The mechanical properties of human adipose tissues and their relationships to the structure and composition of the extracellular matrix

Author:

Alkhouli Nadia1,Mansfield Jessica2,Green Ellen2,Bell James23,Knight Beatrice4,Liversedge Neil5,Tham Ji Chung6,Welbourn Richard6,Shore Angela C.3,Kos Katarina1,Winlove C. Peter2

Affiliation:

1. Obesity Research Group, Institute of Biomedical and Clinical Science, University of Exeter Medical School, University of Exeter, Exeter, United Kingdom;

2. Biomedical Physics Group, Department of Physics, College of Engineering, Mathematics, and Physical Sciences, University of Exeter, Exeter, United Kingdom;

3. Department of Vascular Medicine, NIHR Exeter Clinical Research Facility and Institute of Biomedical and Clinical Science, University of Exeter Medical School, Exeter, United Kingdom

4. National Institute for Health Research (NIHR) Exeter Clinical Research Facility, Royal Devon and Exeter Hospital National Health Service (NHS) Foundation Trust, Exeter, United Kingdom;

5. Department of Obstetrics and Gynaecology, Royal Devon and Exeter Foundation NHS Trust, Exeter, United Kingdom;

6. Department of Bariatric Surgery, Musgrove Park Hospital, Taunton, United Kingdom; and

Abstract

Adipose tissue (AT) expansion in obesity is characterized by cellular growth and continuous extracellular matrix (ECM) remodeling with increased fibrillar collagen deposition. It is hypothesized that the matrix can inhibit cellular expansion and lipid storage. Therefore, it is important to fully characterize the ECM's biomechanical properties and its interactions with cells. In this study, we characterize and compare the mechanical properties of human subcutaneous and omental tissues, which have different physiological functions. AT was obtained from 44 subjects undergoing surgery. Force/extension and stress/relaxation data were obtained. The effects of osmotic challenge were measured to investigate the cellular contribution to tissue mechanics. Tissue structure and its response to tensile strain were determined using nonlinear microscopy. AT showed nonlinear stress/strain characteristics of up to a 30% strain. Comparing paired subcutaneous and omental samples ( n = 19), the moduli were lower in subcutaneous: initial 1.6 ± 0.8 (means ± SD) and 2.9 ± 1.5 kPa ( P = 0.001), final 11.7 ± 6.4 and 32 ± 15.6 kPa ( P < 0.001), respectively. The energy dissipation density was lower in subcutaneous AT ( n = 13): 0.1 ± 0.1 and 0.3 ± 0.2 kPa, respectively ( P = 0.006). Stress/relaxation followed a two-exponential time course. When the incubation medium was exchanged for deionized water in specimens held at 30% strain, force decreased by 31%, and the final modulus increased significantly. Nonlinear microscopy revealed collagen and elastin networks in close proximity to adipocytes and a larger-scale network of larger fiber bundles. There was considerable microscale heterogeneity in the response to strain in both cells and matrix fibers. These results suggest that subcutaneous AT has greater capacity for expansion and recovery from mechanical deformation than omental AT.

Publisher

American Physiological Society

Subject

Physiology (medical),Physiology,Endocrinology, Diabetes and Metabolism

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