Metabolic endotoxemia with obesity: Is it real and is it relevant?
Open accessAbstract
Obesity is associated with metabolic derangements in multiple tissues, which contribute to the progression of insulin resistance and the metabolic syndrome. The underlying stimulus for these metabolic derangements in obesity are not fully elucidated, however recent evidence in rodents and humans suggests that systemic, low level elevations of gut derived endotoxin (lipopolysaccharide, LPS) may play an important role in obesity related, whole-body and tissue specific metabolic perturbations. LPS initiates a well-characterized signaling cascade that elicits many pro- and anti-inflammatory pathways when bound to its receptor, Toll-Like Receptor 4 (TLR4). Low-grade elevation in plasma LPS has been termed "metabolic endotoxemia" and this state is associated with a heightened pro-inflammatory and oxidant environment often observed in obesity. Given the role of inflammatory and oxidative stress in the etiology of obesity related cardio-metabolic disease risk, it has been suggested that metabolic endotoxemia may serve a key mediator of metabolic derangements observed in obesity. This review provides supporting evidence of mechanistic associations with cell and animal models, and provides complimentary evidence of the clinical relevance of metabolic endotoxemia in obesity as it relates to inflammation and metabolic derangements in humans. Discrepancies with endotoxin detection are considered, and an alternate method of reporting metabolic endotoxemia is recommended until a standardized measurement protocol is set forth.
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Obesity is linked to deterioration of the intestinal mucosa and resultant chronic systemic inflammation.
“In addition to changes in energy metabolism, obesity has also been linked to a deterioration of the intestinal mucosa and resultant chronic, systemic inflammation, analogous to type 2 diabetes (see below) (Boutagy et al., 2016).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Boutagy et al., 2016
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Million, M., Maraninchi, M., Henry, M., Armougom, F., Richet, H., Carrieri, P., Valéro, R., Raccah, D., Vialettes, B., & Raoult, D. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.153 · Cited by 664 · see citing works
Retracted(2000) · PubMed · Cited by 13,173 · see citing works
Inflammation and metabolic disorders
Hotamisligil, G. S. (2006) · Nature · doi:10.1038/nature05485 · Cited by 9,199 · see citing works
Human gut microbes associated with obesity
Ley, R. E., Turnbaugh, P. J., Klein, S., & Gordon, J. I. (2006) · Nature · doi:10.1038/4441022a · Cited by 8,785 · see citing works
Prevalence of Overweight and Obesity in the United States, 1999-2004
Ogden, C. L., Carroll, M. D., Curtin, L. R., McDowell, M. A., Tabak, C. J., & Flegal, K. M. (2006) · JAMA · doi:10.1001/jama.295.13.1549 · Cited by 8,720 · see citing works
A core gut microbiome in obese and lean twins
Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., et al. (2009) · Nature · doi:10.1038/nature07540 · Cited by 7,823 · see citing works
Metabolic Endotoxemia Initiates Obesity and Insulin Resistance
Cani, P. D., Amar, J., Iglesias, M. A., Poggi, M., Knauf, C., Bastelica, D., Neyrinck, A. M., Fava, F., Tuohy, K. M., Chabo, C., et al. (2007) · Diabetes · doi:10.2337/db06-1491 · Cited by 6,638 · see citing works
Heart Disease and Stroke Statistics—2015 Update: A Report From the American Heart Association
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., de Ferranti, S., Després, J.-P., Fullerton, H. J., Howard, V. J., et al. (2015) · Circulation · doi:10.1161/cir.0000000000000152 · Cited by 5,797 · see citing works
Insulin signalling and the regulation of glucose and lipid metabolism
Saltiel, A. R., & Kahn, C. R. (2001) · Nature · doi:10.1038/414799a · Cited by 5,326 · see citing works
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819 · see citing works
Raetz, C. R. H., & Whitfield, C. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135414 · Cited by 4,404 · see citing works
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
LPS/TLR4 signal transduction pathway
Lu, Y.-C., Yeh, W.-C., & Ohashi, P. S. (2008) · Cytokine · doi:10.1016/j.cyto.2008.01.006 · Cited by 3,301 · see citing works
Mechanisms linking obesity with cardiovascular disease
Van Gaal, L. F., Mertens, I. L., & De Block, C. E. (2006) · Nature · doi:10.1038/nature05487 · Cited by 2,814 · see citing works
Cani, P. D., Possemiers, S., Van de Wiele, T., Guiot, Y., Everard, A., Rottier, O., Geurts, L., Naslain, D., Neyrinck, A., Lambert, D. M., et al. (2009) · Gut · doi:10.1136/gut.2008.165886 · Cited by 2,518 · see citing works
Microbiota and SCFA in lean and overweight healthy subjects
Schwiertz, A., Taras, D., Schäfer, K., Beijer, S., Bos, N. A., Donus, C., & Hardt, P. D. (2010) · Obesity · doi:10.1038/oby.2009.167 · Cited by 2,457 · see citing works
Inflammation: the link between insulin resistance, obesity and diabetes
Dandona, P. (2004) · Trends in Immunology · doi:10.1016/j.it.2003.10.013 · Cited by 2,170 · see citing works
Human gut microbiota in obesity and after gastric bypass
Zhang, H., DiBaise, J. K., Zuccolo, A., Kudrna, D., Braidotti, M., Yu, Y., Parameswaran, P., Crowell, M. D., Wing, R., Rittmann, B. E., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812600106 · Cited by 1,880 · see citing works
NF-κB activation by reactive oxygen species: Fifteen years later
Gloire, G., Legrand-Poels, S., & Piette, J. G. (2006) · Biochemical Pharmacology · doi:10.1016/j.bcp.2006.04.011 · Cited by 1,540 · see citing works
Mechanism of free fatty acid-induced insulin resistance in humans.
Roden, M., Price, T. B., Perseghin, G., Petersen, K. F., Rothman, D. L., Cline, G. W., & Shulman, G. I. (1996) · Journal of Clinical Investigation · doi:10.1172/jci118742 · Cited by 1,539 · see citing works
Gut Microbiota and Metabolic Endotoxemia in Young Obese Mexican Subjects
Radilla-Vázquez, R. B., Parra‐Rojas, I., Martínez-Hernández, N. E., Márquez‐Sandoval, F., Illades‐Aguiar, B., & Castro-Alarcón, N. (2016) · Obesity Facts · doi:10.1159/000442479 · Cited by 1,197 · see citing works
Differential Adaptation of Human Gut Microbiota to Bariatric Surgery–Induced Weight Loss
Furet, J.-P., Kong, L.-C., Tap, J., Poitou, C., Basdevant, A., Bouillot, J.-L., Mariat, D., Corthier, G., Doré, J., Henegar, C., et al. (2010) · Diabetes · doi:10.2337/db10-0253 · Cited by 1,173 · see citing works
Early differences in fecal microbiota composition in children may predict overweight
Kalliomäki, M. A., Collado, M. C., Salminen, S., & Isolauri, E. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.3.534 · Cited by 1,056 · see citing works
Creely, S. J., McTernan, P. G., Kusminski, C. M., Fisher, F. M., Da Silva, N. F., Khanolkar, M., Evans, M., Harte, A. L., & Kumar, S. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00302.2006 · Cited by 1,043 · see citing works
Santacruz, A., Collado, M. C., García-Valdés, L., Segura, M. T., Martín-Lagos, J. A., Anjos, T., Martí-Romero, M., Lopez, R. M., Florido, J., Campoy, C., et al. (2010) · British Journal of Nutrition · doi:10.1017/s0007114510000176 · Cited by 868 · see citing works
Dewulf, E. M., Cani, P. D., Claus, S. P., Fuentes, S., Puylaert, P. G., Neyrinck, A. M., Bindels, L. B., de Vos, W. M., Gibson, G. R., Thissen, J.-P., et al. (2013) · Gut · doi:10.1136/gutjnl-2012-303304 · Cited by 825 · see citing works
The homeostasis model in the San Antonio Heart Study.
Haffner, S. M., Miettinen, H., & Stern, M. P. (1997) · Diabetes Care · doi:10.2337/diacare.20.7.1087 · Cited by 788 · see citing works
Toxic Shock Syndrome and Bacterial Superantigens: An Update
McCormick, J. K., Yarwood, J. M., & Schlievert, P. M. (2001) · Annual Review of Microbiology · doi:10.1146/annurev.micro.55.1.77 · Cited by 788 · see citing works
Erridge, C., Attina, T., Spickett, C. M., & Webb, D. J. (2007) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/86.5.1286 · Cited by 776 · see citing works
The randle cycle revisited: a new head for an old hat.
Hue, L., & Taegtmeyer, H. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00093.2009 · Cited by 743 · see citing works
The endocannabinoid system links gut microbiota to adipogenesis
Muccioli, G. G., Naslain, D., Bäckhed, F., Reigstad, C. S., Lambert, D. M., Delzenne, N. M., & Cani, P. D. (2010) · Molecular Systems Biology · doi:10.1038/msb.2010.46 · Cited by 691 · see citing works
Chylomicrons promote intestinal absorption of lipopolysaccharides
Ghoshal, S., Witta, J., Zhong, J., de Villiers, W., & Eckhardt, E. (2009) · Journal of Lipid Research · doi:10.1194/jlr.m800156-jlr200 · Cited by 662 · see citing works
Park, H. S., Jung, H. Y., Park, E. Y., Kim, J., Lee, W. J., & Bae, Y. S. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.6.3589 · Cited by 635 · see citing works
Opal, S. M., Scannon, P. J., Vincent, J., White, M., Carroll, S. F., Palardy, J. E., Parejo, N. A., Pribble, J. P., & Lemke, J. H. (1999) · The Journal of Infectious Diseases · doi:10.1086/315093 · Cited by 609 · see citing works
Energy intake is associated with endotoxemia in apparently healthy men
Amar, J., Burcelin, R., Ruidavets, J. B., Cani, P. D., Fauvel, J., Alessi, M., Chamontin, B., & Ferrières, J. (2008) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/87.5.1219 · Cited by 594 · see citing works
Involvement of Reactive Oxygen Species in Toll-Like Receptor 4-Dependent Activation of NF-κB
Asehnoune, K., Strassheim, D., Mitra, S., Kim, J. Y., & Abraham, E. H. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.4.2522 · Cited by 564 · see citing works
A high-fat diet is associated with endotoxemia that originates from the gut
Pendyala, S., Walker, J. M., & Holt, P. R. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.01.034 · Cited by 546 · see citing works
Bifidobacterium longum with Fructo-Oligosaccharides in Patients with Non Alcoholic Steatohepatitis
Malaguarnera, M., Vacante, M., Antic, T., Giordano, M., Chisari, G., Acquaviva, R., Mastrojeni, S., Malaguarnera, G., Mistretta, A., Volti, G. L., et al. (2011) · Digestive Diseases and Sciences · doi:10.1007/s10620-011-1887-4 · Cited by 456 · see citing works
Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes
Song, M. J., Kim, K. H., Yoon, J. M., & Kim, J. B. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.05.170 · Cited by 454 · see citing works
Endotoxemia Is Associated With an Increased Risk of Incident Diabetes
Pussinen, P. J., Havulinna, A. S., Lehto, M. J., Sundvall, J., & Salomaa, V. V. (2011) · Diabetes Care · doi:10.2337/dc10-1676 · Cited by 407 · see citing works
Lassenius, M., Pietiläinen, K., Kaartinen, K., Pussinen, P., Syrjänen, J., Forsblom, C., Pörsti, I., Rissanen, A., Kaprio, J., Mustonen, J., et al. (2011) · Diabetes Care · doi:10.2337/dc10-2197 · Cited by 404 · see citing works
Elevated Toll-Like Receptor 4 Expression and Signaling in Muscle From Insulin-Resistant Subjects
Reyna, S. M., Ghosh, S., Tantiwong, P., Meka, C. S. R., Eagan, P. A., Jenkinson, C. P., Cersósimo, E., DeFronzo, R. A., Coletta, D. K., Sriwijitkamol, A., et al. (2008) · Diabetes · doi:10.2337/db08-0038 · Cited by 381 · see citing works
Maachi, M., Piéroni, L., Bruckert, É., Jardel, C., Fellahi, S., Hainque, B., Capeau, J., & Jp, B. (2004) · International Journal of Obesity · doi:10.1038/sj.ijo.0802718 · Cited by 379 · see citing works
Xiao, S., Fei, N., Pang, X., Shen, J., Wang, L., Zhang, B., Zhang, M. H., Zhang, X., Zhang, C., Li, M., et al. (2013) · FEMS Microbiology Ecology · doi:10.1111/1574-6941.12228 · Cited by 378 · see citing works
Endotoxemia: Methods of detection and clinical correlates
Hurley, J. C. (1995) · Clinical Microbiology Reviews · doi:10.1128/cmr.8.2.268 · Cited by 318 · see citing works
Ghanim, H., Sia, C. L., Upadhyay, M., Korzeniewski, K., Viswanathan, P., Abuaysheh, S., Mohanty, P., & Dandona, P. (2010) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2009.28584 · Cited by 299 · see citing works
Emulsified lipids increase endotoxemia: possible role in early postprandial low-grade inflammation
Laugerette, F., Vors, C., Géloën, A., Chauvin, M., Soulage, C. O., Lambert-Porcheron, S., Peretti, N., Alligier, M., Burcelin, R., Laville, M., et al. (2010) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2009.11.011 · Cited by 291 · see citing works
Lecerf, J.-M., Dépeint, F., Clerc, E., Dugenet, Y., Niamba, C. N., Rhazi, L., Cayzeele, A., Abdelnour, G., Jaruga, A., Younes, H., et al. (2012) · British Journal of Nutrition · doi:10.1017/s0007114511007252 · Cited by 262 · see citing works
Skeletal muscle insulin resistance: role of inflammatory cytokines and reactive oxygen species
Wei, Y., Chen, K., Whaley‐Connell, A. T., Stump, C. S., Ibdah, J. A., & Sowers, J. R. (2007) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00561.2007 · Cited by 258 · see citing works
Frost, R. A., Nystrom, G. J., & Lang, C. H. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00039.2002 · Cited by 253 · see citing works
Pregravid Obesity Associates With Increased Maternal Endotoxemia and Metabolic Inflammation
Basu, S., Haghiac, M., Surace, P., Challier, J.-C., Guerre-Millo, M., Singh, K., Waters, T. P., Minium, J., Presley, L. H., Catalano, P. M., et al. (2010) · Obesity · doi:10.1038/oby.2010.215 · Cited by 246 · see citing works
Deopurkar, R., Ghanim, H., Friedman, J., Abuaysheh, S., Sia, C. L., Mohanty, P., Viswanathan, P., Chaudhuri, A., & Dandona, P. (2010) · Diabetes Care · doi:10.2337/dc09-1630 · Cited by 246 · see citing works
Differential liver sensitization to Toll-like receptor pathways in mice with alcoholic fatty liver
Gustot, T., Lemmers, A., Moreno, C., Nagy, N., Quertinmont, E., Nicaise, C., Franchimont, D. P., Louis, H., Deviere, J. M., & Moine, O. L. (2006) · Hepatology · doi:10.1002/hep.21138 · Cited by 244 · see citing works
Harte, A. L., Varma, M. C., Tripathi, G., McGee, K. C., Al‐Daghri, N. M., Al-Attas, O. S., Sabico, S., O’Hare, J. P., Ceriello, A., Saravanan, P., et al. (2011) · Diabetes Care · doi:10.2337/dc11-1593 · Cited by 236 · see citing works
Dehghan, P., Pourghassem Gargari, B., & Asghari Jafar-abadi, M. (2014) · Nutrition · doi:10.1016/j.nut.2013.09.005 · Cited by 207 · see citing works
Ryan, K. A., Smith, M. F., Sanders, M. K., & Ernst, P. B. (2004) · Infection and Immunity · doi:10.1128/iai.72.4.2123-2130.2004 · Cited by 198 · see citing works
Griffiths, E. A., Duffy, L. C., Schanbacher, F. L., Qiao, H., Dryja, D., Leavens, A., Rossman, J., Rich, G. A., DiRienzo, D. B., & Ogra, P. L. O. (2004) · Digestive Diseases and Sciences · doi:10.1023/b:ddas.0000026302.92898.ae · Cited by 197 · see citing works
The Role of Bifidobacteria in Gut Barrier Function After Thermal Injury in Rats
Wang, Z., Xiao, G., Yao, Y.-M., Guo, S., Lu, K., & Sheng, Z. (2006) · The Journal of Trauma: Injury, Infection, and Critical Care · doi:10.1097/01.ta.0000196574.70614.27 · Cited by 193 · see citing works
Metabolic syndrome and oxidative stress
Ando, K., & Fujita, T. (2009) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2009.04.030 · Cited by 164 · see citing works
Bone, R. C. (1996) · Clinics in Chest Medicine · doi:10.1016/s0272-5231(05)70307-5 · Cited by 158 · see citing works
Toll-like receptor 4 modulates skeletal muscle substrate metabolism
Frisard, M. I., McMillan, R. P., Marchand, J., Wahlberg, K. A., Wu, Y., Voelker, K. A., Heilbronn, L. K., Haynie, K. R., Muoio, B. M., Li, L., et al. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00307.2009 · Cited by 157 · see citing works
Self-citationRecent advances in biosensor based endotoxin detection
Das, A. P., Kumar, P., & Swain, S. K. (2013) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2013.07.020 · Cited by 155 · see citing works
Development of endotoxin tolerance in humans in vivo
Draisma, A., Pickkers, P., Bouw, M. P. W. J. M., et al. (2009) · Critical Care Medicine · doi:10.1097/ccm.0b013e31819c3c67 · Cited by 152 · see citing works
Direct effects of endotoxin on the endothelium: barrier function and injury.
Bannerman, D. D., & Goldblum, S. E. (1999) · PubMed · Cited by 150 · see citing works
Detoxifying endotoxin: time, place and person
Munford, R. S. (2005) · Journal of Endotoxin Research · doi:10.1179/096805105x35161 · Cited by 150 · see citing works
Changes in endotoxin levels in T2DM subjects on anti-diabetic therapies
Al-Attas, O. S., Al‐Daghri, N. M., Al-Rubeaan, K. A., da Silva, N. F., Sabico, S., Kumar, S., McTernan, P. G., & Harte, A. L. (2009) · Cardiovascular Diabetology · doi:10.1186/1475-2840-8-20 · Cited by 145 · see citing works
Monte, S. V., Caruana, J. A., Ghanim, H., Sia, C. L., Korzeniewski, K., Schentag, J. J., & Dandona, P. (2012) · Surgery · doi:10.1016/j.surg.2011.09.038 · Cited by 143 · see citing works
Hudgins, L. C., Parker, T. S., Levine, D. M., Gordon, B. R., Saal, S. D., Jiang, X., Seidman, C. E., Tremaroli, J. D., Lai, J., & Rubin, A. L. (2003) · Journal of Lipid Research · doi:10.1194/jlr.m200440-jlr200 · Cited by 141 · see citing works
Continuous infusion chemotherapy: a critical review.
Vogelzang, N. J. (1984) · Journal of Clinical Oncology · doi:10.1200/jco.1984.2.11.1289 · Cited by 136 · see citing works
Hulston, C. J., Churnside, A. A., & Venables, M. (2015) · British Journal Of Nutrition · doi:10.1017/s0007114514004097 · Cited by 133 · see citing works
Laugerette, F., Alligier, M., Bastard, J., Drai, J., Chanséaume, E., Lambert-Porcheron, S., Laville, M., Morio, B., Vidal, H., & Michalski, M. (2014) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201400044 · Cited by 132 · see citing works
Endotoxemia, nutrition, and cardiometabolic disorders
Kallio, K. A. E., Hätönen, K. A., Lehto, M., Salomaa, V., Männistö, S., & Pussinen, P. J. (2015) · Acta Diabetologica · doi:10.1007/s00592-014-0662-3 · Cited by 125 · see citing works
Ding, J. L., & Ho, B. (2001) · Trends in biotechnology · doi:10.1016/s0167-7799(01)01694-8 · Cited by 115 · see citing works
Cohen, J., & McConnell, J. (1984) · The Journal of Infectious Diseases · doi:10.1093/infdis/150.6.916 · Cited by 96 · see citing works
The impairment of glucogenesis by gram negative infection
LaNoue, K. F., Mason, A. D., & Daniels, J. P. (1968) · Metabolism · doi:10.1016/0026-0495(68)90019-x · Cited by 90 · see citing works
Endotoxin Detection – from Limulus Amebocyte Lysate to Recombinant Factor C
Ding, J. L., & Ho, B. (2010) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-90-481-9078-2_9 · Cited by 89 · see citing works
Liu, X., Lu, L., Yao, P., Ma, Y., Wang, F., Jin, Q., Ye, X., Li, H., Hu, F. B., Sun, L., et al. (2014) · Diabetologia · doi:10.1007/s00125-014-3288-7 · Cited by 78 · see citing works
Limulus amebocyte lysate (LAL) detection of endotoxin in human blood
Novitsky, T. J. (1994) · Journal of Endotoxin Research · doi:10.1177/096805199400100407 · Cited by 76 · see citing works
EFFECTS OF BACTERIAL ENDOTOXINS ON METABOLISM
Berry, L. J., & Smythe, D. S. (1964) · The Journal of Experimental Medicine · doi:10.1084/jem.120.5.721 · Cited by 73 · see citing works
Deopurkar, R., Ghanim, G., Friedman, & Abuaysheh (2010) · Diabetes Care · Cited by 71 · see citing works
Limitations of the Limulus Amebocyte Lysate Test in Demonstrating Circulating Lipopolysaccharides
Novitsky, T. J. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09018.x · Cited by 65 · see citing works
Plasma endotoxin level of healthy donors
Nádházi, Z., Takáts, A., Offenmüller, K., & Bertók, L. (2002) · Acta Microbiologica et Immunologica Hungarica · doi:10.1556/amicr.49.2002.1.15 · Cited by 60 · see citing works
Alterations of mitochondrial metabolism and protein concentrations in subacute septicemia
Tavakoli, H., & Mela, L. (1982) · Infection and Immunity · doi:10.1128/iai.38.2.536-541.1982 · Cited by 60 · see citing works
Patel, P. N., Shah, R. Y., Ferguson, J. F., & Reilly, M. P. (2014) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.114.304455 · Cited by 58 · see citing works
Cytokine Abnormalities in the Etiology of the Cardiometabolic Syndrome
DeMarco, V. G., Johnson, M. S., Whaley‐Connell, A. T., & Sowers, J. R. (2010) · Current Hypertension Reports · doi:10.1007/s11906-010-0095-5 · Cited by 54 · see citing works
Low Levels of Lipopolysaccharide Modulate Mitochondrial Oxygen Consumption in Skeletal Muscle
Frisard, M. I., Wu, Y., McMillan, R. P., Voelker, K. A., Wahlberg, K. A., Anderson, A. S., Boutagy, N. E., Resendes, K., Ravussin, É., & Hulver, M. W. (2014) · Metabolism · doi:10.1016/j.metabol.2014.11.007 · Cited by 50 · see citing works
Self-citationRickels, M. R., Naji, A., & Teff, K. L. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2519 · Cited by 45 · see citing works
Prognostic value of endotoxin activity assay in patients with severe sepsis after cardiac surgery
Yaroustovsky, M., Plyushch, M., Попов, Д. А., et al. (2013) · Journal of Inflammation · doi:10.1186/1476-9255-10-8 · Cited by 45 · see citing works
Mehta, N. N., Heffron, S. P., Patel, P. N., Ferguson, J. F., Shah, R. D., Hinkle, C. C., Krishnamoorthy, P. M., Shah, R., Tabita‐Martinez, J., Terembula, K., et al. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-124 · Cited by 44 · see citing works
Temporal Metabolic Profiling of Plasma During Endotoxemia in Humans
Kamisoglu, K., Sleight, K. E., Calvano, S. E., Coyle, S. M., Corbett, S., & Androulakis, I. P. (2013) · Shock · doi:10.1097/shk.0000000000000063 · Cited by 42 · see citing works
Ortiz, S., Zapater, P., Estrada, J. L., Enriquez, P., Rey, M., Abad, Á. L., Such, J. M., Lluı́s, F., & Francés, R. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-4483 · Cited by 37 · see citing works
Altered control of carbohydrate metabolism in endotoxemia.
Jj, S., Gj, B., Mészáros, K., et al. (1989) · PubMed · Cited by 36 · see citing works
Anderson, A. S., Haynie, K. R., McMillan, R. P., Osterberg, K. L., Boutagy, N. E., Frisard, M. I., Davy, B. M., Davy, K. P., & Hulver, M. W. (2015) · Obesity · doi:10.1002/oby.21031 · Cited by 35 · see citing works
Self-citationDixon, A., Valsamakis, G., Hanif, M. W., Field, A., Boutsiadis, A., Harte, A. L., McTernan, P. G., Barnett, A. H., & Kumar, S. (2008) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2008.01800.x · Cited by 32 · see citing works
Lira, F. S., Neto, J. C. R., Pimentel, G. D., dos Santos, R. V. T., Carnier, J., Sanches, P. D. L., de Piano, A., de Souza, C. T., Tock, L., Tufik, S., et al. (2012) · Nutrition Journal · doi:10.1186/1475-2891-11-74 · Cited by 30 · see citing works
Ditter, B., Becker, K. P., URBASCHEK, R., & Urbaschek, B. (1982) · PubMed · Cited by 25 · see citing works
Buhl, M. R., Bosnjak, E., Vendelbo, M. H., Gjedsted, J., Nielsen, R. R., Krusenstjerna-Hafstrøm, T., Vestergaard, E. T., Jessen, N., Tønnesen, E., Møller, A. B., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3836 · Cited by 21 · see citing works
Interference with the LAL Test and How to Address It
Dawson, M. E., & Lal, D. (2005) · Cited by 21 · see citing works
Inhibitory Effect of Heparin on the Limulus Test for Endotoxin
Sullivan, J. D., & Watson, S. W. (1975) · Journal of Clinical Microbiology · doi:10.1128/jcm.2.2.151-151.1975 · Cited by 20 · see citing works
Quantification of endotoxin inhibition in serum and plasma using a turbidimetric LAL assay.
Novitsky, T. J., & Roslansky, P. F. (1985) · PubMed · Cited by 17 · see citing works
Delafield, M. E. (1932) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700350108 · Cited by 14 · see citing works
Zeckwer, I. T., & Goodell, H. (1925) · The Journal of Experimental Medicine · doi:10.1084/jem.42.1.57 · Cited by 13 · see citing works
Morita, T., Nakamura, T., Miyata, T., et al. (1985) · PubMed · Cited by 11 · see citing works
Haimovich, B., Zhang, Z., Calvano, J. E., Calvano, S. E., Kumar, A., Macor, M., Corbett, S., Coyle, S. M., & Lowry, S. F. (2013) · Annals of Surgery · doi:10.1097/sla.0b013e31829a4352 · Cited by 8 · see citing works
Galgani, J. E., & Moro, C. (2014) · Obesity · doi:10.1002/oby.20933 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [47]Gregor MF Hotamisligil GS Inflammatory mechanisms in obesity Annual Review of Immunology 2011 29 415 445 21219177
Cited by
Sorted by citations
Postler, T. S., & Ghosh, S. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.05.008 · Cited by 876 · see citing works
“In addition to changes in energy metabolism, obesity has also been linked to a deterioration of the intestinal mucosa and resultant chronic, systemic inflammation, analogous to type 2 diabetes (see below) (Boutagy et al., 2016).”
BackgroundRole of Metabolic Endotoxemia in Systemic Inflammation and Potential Interventions
Mohammad, S., & Thiemermann, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.594150 · Cited by 585 · see citing works
Endotoxemia—menace, marker, or mistake?
Munford, R. S. (2016) · Journal of Leukocyte Biology · doi:10.1189/jlb.3ru0316-151r · Cited by 219 · see citing works
New insights into the role of adipose tissue in thrombosis
Vilahur, G., Ben-Aicha, S., & Badimon, L. (2017) · Cardiovascular Research · doi:10.1093/cvr/cvx086 · Cited by 216 · see citing works
The initiation of metabolic inflammation in childhood obesity
Singer, K., & Lumeng, C. N. (2017) · Journal of Clinical Investigation · doi:10.1172/jci88882 · Cited by 194 · see citing works
Endotoxin-initiated inflammation reduces testosterone production in men of reproductive age
Tremellen, K., McPhee, N., Pearce, K., Benson, S., Schedlowski, M., & Engler, H. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00279.2017 · Cited by 98 · see citing works
Wang, Y., Yang, J., Wang, W., Sanidad, K. Z., Cinelli, M. A., Wan, D., Hwang, S. H., Kim, D., Lee, K. S. S., Xiao, H., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1916189117 · Cited by 59 · see citing works
Seth, R. K., Kimono, D., Alhasson, F., Sarkar, S., Albadrani, M., Lasley, S. K., Horner, R., Janulewicz, P., Nagarkatti, M., Nagarkatti, P., et al. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.05.006 · Cited by 55 · see citing works
Fedirko, V., Tran, H. Q., Gewirtz, A. T., Stepien, M., Trichopoulou, A., Aleksandrova, K., Olsen, A., Tjønneland, A., Overvad, K., Carbonnel, F., et al. (2017) · BMC Medicine · doi:10.1186/s12916-017-0830-8 · Cited by 50 · see citing works
Metabolic endotoxaemia related inflammation is associated with hypogonadism in overweight men
Tremellen, K., McPhee, N., & Pearce, K. (2017) · Basic and Clinical Andrology · doi:10.1186/s12610-017-0049-8 · Cited by 45 · see citing works
Ramos, F. M. M., Ribeiro, C. B., Cesar, T. B., Milenkovic, D., Cabral, L., Noronha, M. F., & Sivieri, K. (2023) · Food Science & Nutrition · doi:10.1002/fsn3.3654 · Cited by 17 · see citing works
- Authors
- Boutagy, N. E., McMillan, R. P., Frisard, M. I., & Hulver, M. W.
- Affiliations
- Virginia Tech (US)
- Corresponding author
- Hulver, Matthew W.
- Venue
- Biochimie
- Publisher
- Elsevier BV
- Published
- 2016-05
- Volume
- 124
- Pages
- 11-20
- ISSN
- 0037-9042 (ISSN-L)
- 0300-9084
- PMC
- PMC4695328
- OpenAlex
- W769942964
- Cited by
- 413
- References
- 105
- Citations by year
- 2026: 25 · 2025: 32 · 2024: 41 · 2023: 37 · 2022: 38 · 2021: 55 · 2020: 52 · 2019: 44 · 2018: 33 · 2017: 33 · 2016: 20 · 2015: 3
- FWCI
- 3.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biochimie (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R56DK078765, R01DK078765)
- Topics
- Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- metabolic endotoxemia, obesity, lipopolysaccharide, gut-derived endotoxin, TLR4, insulin resistance, metabolic syndrome, inflammation, oxidative stress, cardiometabolic disease, endotoxin detection
- MeSH terms
- Animals, Humans, Inflammation, Intestinal Mucosa, Lipopolysaccharides, Obesity, Oxidative Stress, Endotoxemia, Toll-Like Receptor 4
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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.
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