circulating proteins, including monocyte-colony-stimulating factor 1 and hepatocyte growth factor, are associated with sSAT in women and VAT in men. Only in women, SAT volume is associated with SAT expression of inflammatory proteins, including leptin, CD68, TNFα and IL-1α.

Conclusion

In women living with obesity, abdominal SAT volume, especially sSAT, is associated with circulating leukocytes and inflammatory proteins. In men, these parameters mainly show associations with VAT volume. This could be because only in women, sSAT volume is associated with sSAT expression of inflammatory proteins. These findings underscore that future research on adipose tissue in relation to cardiometabolic and cardiovascular disease should take sex differences into account.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

Data availability

The dataset used and/or analyzed during the current study is available from the corresponding author upon reasonable request.

References

  1. Neeland IJ, Ayers CR, Rohatgi AK, Turer AT, Berry JD, Das SR, et al. Associations of visceral and abdominal subcutaneous adipose tissue with markers of cardiac and metabolic risk in obese adults. Obesity. 2013;21:E439–47.

    Article  CAS  PubMed  Google Scholar 

  2. Cancello R, Zulian A, Gentilini D, Maestrini S, Della Barba A, Invitti C, et al. Molecular and morphologic characterization of superficial- and deep-subcutaneous adipose tissue subdivisions in human obesity. Obesity. 2013;21:2562–70.

    Article  CAS  PubMed  Google Scholar 

  3. Brand T, Van Den Munckhof ICL, Van Der Graaf M, Schraa K, Dekker HM, Joosten LAB, et al. Superficial vs deep subcutaneous adipose tissue: sex-specific associations with hepatic steatosis and metabolic traits. J Clin Endocrinol Metab. 2021;106:e3881–9.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cossins BC, van den Munckhof I, Rutten JHW, van der Graaf M, Stienstra R, Joosten LAB, et al. Sex-specific association between adipose tissue inflammation and vascular and metabolic complications of obesity. J Clin Endocrinol Metab. 2023;108:2537–49.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bahrar H, Bekkering S, Stienstra R, Netea MG, Riksen NP. Innate immune memory in cardiometabolic disease. Cardiovasc Res. 2023; cvad030, https://doi.org/10.1093/cvr/cvad030.

  6. Rohm TV, Meier DT, Olefsky JM, Donath MY. Inflammation in obesity, diabetes, and related disorders. Immunity. 2022;55:31–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ter Horst R, van den Munckhof ICL, Schraa K, Aguirre-Gamboa R, Jaeger M, Smeekens SP, et al. Sex-specific regulation of inflammation and metabolic syndrome in obesity. Arterioscler Thromb Vasc Biol. 2020;40:1787–1800.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Pou KM, Massaro JM, Hoffmann U, Vasan RS, Maurovich-Horvat P, Larson MG, et al. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation. 2007;116:1234–41.

    Article  CAS  PubMed  Google Scholar 

  9. Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007;56:1010–3.

    Article  CAS  PubMed  Google Scholar 

  10. Lee JJ, Pedley A, Hoffmann U, Massaro JM, Keaney JF, Vasan RS, et al. Cross‐sectional associations of computed tomography (CT)‐derived adipose tissue density and adipokines: the Framingham Heart Study. J Am Heart Assoc. 2016;5:e002545.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Koster A, Stenholm S, Alley DE, Kim LJ, Simonsick EM, Kanaya AM, et al. Body fat distribution and inflammation among obese older adults with and without metabolic syndrome. Obesity. 2010;18:2354–61.

    Article  CAS  PubMed  Google Scholar 

  12. Kim S-H, Chung J-H, Song S-W, Jung WS, Lee Y-A, Kim H-N. Relationship between deep subcutaneous abdominal adipose tissue and metabolic syndrome: a case control study. Diabetol Metab Syndr. 2016;8:10

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kurilshikov A, van den Munckhof ICL, Chen L, Bonder MJ, Schraa K, Rutten JHW, et al. Gut microbial associations to plasma metabolites linked to cardiovascular phenotypes and risk. Circ Res. 2019;124:1808–20.

    Article  CAS  PubMed  Google Scholar 

  14. Positano V, Gastaldelli A, Sironi AM, Santarelli MF, Lombardi M, Landini L. An accurate and robust method for unsupervised assessment of abdominal fat by MRI. J Magn Reson Imaging 2004;20:684–9.

    Article  PubMed  Google Scholar 

  15. Positano V, Cusi K, Santarelli MF, Sironi A, Petz R, Defronzo R, et al. Automatic correction of intensity inhomogeneities improves unsupervised assessment of abdominal fat by MRI. J Magn Reson Imaging. 2008;28:403–10.

    Article  PubMed  Google Scholar 

  16. Oosting M, Buffen K, Cheng SC, Verschueren IC, Koentgen F, van de Veerdonk FL, et al. Borrelia-induced cytokine production is mediated by spleen tyrosine kinase (Syk) but is Dectin-1 and Dectin-2 independent. Cytokine. 2015;76:465–472.

    Article  CAS  PubMed  Google Scholar 

  17. Koeken V, de Bree LCJ, Mourits VP, Moorlag SJ, Walk J, Cirovic B, et al. BCG vaccination in humans inhibits systemic inflammation in a sex-dependent manner. J Clin Invest. 2020;130:5591–5602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Assarsson E, Lundberg M, Holmquist G, Bjorkesten J, Thorsen SB, Ekman D, et al. Homogenous 96-plex PEA immunoassay exhibiting high sensitivity, specificity, and excellent scalability. PLoS ONE. 2014;9:e95192.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Stienstra R, Duval C, Keshtkar S, van der Laak J, Kersten S, Muller M. Peroxisome proliferator-activated receptor gamma activation promotes infiltration of alternatively activated macrophages into adipose tissue. J Biol Chem. 2008;283:22620–7.

    Article  CAS  PubMed  Google Scholar 

  20. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, et al. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res. 2005;46:2347–55.

    Article  CAS  PubMed  Google Scholar 

  21. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Methodol. 1995;57:289–300.

    Google Scholar 

  22. Swirski FK, Nahrendorf M. Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science. 2013;339:161–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Netea MG, Joosten LA, Lewis E, Jensen DR, Voshol PJ, Kullberg BJ, et al. Deficiency of interleukin-18 in mice leads to hyperphagia, obesity and insulin resistance. Nat Med. 2006;12:650–6.

    Article  CAS  PubMed  Google Scholar 

  24. Bekkering S, van den Munckhof I, Nielen T, Lamfers E, Dinarello C, Rutten J, et al. Innate immune cell activation and epigenetic remodeling in symptomatic and asymptomatic atherosclerosis in humans in vivo. Atherosclerosis. 2016;254:228–36.

    Article  CAS  PubMed  Google Scholar 

  25. Shirai T, Nazarewicz RR, Wallis BB, Yanes RE, Watanabe R, Hilhorst M, et al. The glycolytic enzyme PKM2 bridges metabolic and inflammatory dysfunction in coronary artery disease. J Exp Med. 2016;213:337–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lakoski SG, Cushman M, Criqui M, Rundek T, Blumenthal RS, D’Agostino RB Jr, et al. Gender and C-reactive protein: data from the Multiethnic Study of Atherosclerosis (MESA) cohort. Am Heart J. 2006;152:593–8.

    Article  CAS  PubMed  Google Scholar 

  27. Lee Y, Shin H, Vassy JL, Kim JT, Cho SI, Kang SM, et al. Comparison of regional body composition and its relation with cardiometabolic risk between BMI-matched young and old subjects. Atherosclerosis. 2012;224:258–65.

    Article  CAS  PubMed  Google Scholar 

  28. Saito T, Murata M, Otani T, Tamemoto H, Kawakami M, Ishikawa SE. Association of subcutaneous and visceral fat mass with serum concentrations of adipokines in subjects with type 2 diabetes mellitus. Endocr J. 2012;59:39–45.

    Article  CAS  PubMed  Google Scholar 

  29. Sam S, Haffner S, Davidson MH, D’Agostino RB Sr, Feinstein S, Kondos G, et al. Relation of abdominal fat depots to systemic markers of inflammation in type 2 diabetes. Diabetes Care. 2009;32:932–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Grundy SM, Adams-Huet B, Vega GL. Variable contributions of fat content and distribution to metabolic syndrome risk factors. Metab Syndr Relat Disord. 2008;6:281–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Monzon JR, Basile R, Heneghan S, Udupi V, Green A. Lipolysis in adipocytes isolated from deep and superficial subcutaneous adipose tissue. Obes Res. 2002;10:266–9.

    Article  PubMed  Google Scholar 

  32. Sniderman AD, Bhopal R, Prabhakaran D, Sarrafzadegan N, Tchernof A. Why might South Asians be so susceptible to central obesity and its atherogenic consequences? The adipose tissue overflow hypothesis. Int J Epidemiol. 2007;36:220–5.

    Article  PubMed  Google Scholar 

  33. Marinou K, Hodson L, Vasan SK, Fielding BA, Banerjee R, Brismar K, et al. Structural and functional properties of deep abdominal subcutaneous adipose tissue explain its association with insulin resistance and cardiovascular risk in men. Diabetes Care. 2014;37:821–9.

    Article  PubMed  Google Scholar 

  34. Rana MN, Neeland IJ. Adipose tissue inflammation and cardiovascular disease: an update. Curr Diab Rep. 2022;22:27–37.

    Article  CAS  PubMed  Google Scholar 

  35. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116:39–48.

    Article  PubMed  Google Scholar 

  36. Snijder MB, Visser M, Dekker JM, Goodpaster BH, Harris TB, Kritchevsky SB, et al. Low subcutaneous thigh fat is a risk factor for unfavourable glucose and lipid levels, independently of high abdominal fat. The Health ABC Study. Diabetologia. 2005;48:301–8.

    Article  CAS  PubMed  Google Scholar 

  37. Agrawal S, Klarqvist MDR, Diamant N, Stanley TL, Ellinor PT, Mehta NN, et al. BMI-adjusted adipose tissue volumes exhibit depot-specific and divergent associations with cardiometabolic diseases. Nat Commun. 2023;14:266.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Alser M, Elrayess MA. From an apple to a pear: moving fat around for reversing insulin resistance. Int J Environ Res Public Health. 2022;19:14251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Golan R, Shelef I, Rudich A, Gepner Y, Shemesh E, Chassidim Y, et al. Abdominal superficial subcutaneous fat: a putative distinct protective fat subdepot in type 2 diabetes. Diabetes Care. 2012;35:640–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Beasley LE, Koster A, Newman AB, Javaid MK, Ferrucci L, Kritchevsky SB, et al. Inflammation and race and gender differences in computerized tomography-measured adipose depots. Obesity. 2009;17:1062–9.

    Article  PubMed  Google Scholar 

  41. Cartier A, Côté M, Lemieux I, Pérusse L, Tremblay A, Bouchard C, et al. Sex differences in inflammatory markers: what is the contribution of visceral adiposity? Am J Clin Nutr. 2009;89:1307–14.

    Article  CAS  PubMed  Google Scholar 

  42. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med. 2009;15:930–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vasanthakumar A, Chisanga D, Blume J, Gloury R, Britt K, Henstridge DC, et al. Sex-specific adipose tissue imprinting of regulatory T cells. Nature. 2020;579:581–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Ryder E, Diez-Ewald M, Mosquera J, Fernández E, Pedreañez A, Vargas R, et al. Association of obesity with leukocyte count in obese individuals without metabolic syndrome. Diabetes Metab Syndr. 2014;8:197–204.

    Article  PubMed  Google Scholar 

  45. Yoshimura A, Ohnishi S, Orito C, Kawahara Y, Takasaki H, Takeda H, et al. Association of peripheral total and differential leukocyte counts with obesity-related complications in young adults. Obes Facts. 2015;8:1–16.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Nagareddy PR, Kraakman M, Masters SL, Stirzaker RA, Gorman DJ, Grant RW, et al. Adipose tissue macrophages promote myelopoiesis and monocytosis in obesity. Cell Metab. 2014;19:821–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hino M, Inaba M, Goto H, Nishizawa Y, Tatsumi N, Nishino T, et al. Hepatocyte growth factor levels in bone marrow plasma of patients with leukaemia and its gene expression in leukaemic blast cells. Br J Cancer. 1996;73:119–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Bell LN, Ward JL, Degawa-Yamauchi M, Bovenkerk JE, Jones R, Cacucci BM, et al. Adipose tissue production of hepatocyte growth factor contributes to elevated serum HGF in obesity. Am J Physiol Endocrinol Metab. 2006;291:E843–8.

    Article  CAS  PubMed  Google Scholar 

  49. Osibogun O, Ogunmoroti O, Ferraro RA, Ndumele CE, Burke GL, Larson NB, et al. Favorable cardiovascular health is associated with lower hepatocyte growth factor levels in the multi-ethnic study of atherosclerosis. Front Cardiovasc Med. 2021;8:760281.

    Article  PubMed  Google Scholar 

  50. Levine JA, Jensen MD, Eberhardt NL, O’Brien T. Adipocyte macrophage colony-stimulating factor is a mediator of adipose tissue growth. J Clin Invest. 1998;101:1557–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, et al. Tissue-based map of the human proteome. Science. 2015. https://www.proteinatlas.org/ENSG00000173391-OLR1/single+cell+type.

  52. Rasouli N, Yao-Borengasser A, Varma V, Spencer HJ, McGehee RE, Peterson CA, et al. Association of scavenger receptors in adipose tissue with insulin resistance in nondiabetic humans. Arterioscler Thromb Vasc Biol. 2009;29:1328–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Brinkley TE, Kume N, Mitsuoka H, Phares DA, Hagberg JM. Elevated soluble lectin-like oxidized LDL receptor-1 (sLOX-1) levels in obese postmenopausal women. Obesity. 2008;16:1454–6.

    Article  CAS  PubMed  Google Scholar 

  54. Stinson SE, Jonsson AE, Andersen MK, Lund MAV, Holm LA, Fonvig CE, et al. High plasma levels of soluble lectin‐like oxidized low‐density lipoprotein receptor‐1 are associated with inflammation and cardiometabolic risk profiles in pediatric overweight and obesity. J Am Heart Assoc. 2023;12:e8145.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Kataoka H, Kume N, Miyamoto S, Minami M, Moriwaki H, Murase T, et al. Expression of lectinlike oxidized low-density lipoprotein receptor-1 in human atherosclerotic lesions. Circulation. 1999;99:3110–7.

    Article  CAS  PubMed  Google Scholar 

  56. Markstad H, Edsfeldt A, Yao Mattison I, Bengtsson E, Singh P, Cavalera M, et al. High levels of soluble lectin like oxidized low‐density lipoprotein receptor‐1 are associated with carotid plaque inflammation and increased risk of ischemic stroke. J Am Heart Assoc. 2019;8:e009874.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Hofmann A, Brunssen C, Wolk S, Reeps C, Morawietz H. Soluble LOX‐1: a novel biomarker in patients with coronary artery disease, stroke, and acute aortic dissection? J Am Heart Assoc. 2020;9:e013803.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Kraler S, Wenzl FA, Georgiopoulos G, Obeid S, Liberale L, von Eckardstein A, et al. Soluble lectin-like oxidized low-density lipoprotein receptor-1 predicts premature death in acute coronary syndromes. Eur Heart J. 2022;43:1849–60.

    Article  CAS  PubMed  Google Scholar 

  59. Dregoesc MI, Ţigu AB, Bekkering S, van der Heijden C, Bolboacǎ SD, Joosten LAB, et al. Relation between plasma proteomics analysis and major adverse cardiovascular events in patients with stable coronary artery disease. Front Cardiovasc Med. 2022;9:731325.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Karason K, Girerd N, Andersson-Asssarsson J, Duarte K, Taube M, Svensson P-A, et al. Heart failure in obesity: insights from proteomics in patients treated with or without weight-loss surgery. Int J Obes. 2022;46:2088–94.

    Article  CAS  Google Scholar 

  61. Koliaki C, Katsilambros N. Repositioning the role of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) on the TRAIL to the development of diabetes mellitus: an update of experimental and clinical evidence. Int J Mol Sci. 2022;23:3225.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all of the volunteers in the 300-OB cohort for their participation. LABJ, MGN, NPR and JHWR received a CVON grant from the Dutch Heart Foundation/Dutch Cardiovascular Alliance (IN CONTROL II: CVON2018-27). MGN is further supported by a European Research Council (ERC) Advanced Grant (FP/2007-2013/ERC grant 2012-322698), and a Spinoza Prize (NWO SPI 92-266). RS was supported by a VIDI-grant from the Dutch Research Council and a senior fellowship of the Dutch Diabetes Foundation. NPR was recipient of a grant of the ERA-CVD Joint Transnational Call 2018 supported by the Dutch Heart Foundation (JTC2018, project MEMORY; 2018T093).

Author information

Author notes

  1. These authors contributed equally: Inge C. L. van den Munckhof, Harsh Bahrar.

Authors and Affiliations

  1. Department of Internal Medicine, Radboud University Medical Center, Nijmegen, The Netherlands

    Inge C. L. van den Munckhof, Harsh Bahrar, Kiki Schraa, Tessa Brand, Rob ter Horst, Rinke Stienstra, Jacqueline de Graaf, Leo A. B. Joosten, Mihai G. Netea, Niels P. Riksen & Joost H. W. Rutten

  2. CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria

    Rob ter Horst

  3. Department of Medical Imaging, Radboud University Medical Center, Nijmegen, The Netherlands

    Marinette van der Graaf & Helena M. Dekker

  4. Division of Human Nutrition and Health, Wageningen University, Wageningen, The Netherlands

    Rinke Stienstra

  5. Department of Medical Genetics, Iuliu Haţieganu University of Medicine and Pharmacy, Cluj-Napoca, Romania

    Leo A. B. Joosten

  6. Department for Immunology and Metabolism, Life and Medical Sciences Institute (LIMES), University of Bonn, 53115, Bonn, Germany

    Mihai G. Netea

Authors
  1. Inge C. L. van den Munckhof
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harsh Bahrar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kiki Schraa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tessa Brand
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rob ter Horst
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marinette van der Graaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Helena M. Dekker
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rinke Stienstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jacqueline de Graaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Leo A. B. Joosten
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mihai G. Netea
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Niels P. Riksen
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Joost H. W. Rutten
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ICLM and HB: drafting of the manuscript, data acquisition, analysis, equal contribution. KS and TB: data acquisition. RH, MvdG, and HMD: data acquisition and analysis. RS, JG, LABJ, MGN, NPR, and JHWR: study design and funding, supervision of data acquisition and analyses. All co-authors contributed to writing of the manuscript. All authors provided critical revisions for important intellectual content, approved the final version submitted for publication, and agreed to be accountable for all aspects of the work.

Corresponding author

Correspondence to Joost H. W. Rutten.

Ethics declarations

Competing interests

LABJ and MGN declare that they are scientific founders of Trained Therapeutics Discovery (TTxD) and LEMBA therapeutics. All other authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

van den Munckhof, I.C.L., Bahrar, H., Schraa, K. et al. Sex-specific association of visceral and subcutaneous adipose tissue volumes with systemic inflammation and innate immune cells in people living with obesity. Int J Obes 48, 523–532 (2024). https://doi.org/10.1038/s41366-023-01444-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41366-023-01444-9

This article is cited by

Search

Advanced search

Quick links