Lipid and cellular profiles of acetabular and femoral bone marrow adipose tissues are distinct in hip osteoarthritis patients

Abstract

Bone marrow (BM) adipose tissue (BMAT) has been described as lipotoxic factor with negative impacts on skeletal system regeneration and repair. As BMAT undergoes metabolic and cellular adaptations with age and disease, we assumed that investigation of BMAT-associated lipid profile and cellularity at different skeletal locations in osteoarthritis (OA) patients might contribute to understanding of lipid involvement in OA development and progression.Acetabular and femoral BM, and femoral subcutaneous adipose tissue (fSAT) were obtained from matched patients (n=11, 5 women, 6 men; age: 65±11 years; BMI: 27.89±4.42 kg/m2) undergoing hip arthroplasty surgery (Ethical approval I-97/11). BM, BMAT and fSAT were explored at the levels of total lipids, fatty acids, and cells, by using thin layer and gas chromatography and ex vivo cellular 24734039, 2023, S3, Downloaded from https://asbmr.onlinelibrary.wiley.com/doi/10.1002/jbm4.10738 by Readcube (Labtiva Inc.), Wiley Online Library on [23/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License assays. Statistical significance was estimated by non-parametric tests and Spearman’s rank correlation (r) was calculated.BMAT content was significantly higher in femoral (0.262±0.088 mL/g) than in acetabular BM (0.063±0.051 mL/g) (n=11, p=0.016). Negative associations with BMI of patients were found for femoral BM (r=-0.783, p=0.017, n=11) and BMAT (n=9, r=-1.000, p=0.017) tissue cellularity. Additionally, femoral BMAT cellularity declined with age (r=-0.675, n=10, p=0.037). Total lipid analyses revealed significantly lower triglyceride content in femoral than in acetabular BMAT and fSAT. Frequency of saturated palmitic, myristic and stearic acids were higher in femoral than in acetabular BMAT and fSAT, where palmitoleic, linoleic, oleic acids were more dominant. BMAT associated compartments from both locations host lower frequency of non-hematopoietic CD45- neutral lipid-loaded cells when compared to BM. This associated with higher incidence of clonogenic mesenchymal stromal (stem) cells in acetabular (0.032± 0.04%) and femoral (0.021± 0.028%) BMATs and fSAT (0.031 ± 0.016%) than in their BM counterparts. Collectively, our results indicate that the lipid profiles of hip BMAT impose significantly different BM microenvironments and distribution of cells with regenerative potential in OA patients.