Macrophage Infiltration into Omental Versus Subcutaneous Fat across Different Populations: Effect of Regional Adiposity and the Comorbidities of Obesity
Abstract
CONTEXT: Macrophage infiltration into adipose tissue has been demonstrated to accompany obesity, with a potential preferential infiltration into intraabdominal vs. sc fat. OBJECTIVE: Our objective was to determine whether this occurs across different populations with a range of body mass indexes and to assess the relationship with regional adiposity and comorbidity of obesity. SETTING AND PATIENTS: In two independent cohorts, we used paired omental (OM) and sc fat biopsies from lean controls or predominantly sc or intraabdominally obese persons with minimal comorbidity (n = 60, cohort 1), or from severely obese women with a significant rate of comorbidity (n = 29, cohort 2). RESULTS: Elevated macrophage infiltration into OM vs. sc fat was observable in lean subjects and exaggerated by obesity, particularly if predominantly intraabdominal. This was paralleled by increased monocyte chemoattractant protein-1 (MCP1) and colony-stimulating factor-1 (CSF1) mRNA levels. Level of CSF1 and MCP1 mRNA correlated with the number of OM macrophages (r = 0.521, P < 0.0001 and r = 0.258, P < 0.051, respectively). In severely obese women (mean body mass index = 43.0 +/- 1.1 kg/m(2)), higher protein expression of both MCP1 and CSF1 was detected in OM vs. sc fat. Number of OM macrophages, but not of sc macrophages, correlated with waist circumference (r = 0.636, P = 0.001 vs. r = 0.170, P = 0.427) and with the number of metabolic syndrome parameters (r = 0.385, P = 0.065 vs. r = -0.158, P = 0.472, respectively). Preferential macrophage infiltration into OM fat was mainly observed in a subgroup in whom obesity was associated with impaired glucose homeostasis. CONCLUSIONS: Preferential macrophage infiltration into OM fat is a general phenomenon exaggerated by central obesity, potentially linking central adiposity with increased risk of diabetes and coronary heart disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Casein-derived peptides Ile-Pro-Pro and Val-Pro-Pro slightly, though not significantly, lower CRP concentration in hypertensive subjects after 10 weeks.
“Indeed, the casein-derived peptides Ile-Pro-Pro and Val-Pro-Pro slightly, though not significantly, lowered CRP concentration in hypertensive subjects after 10 weeks (684) .”
From Dietary factors and low-grade inflammation in relation to overweight and obesity (2011) · cites this paper as [684]
Visceral adipose tissue macrophage counts are higher in insulin-resistant obese patients than in lean or insulin-sensitive obese patients.
“Several detailed studies have also reported a higher macrophage count in visceral AT of insulin-resistant obese patients compared with lean or insulin-sensitive obese counterparts, an effect that was significantly mitigated following bariatric surgery (10,(114)(115)(116).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [115]
Bariatric surgery significantly reduces the elevated visceral adipose tissue macrophage count in insulin-resistant obese patients.
“Several detailed studies have also reported a higher macrophage count in visceral AT of insulin-resistant obese patients compared with lean or insulin-sensitive obese counterparts, an effect that was significantly mitigated following bariatric surgery (10,(114)(115)(116).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [115]
Cites
Obesity is associated with macrophage accumulation in adipose tissue
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319246 · Cited by 10,041 · see citing works
Glucose clamp technique: a method for quantifying insulin secretion and resistance.
DeFronzo, R. A., Tobin, J. D., & Andres, R. (1979) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1979.237.3.e214 · Cited by 7,425 · see citing works
Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A., et al. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319451 · Cited by 6,760 · see citing works
Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome
Wajchenberg, B. L. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.6.0415 · Cited by 2,961 · see citing works
Kanda, H. (2006) · Journal of Clinical Investigation · doi:10.1172/jci26498 · Cited by 2,682 · see citing works
Cinti, S., Mitchell, G., Barbatelli, G., Murano, I., Ceresi, E., Faloia, E., Wang, S., Fortier, M., Greenberg, A. S., & Obin, M. S. (2005) · Journal of Lipid Research · doi:10.1194/jlr.m500294-jlr200 · Cited by 2,529 · see citing works
Obesity-induced inflammatory changes in adipose tissue
Wellen, K. E., & Hotamisligil, G. S. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200320514 · Cited by 1,823 · see citing works
CCR2 modulates inflammatory and metabolic effects of high-fat feeding
Weisberg, S. P., Hunter, D., Huber, R., Lemieux, J., Slaymaker, S., Vaddi, K., Charo, I., Leibel, R. L., & Jr., A. W. F. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24335 · Cited by 1,497 · see citing works
CCR2 modulates inflammatory and metabolic effects of high-fat feeding
Weisberg, S. P. (2006) · Journal of Clinical Investigation · doi:10.1172/jci24335c1 · Cited by 1,424 · see citing works
Cancello, R., Henegar, C., Viguerie, N., Taleb, S., Poitou, C., Rouault, C., Coupaye, M., Pelloux, V., Hugol, D., Bouillot, J.-L., et al. (2005) · Diabetes · doi:10.2337/diabetes.54.8.2277 · Cited by 1,164 · see citing works
Cancello, R., Tordjman, J., Poitou, C., Guilhem, G., Bouillot, J. L., Hugol, D., Coussieu, C., Basdevant, A., Hen, A. B., Bedossa, P., et al. (2006) · Diabetes · doi:10.2337/db06-0133 · Cited by 607 · see citing works
From Blood Monocytes to Adipose Tissue-Resident Macrophages
Curat, C. A., Miranville, A., Sengenès, C., Diehl, M., Tonus, C., Busse, R., & Bouloumié, A. (2004) · Diabetes · doi:10.2337/diabetes.53.5.1285 · Cited by 600 · see citing works
Gabir, M. M., Hanson, R. L., Dabelea, D., Imperatore, G., Roumain, J., Bennett, P. H., & Knowler, W. C. (2000) · Diabetes Care · doi:10.2337/diacare.23.8.1108 · Cited by 568 · see citing works
Bruun, J. M., Lihn, A. S., Pedersen, S. B., & Richelsen, B. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1696 · Cited by 535 · see citing works
Misra, A., & Vikram, N. (2003) · Nutrition (Burbank, Los Angeles County, Calif.) · doi:10.1016/s0899-9007(02)01003-1 · Cited by 329 · see citing works
Sell, H., Dietze‐Schroeder, D., Kaiser, U., & Eckel, J. (2006) · Endocrinology · doi:10.1210/en.2005-0969 · Cited by 226 · see citing works
Dahlman, I. A., Kaaman, M., Olsson, T., Tan, G. D., Bickerton, A. S. T., Wåhlén, K., Andersson, J. S. O., Nordström, E. A., Blomqvist, L., Sjögren, A., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0369 · Cited by 207 · see citing works
Adipocyte macrophage colony-stimulating factor is a mediator of adipose tissue growth.
Levine, J. A., Jensen, M. D., Eberhardt, N. L., & O’Brien, T. (1998) · Journal of Clinical Investigation · doi:10.1172/jci2293 · Cited by 143 · see citing works
Low Plasma Adiponectin Levels Are Associated With Increased Hepatic Lipase Activity In Vivo
Schneider, J. G., von Eynatten, M., Schiekofer, S., Nawroth, P. P., & Dugi, K. A. (2005) · Diabetes Care · doi:10.2337/diacare.28.9.2181 · Cited by 129 · see citing works
Serum leptin is associated with serum uric acid concentrations in humans
Fruehwald‐Schultes, B., Peters, A., Kern, W., Beyer, J., & Pfützner, A. (1999) · Metabolism · doi:10.1016/s0026-0495(99)90163-4 · Cited by 97 · see citing works
Strączkowski, M., Lewczuk, P., Dzienis-Straczkowska, S., Kowalska, I., Stecedilpienacute, A., & Kinalska, I. (2002) · Metabolism · doi:10.1053/meta.2002.28095 · Cited by 60 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Inflammatory Mechanisms in Obesity
Gregor, M. F., & Hotamisligil, G. S. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101322 · Cited by 3,754 · see citing works
Type 2 diabetes as an inflammatory disease
Donath, M. Y., & Shoelson, S. E. (2011) · Nature Reviews Immunology · doi:10.1038/nri2925 · Cited by 3,737 · see citing works
Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes.
Guilherme, A., Virbasius, J. V., Puri, V., & Czech, M. P. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2391 · Cited by 2,292 · see citing works
Adipose tissue inflammation and metabolic dysfunction in obesity
Kawai, T., Autieri, M. V., & Scalia, R. (2021) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00379.2020 · Cited by 1,947 · see citing works
Chait, A., & den Hartigh, L. J. (2020) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2020.00022 · Cited by 1,529 · see citing works
Molecular inflammation: Underpinnings of aging and age-related diseases
Chung, H. Y., Cesari, M., Anton, S., Marzetti, E., Giovannini, S., Seo, A. Y., Carter, C., Yu, B. P., & Leeuwenburgh, C. (2009) · Ageing Research Reviews · doi:10.1016/j.arr.2008.07.002 · Cited by 1,203 · see citing works
Dietary factors and low-grade inflammation in relation to overweight and obesity
Calder, P. C., Ahluwalia, N., Brouns, F., Buetler, T., Clement, K., Cunningham, K., Esposito, K., Jönsson, L. S., Kolb, H., Lansink, M., et al. (2011) · British Journal of Nutrition · doi:10.1017/s0007114511005460 · Cited by 1,098 · see citing works
Adipokine dysregulation, adipose tissue inflammation and metabolic syndrome
Maury, E., & Brichard, S. M. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.07.031 · Cited by 1,026 · see citing works
Adipocyte Death, Adipose Tissue Remodeling, and Obesity Complications
Strissel, K. J., Stancheva, Z., Miyoshi, H., Perfield, J. W., DeFuria, J., Jick, Z., Greenberg, A. S., & Obin, M. S. (2007) · Diabetes · doi:10.2337/db07-0767 · Cited by 1,007 · see citing works
Klöting, N., Fasshauer, M., Dietrich, A., Kovacs, P., Schön, M. R., Kern, M., Stumvoll, M., & Blüher, M. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00586.2009 · Cited by 856 · see citing works
Self-citationMurano, I., Barbatelli, G., Parisani, V., Latini, C., Muzzonigro, G., Castellucci, M., & Cinti, S. (2008) · Journal of Lipid Research · doi:10.1194/jlr.m800019-jlr200 · Cited by 726 · see citing works
The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis.
Crewe, C., An, Y. A., & Scherer, P. E. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88883 · Cited by 732 · see citing works
Obesity and cancer: the role of dysfunctional adipose tissue
van Kruijsdijk, R. C. M., van der Wall, E., & Visseren, F. L. J. (2009) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-09-0372 · Cited by 715 · see citing works
Transdifferentiation properties of adipocytes in the adipose organ
Cinti, S. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00183.2009 · Cited by 379 · see citing works
Adipose tissue-resident immune cells: key players in immunometabolism
Schipper, H. S., Prakken, B., Kalkhoven, E., & Boes, M. (2012) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.05.011 · Cited by 342 · see citing works
The infrapatellar fat pad of patients with osteoarthritis has an inflammatory phenotype
Klein-Wieringa, I. R., Kloppenburg, M., Bastiaansen-Jenniskens, Y. M., Yusuf, E., Kwekkeboom, J. C., El-Bannoudi, H., Nelissen, R. G. H. H., Zuurmond, A., Stojanovic-Susulic, V, Van Osch, G. J. V. M., et al. (2011) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2010.140046 · Cited by 289 · see citing works
Aging and Regional Differences in Fat Cell Progenitors – A Mini-Review
Sepe, A., Tchkonia, T., Thomou, T., Zamboni, M., & Kirkland, J. L. (2011) · Gerontology · doi:10.1159/000279755 · Cited by 232 · see citing works
The hematologic consequences of obesity
Purdy, J. C., & Shatzel, J. J. (2021) · European Journal Of Haematology · doi:10.1111/ejh.13560 · Cited by 227 · see citing works
Obesity, pregnancy, inflammation, and vascular function
Denison, F. C., Roberts, K. A., Barr, S. M., & Norman, J. E. (2010) · Reproduction · doi:10.1530/rep-10-0074 · Cited by 221 · see citing works
Altintas, M. M., Azad, A., Nayer, B., Contreras, G., Zaias, J., Faul, C., Reiser, J., & Nayer, A. (2011) · Journal of Lipid Research · doi:10.1194/jlr.m011338 · Cited by 198 · see citing works
Barrea, L., Marzullo, P., Muscogiuri, G., Di Somma, C., Scacchi, M., Orio, F., Aimaretti, G., Colao, A., & Savastano, S. (2018) · Nutrition Research Reviews · doi:10.1017/s0954422418000136 · Cited by 171 · see citing works
Chronic Stress and Diabetes Mellitus: Interwoven Pathologies
Sharma, V. K., & Singh, T. G. (2020) · Current Diabetes Reviews · doi:10.2174/1573399815666191111152248 · Cited by 116 · see citing works
Ageing, adipose tissue, fatty acids and inflammation
Pararasa, C., Bailey, C. J., & Griffiths, H. R. (2015) · Biogerontology · doi:10.1007/s10522-014-9536-x · Cited by 110 · see citing works
Physical inactivity, insulin resistance, and the oxidative-inflammatory loop
Gratas-Delamarche, A., Derbré, F., Vincent, S., & Cillard, J. (2014) · Free Radical Research · doi:10.3109/10715762.2013.847528 · Cited by 99 · see citing works
Role of the gut in visceral fat inflammation and metabolic disorders
Lam, Y. Y., Mitchell, A. J., Holmes, A. J., Denyer, G. S., Gummesson, A., Caterson, I. D., Hunt, N. H., & Storlien, L. H. (2011) · Obesity · doi:10.1038/oby.2011.68 · Cited by 97 · see citing works
Kranendonk, M. E. G., van Herwaarden, J. A., Stupkova, T., Jager, W. D., Vink, A., Moll, F. L., Kalkhoven, E., & Visseren, F. L. J. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.01.035 · Cited by 91 · see citing works
Adipose tissue in health and disease through the lens of its building blocks.
Lenz, M., Arts, I. C. W., Peeters, R. L. M., de Kok, T. M., & Ertaylan, G. (2020) · Scientific Reports · doi:10.1038/s41598-020-67177-1 · Cited by 89 · see citing works
Li, Y.-F., Chang, Y.-Y., Huang, H.-C., Wu, Y.-C., Yang, M.-D., & Chao, P.-M. (2015) · Nutrition · doi:10.1016/j.nut.2014.11.008 · Cited by 81 · see citing works
Sick fat: the good and the bad of old and new circulating markers of adipose tissue inflammation
Barchetta, I., Cimini, F. A., Ciccarelli, G., Baroni, M. G., & Cavallo, M. G. (2019) · Journal of Endocrinological Investigation · doi:10.1007/s40618-019-01052-3 · Cited by 77 · see citing works
Glintborg, D., Andersen, M., Richelsen, B., & Bruun, J. M. (2009) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2009.03523.x · Cited by 78 · see citing works
Sex-dependent depot differences in adipose tissue development and function; role of sex steroids
Lee, M.-J., & Fried, S. K. (2017) · Journal of Obesity & Metabolic Syndrome · doi:10.7570/jomes.2017.26.3.172 · Cited by 72 · see citing works
From neutrophils to macrophages: Differences in regional adipose tissue depots
Dam, V., Sikder, T., & Santosa, S. (2016) · Obesity Reviews · doi:10.1111/obr.12335 · Cited by 65 · see citing works
Inflammation and the depot-specific secretome of human preadipocytes
Zhu, Y., Tchkonia, T., Stout, M. B., Giorgadze, N., Wang, L., Li, P. W., Heppelmann, C. J., Bouloumié, A., Jensen, M. D., Bergen, H. R., et al. (2015) · Obesity · doi:10.1002/oby.21053 · Cited by 42 · see citing works
ADCY5 Gene Expression in Adipose Tissue Is Related to Obesity in Men and Mice
Knigge, A., Klöting, N., Schön, M. R., Dietrich, A., Fasshauer, M., Gärtner, D., Lohmann, T., Dreßler, M., Stumvoll, M., Kovacs, P., et al. (2015) · PLOS ONE · doi:10.1371/journal.pone.0120742 · Cited by 24 · see citing works
Self-citation
- Authors
- Harman-Boehm, I., Blüher, M., Redel, H., Sion-Vardy, N., Ovadia, S., Avinoach, E., Shai, I., Klöting, N., Stumvoll, M., Bashan, N., & Rudich, A.
- Affiliations
- Diabetes Unit and Internal Medicine C (I.H.-B.), Soroka Medical Center, Beer-Sheva 84101, Israel
- Medical Department III (M.B., N.K., M.S.), University of Leipzig, 04109 Leipzig, Germany
- Soroka Medical Center (IL)
- Pathology Institute (H.R., N.S.-V.), Soroka Medical Center, Beer-Sheva 84101, Israel
- Ben-Gurion University of the Negev (IL)
- Corresponding author
- Rudich, Assaf
- Venue
- The Journal of Clinical Endocrinology & Metabolism
- Publisher
- The Endocrine Society
- Published
- 2007-06-01
- Volume
- 92
- Issue
- 6
- Pages
- 2240-2247
- ISSN
- 0021-972X (ISSN-L)
- 1945-7197
- OpenAlex
- W1976844022
- Cited by
- 574
- References
- 21
- Citations by year
- 2026: 8 · 2025: 20 · 2024: 20 · 2023: 25 · 2022: 29 · 2021: 23 · 2020: 37 · 2019: 38 · 2018: 24 · 2017: 36 · 2016: 30 · 2015: 33 · 2014: 38 · 2013: 37 · 2012: 32
- FWCI
- 25.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Clinical Endocrinology & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Keywords
- macrophage infiltration, omental fat, subcutaneous adipose tissue, regional adiposity, abdominal obesity, intra-abdominal fat, obesity-related comorbidities, metabolic syndrome, MCP-1, colony-stimulating factor 1, adipose tissue inflammation, impaired glucose homeostasis
- MeSH terms
- Adult, Aged, Biopsy, Cell Movement, Female, Humans, Macrophages, Male, Middle Aged, Obesity, Omentum, RNA, Messenger, Cohort Studies, Comorbidity, Body Mass Index, Macrophage Colony-Stimulating Factor, Chemokine CCL2, Subcutaneous Fat, Abdominal
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review