Elevated Circulating Levels of Tumor Necrosis Factor in Severe Chronic Heart Failure

Levine, Beth; Kalman, Jill; Mayer, Lloyd; Fillit, Howard M.; Packer, Milton

doi:10.1056/nejm199007263230405

Cited by 2,582Heart Failure Treatment and ManagementCardiac Fibrosis and RemodelingNutrition and Health in Aging

Elevated Circulating Levels of Tumor Necrosis Factor in Severe Chronic Heart Failure

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Levine, Beth, Kalman, Jill, Mayer, Lloyd, Fillit, Howard M., Packer, Milton·1990·New England Journal of Medicine

DOI 10.1056/nejm199007263230405

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Abstract

BACKGROUND AND METHODS: Although cachexia often accompanies advanced heart failure, little is known about the causes of the cachectic state. To assess the potential role of tumor necrosis factor in the pathogenesis of cardiac cachexia, we measured serum levels of the factor in 33 patients with chronic heart failure, 33 age-matched healthy controls, and 9 patients with chronic renal failure. RESULTS: Mean (+/- SEM) serum levels of tumor necrosis factor were higher in the patients with heart failure (115 +/- 25 U per milliliter) than in the healthy controls (9 +/- 3 U per milliliter; P less than 0.001). Nineteen of the patients with chronic heart failure had serum levels of tumor necrosis factor greater than or equal to 39 U per milliliter (greater than 2 SD above the mean value for the control group), whereas the remaining 14 patients had serum levels of tumor necrosis factor below this level. The patients with high levels of tumor necrosis factor were more cachectic than those with low levels (82 +/- 3 vs. 95 +/- 6 percent of ideal body weight, respectively; P less than 0.05) and had more advanced heart failure, as evidenced by their higher values for plasma renin activity (2.92 +/- 0.53 vs. 1.06 +/- 0.53 ng per liter per second [10.5 +/- 1.9 vs. 3.8 +/- 1.9 ng per milliliter per hour]; P less than 0.01) and lower serum sodium concentration (135 +/- 1 vs. 138 +/- 1 mmol per liter; P less than 0.05). The group with high levels of tumor necrosis factor also had lower hemoglobin levels (7.82 +/- 0.2 vs. 8.69 +/- 0.4 mmol per liter [12.6 +/- 0.4 vs. 14.0 +/- 0.6 g per deciliter]) and higher values for blood urea nitrogen (19.5 +/- 2.2 vs. 12.5 +/- 1.8 mmol per liter) than the group with low levels of tumor necrosis factor (P less than 0.05 for both). The high levels of tumor necrosis factor were not due solely to decreased renal clearance, however, since the levels in the patients with heart failure were considerably higher than those in the nine patients with chronic renal failure (115 +/- 25 vs. 45 +/- 25 U per milliliter; P less than 0.05). CONCLUSIONS: These findings indicate that circulating levels of tumor necrosis factor are increased in cachectic patients with chronic heart failure and that this elevation is associated with the marked activation of the renin-angiotensin system seen in patients with end-stage cardiac disease.

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In congestive heart failure, pro-inflammatory cytokines TNF, IL-6, and IL-1 are markedly elevated, and TNF level is a negative prognostic factor.
“in patients with congestive heart failure, the levels of pro-inflammatory cytokines, especially TNF, IL-6, and IL-1, are markedly elevated, and the TNF level is a negative prognostic factor”
From Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty (2018) · cites this paper as [191]

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Pathophysiologically Relevant Concentrations of Tumor Necrosis Factor-α Promote Progressive Left Ventricular Dysfunction and Remodeling in Rats
Bozkurt, B., Kribbs, S. B., Clubb, F. J., Michael, L. H., Didenko, V. V., Hornsby, P. J., Seta, Y., Oral, H., Spinale, F. G., & Mann, D. L. (1998) · Circulation · doi:10.1161/01.cir.97.14.1382 · Cited by 821 · see citing works
“In preliminary control experiments using TNF-a infusion rates of 0.125 to 7.5mg z kg21 z min21, we established that an infusion rate of 2.5 mg z kg21 z min21 resulted in systemic levels of biologically active TNF-a comparable to those reported in patients with heart failure, that is,'80 to 100 U/mL.1 Accordingly, this…”
ResultInfluential
Plasma Cytokine Parameters and Mortality in Patients With Chronic Heart Failure
Rauchhaus, M., Doehner, W., Francis, D. P., Davos, C., Kemp, M., Liebenthal, C., Niebauer, J., Hooper, J., Volk, H.-D., Coats, A. J. S., et al. (2000) · Circulation · doi:10.1161/01.cir.102.25.3060 · Cited by 810 · see citing works
Are there two types of malnutrition in chronic renal failure? Evidence for relationships between malnutrition, inflammation and atherosclerosis (MIA syndrome)
Stenvinkel, P., Heimbürger, O., Lindholm, B., Kaysen, G. A., & Bergström, J. P. (2000) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/15.7.953 · Cited by 812 · see citing works
The Obesity Paradox: Body Mass Index and Outcomes in Patients With Heart Failure
Curtis, J. P., Selter, J. G., Wang, Y., Rathore, S. S., Jovin, I. S., Jadbabaie, F., Kosiborod, M., Portnay, E. L., Sokol, S. I., Bader, F., et al. (2005) · Archives of Internal Medicine · doi:10.1001/archinte.165.1.55 · Cited by 809 · see citing works
Hormonal changes and catabolic/anabolic imbalance in chronic heart failure and their importance for cardiac cachexia
Anker, S. D., Chua, T. P., Ponikowski, P., Harrington, D., Swan, J. W., Kox, W. J., Poole-Wilson, P. A., & Coats, A. J. S. (1997) · Circulation · doi:10.1161/01.cir.96.2.526 · Cited by 800 · see citing works
Reappraising the role of inflammation in heart failure
Adamo, L., Resende, C. R., Prabhu, S. D., & Mann, D. L. (2020) · Nature Reviews Cardiology · doi:10.1038/s41569-019-0315-x · Cited by 773 · see citing works
Tumor necrosis factor in the heart
Meldrum, D. R. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.274.3.r577 · Cited by 747 · see citing works
Inflammatory Markers and Risk of Heart Failure in Elderly Subjects Without Prior Myocardial Infarction
Vasan, R. S., SULLIVAN, L. M., Roubenoff, R., Dinarello, C. A., Harris, T. B., Benjamin, E. J., Sawyer, D. B., Levy, D. A., Wilson, P. W. F., & D’Agostino, R. B. (2003) · Circulation · doi:10.1161/01.cir.0000057810.48709.f6 · Cited by 749 · see citing works
Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure.
MANCINI, D. M., Walter, G., Reichek, N., Lenkinski, R. E., McCully, K. K., Mullen, J. L., & Wilson, J. R. (1992) · Circulation · doi:10.1161/01.cir.85.4.1364 · Cited by 736 · see citing works
Tumor necrosis factor alpha-induced apoptosis in cardiac myocytes. Involvement of the sphingolipid signaling cascade in cardiac cell death.
Krown, K. A., Pagé, M., Nguyen, C., Zechner, D., Gutierrez, V., Comstock, K. L., Glembotski, C. C., Quintana, P. J. E., & Sabbadini, R. A. (1996) · Journal of Clinical Investigation · doi:10.1172/jci119114 · Cited by 728 · see citing works
Prognostic importance of weight loss in chronic heart failure and the effect of treatment with angiotensin-converting-enzyme inhibitors: an observational study
Anker, S. D., Negassa, A., Coats, A. J. S., Afzal, R., Poole-Wilson, P. A., Cohn, J. N., & Yusuf, S. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12892-9 · Cited by 725 · see citing works
The use of subcutaneous erythropoietin and intravenous iron for the treatment of the anemia of severe, resistant congestive heart failure improves cardiac and renal function and functional cardiac class, and markedly reduces hospitalizations
Silverberg, D. S., Wexler, D., Blum, M., Keren, G., Sheps, D. S., Leibovitch, E., Brosh, D., Laniado, S., Schwartz, D., Yachnin, T., et al. (2000) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(00)00613-6 · Cited by 725 · see citing works
“Tumor necrosis factor blood levels have been found to be elevated in CHF (51,52), have been found to correlate with the severity of the anemia (51,53) and may cause bone marrow depression (53), interference in the action of EPO (53) and in the cellular release and utilization of Fe (54).”
Background
Report of the Conference on Low Blood Cholesterol: Mortality Associations.
Jacobs, D. R., Blackburn, H., HIGGINS, M. W., REED, D. M., Iso, H., McMillan, G. C., Neaton, J. D., Nelson, J., Potter, J., & Rifkind, B. M. (1992) · Circulation · doi:10.1161/01.cir.86.3.1046 · Cited by 718 · see citing works
Cellular basis for the negative inotropic effects of tumor necrosis factor-alpha in the adult mammalian heart.
Yokoyama, T., Vaca, L. A., Rossen, R. D., Durante, W., Hazarika, P., & Mann, D. L. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116834 · Cited by 714 · see citing works
Association of serum albumin and mortality risk
Goldwasser, P., & Feldman, J. G. (1997) · Journal of Clinical Epidemiology · doi:10.1016/s0895-4356(97)00015-2 · Cited by 716 · see citing works
Pathophysiology of cardiac hypertrophy and heart failure: signaling pathways and novel therapeutic targets
Tham, Y. K., Bernardo, B. C., Ooi, J. Y. Y., Weeks, K. L., & McMullen, J. R. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1477-x · Cited by 707 · see citing works
“…levels of the pro-inflammatory cytokine TNF-α in animal models of cardiac disease (Aker et al. 2003; Marin-Garcia et al. 2001; Recchia et al. 2000) and patients with HF (Aukrust et al. 1999; Kubota et al. 1998; Levine et al. 1990; Munger et al. 1996; Petretta et al. 2000; Torre-Amione et al. 1996).”
Background
JCS 2017/JHFS 2017 Guideline on Diagnosis and Treatment of Acute and Chronic Heart Failure ― Digest Version ―
Tsutsui, H., Isobe, M., Ito, H., Ito, H., Okumura, K., Ōno, M., Kitakaze, M., Kinugawa, K., Kihara, Y., Goto, Y., et al. (2019) · Circulation Journal · doi:10.1253/circj.cj-19-0342 · Cited by 708 · see citing works
Innate Immunity and the Failing Heart
Mann, D. L. (2015) · Circulation Research · doi:10.1161/circresaha.116.302317 · Cited by 690 · see citing works
Reverse epidemiology of conventional cardiovascular risk factors in patients with chronic heart failure
Kalantar‐Zadeh, K., Block, G., Horwich, T. B., & Fonarow, G. C. (2004) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2003.11.039 · Cited by 689 · see citing works
Altered intestinal function in patients with chronic heart failure
Sandek, A., Bauditz, J., Swidsinski, A., Buhner, S., Weber-Eibel, J., von Haehling, S., Schroedl, W., Karhausen, T., Doehner, W., Rauchhaus, M., et al. (2007) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2007.07.016 · Cited by 661 · see citing works
“lasma levels of pro-inflammatory cytokines, such as tumor ecrosis factor (TNF)-alpha, are long known to be related o disease severity in CHF patients (1) and to predict poor urvival (2).”
Background
Red cell distribution width in heart failure: Prediction of clinical events and relationship with markers of ineffective erythropoiesis, inflammation, renal function, and nutritional state
Förhécz, Z., Gombos, T., Borgulya, G., Pozsonyi, Z., Prohászka, Z., & Jánoskuti, L. (2009) · American Heart Journal · doi:10.1016/j.ahj.2009.07.024 · Cited by 663 · see citing works
Plasma N-Terminal Pro–Brain Natriuretic Peptide and Adrenomedullin
Richards, M., Nicholls, M. G., Yandle, T. G., Frampton, C. M., Espiner, E. A., Turner, J. G., Buttimore, R. C., Lainchbury, J. G., Elliott, J. M., Ikram, H., et al. (1998) · Circulation · doi:10.1161/01.cir.97.19.1921 · Cited by 646 · see citing works
Inflammatory mediators in chronic heart failure: an overview
Anker, S. D., & von Haehling, S. (2004) · Heart · doi:10.1136/hrt.2002.007005 · Cited by 627 · see citing works
Cytokine Patterns in Patients After Major Vascular Surgery, Hemorrhagic Shock, and Severe Blunt Trauma Relation with Subsequent Adult Respiratory Distress Syndrome and Multiple Organ Failure
Roumen, R. M. H., Hendriks, T., van der Ven‐Jongekrijg, J., Nieuwenhuijzen, G. A. P., Sauerwein, R. W., van der Meer, J. W. M., & Goris, R. J. A. (1993) · Annals of Surgery · doi:10.1097/00000658-199312000-00011 · Cited by 617 · see citing works
Cardiac Failure in Transgenic Mice With Myocardial Expression of Tumor Necrosis Factor-α
Bryant, D. D., Becker, L., Richardson, J. A., Shelton, J. M., Franco, F., Peshock, R. M., Thompson, M. T., & Giroir, B. P. (1998) · Circulation · doi:10.1161/01.cir.97.14.1375 · Cited by 593 · see citing works
Apoptosis in heart failure: Release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy
Narula, J., Pandey, P., Arbustini, E., Haider, N., Narula, N., Kolodgie, F. D., Bello, B. D., Semigran, M. J., Bielsa-Masdeu, A., Dec, G. W., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.14.8144 · Cited by 586 · see citing works
Interleukin-6 Spillover in the Peripheral Circulation Increases With the Severity of Heart Failure, and the High Plasma Level of Interleukin-6 Is an Important Prognostic Predictor in Patients With Congestive Heart Failure
Tsutamoto, T., 久永, 智., Wada, A., Maeda, K., Ohnishi, M., 深井, 大., Mabuchi, N., Sawaki, M., & Kinoshita, M. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(97)00494-4 · Cited by 563 · see citing works
“Why are the plasma IL-6 levels increased in patients with CHF? Because both TNF-alpha and ET-1 are increased in CHF (5,6,12,21) and stimulate IL-6 production in the endothelium in vitro (26,32), we hypothesized that IL-6 spillover is regulated by the local plasma levels of TNF-alpha and ET-1.”
Background
Reduction in the incidence of myocardial infarction in patients with rheumatoid arthritis who respond to anti–tumor necrosis factor α therapy: Results from the British Society for Rheumatology Biologics Register
Dixon, W. G., Watson, K. D., Lunt, M., Hyrich, K. L., Silman, A. J., & Symmons, D. P. M. (2007) · Arthritis & Rheumatism · doi:10.1002/art.22809 · Cited by 557 · see citing works
“Raised levels of TNF in chronic heart failure (28), along with the predictive value of high levels of TNF on adverse outcome in chronic heart failure (29), led to studies to explore the potential benefit of anti-TNF therapy in severe chronic heart failure.”
Background
Increased Oxidative Stress in Patients With Congestive Heart Failure 11This study was supported by a grant jointly sponsored by the Medical Research Council of Canada, Ottawa and Bayer Pharmaceuticals, Etobicoke, Ontario, Canada.
Keith, M. E., Geranmayegan, A., Sole, M. J., Kurian, R., Robinson, A., Omran, A., & Jeejeebhoy, K. N. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(98)00101-6 · Cited by 556 · see citing works
“This finding is not surprising because a number of factors associated with heart failure, such as increased plasma catecholamines (5), cardiac sympathetic tone (6), microvascular reperfusion injury (7,8), cytokine stimulation ( 9 ,10) and mitochondrial deoxyribonucleic acid mutations (11) (particularly complex I), are…”
From Myocarditis to Cardiomyopathy: Mechanisms of Inflammation and Cell Death
Kawai, C. (1999) · Circulation · doi:10.1161/01.cir.99.8.1091 · Cited by 550 · see citing works
Endothelial function in chronic congestive heart failure
Drexler, H., Hayoz, D., Münzel, T. F., Hornig, B., Just, H., Brunner, H. R., & ZELIS, R. F. (1992) · The American Journal of Cardiology · doi:10.1016/0002-9149(92)90710-g · Cited by 549 · see citing works
Mechanisms of Vascular Smooth Muscle Contraction and the Basis for Pharmacologic Treatment of Smooth Muscle Disorders
Brozovich, F. V., Nicholson, C., Degen, C. V., Gao, Y. Z., Aggarwal, M., & Morgan, K. G. (2016) · Pharmacological Reviews · doi:10.1124/pr.115.010652 · Cited by 539 · see citing works
“gressive elevation of the proinflammatory marker TNF-a (Levine et al., 1990; Torre-Amione et al., 1996), which has been demonstrated to contribute to endothelial dysfunction and also an increase in vascular tone that is produced by a RhoA/Rho kinase-mediated inhibition of MLC phosphatase (Parris et al.”
Background
Circulating Levels of Cytokines and Their Endogenous Modulators in Patients With Mild to Severe Congestive Heart Failure Due to Coronary Artery Disease or Hypertension
TESTA, M., YEH, M., Lee, P. C., Berman, J. W., LeJemtel, T. H., Fanelli, R., & Loperfido, F. (1996) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(96)00268-9 · Cited by 539 · see citing works
Tumor Necrosis Factor Soluble Receptors in Patients With Various Degrees of Congestive Heart Failure
Ferrari, R., Bachetti, T., Confortini, R., Opasich, C., Febo, O., Corti, A., Cassani, G., & Visioli, O. (1995) · Circulation · doi:10.1161/01.cir.92.6.1479 · Cited by 535 · see citing works
The NF-κB Regulatory Network
Brasier, A. R. (2006) · Cardiovascular Toxicology · doi:10.1385/ct:6:2:111 · Cited by 528 · see citing works
Effect of inflammatory cytokines on hypoxia-induced erythropoietin production
Wc, F., Schneider, T., & Goldberg, M. (1992) · Blood · doi:10.1182/blood.v79.8.1987.1987 · Cited by 518 · see citing works
Exercise limitation in chronic heart failure: Central role of the periphery
Clark, A. L., Poole-Wilson, P. A., & Coats, A. J. S. (1996) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(96)00323-3 · Cited by 523 · see citing works
Increased circulating cytokines in patients with myocarditis and cardiomyopathy.
Matsumori, A., Yamada, T., Suzuki, H., Matoba, Y., & Sasayama, S. (1994) · Heart · doi:10.1136/hrt.72.6.561 · Cited by 524 · see citing works
Adaptation and Maladaptation of the Heart in Diabetes: Part I
Taegtmeyer, H., McNulty, P. H., & Young, M. E. (2002) · Circulation · doi:10.1161/01.cir.0000012466.50373.e8 · Cited by 517 · see citing works
Evidence for a relation between metabolic derangements and increased levels of inflammatory mediators in a subgroup of patients with chronic obstructive pulmonary disease.
Schols, A. M. W. J., Buurman, W. A., den Brekel, A. J. S.-V., Dentener, M. A., & Wouters, E. F. �. (1996) · Thorax · doi:10.1136/thx.51.8.819 · Cited by 520 · see citing works
Vascular Oxidative Stress and Endothelial Dysfunction in Patients With Chronic Heart Failure
Landmesser, U., Spiekermann, S., Dikalov, S., Tatge, H., Wilke, R., Kohler, C., Harrison, D. G., Hornig, B., & Drexler, H. (2002) · Circulation · doi:10.1161/01.cir.0000041431.57222.af · Cited by 517 · see citing works
Elevated circulating tumor necrosis factor levels in Alzheimer's disease
Fillit, H. M., Ding, W., Buée, L., Kalman, J., Altstiel, L. D., LAWLOR, B. A., & Wolf-Klein, G. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90490-k · Cited by 513 · see citing works
Self-citation
Inhibitory Effects of Antioxidants on Neonatal Rat Cardiac Myocyte Hypertrophy Induced by Tumor Necrosis Factor-α and Angiotensin II
Nakamura, K., Fushimi, K., Kouchi, H., Mihara, K., Miyazaki, M., Ohe, T., & Namba, M. (1998) · Circulation · doi:10.1161/01.cir.98.8.794 · Cited by 510 · see citing works
The role of tumor necrosis factor in the pathophysiology of heart failure
Feldman, A. M., Combes, A., Wagner, D., Kadakomi, T., Kubota, T., Li, Y. Y., & McTiernan, C. F. (2000) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(99)00600-2 · Cited by 502 · see citing works
“(31) demonstrated that circulating levels of”
The Impact of Obesity on the Cardiovascular System
Csige, I., Ujvárosy, D., Szabó, Z., Lőrincz, I., Paragh, G., Harangi, M., & Somodi, S. (2018) · Journal of Diabetes Research · doi:10.1155/2018/3407306 · Cited by 518 · see citing works
Skeletal muscle wasting in cachexia and sarcopenia: molecular pathophysiology and impact of exercise training
Lenk, K., Schuler, G. C., & Adams, V. (2010) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1007/s13539-010-0007-1 · Cited by 492 · see citing works
“Since the influential report of elevated levels of TNF-α in patients with cardiac cachexia, it has become clear that proinflammatory cytokines play an important role in the evolvement of cachexia and other muscle wasting disorders [58].”
Background
Expression of Inducible Nitric Oxide Synthase in Human Heart Failure
Haywood, G. A., Tsao, P. S., von der Leyen, H. E., Mann, M. J., Keeling, P. J., Trindade, P. T., Lewis, N. P., Byrne, C. D., Rickenbacher, P. R., Bishopric, N. H., et al. (1996) · Circulation · doi:10.1161/01.cir.93.6.1087 · Cited by 490 · see citing works
Inflammatory Markers and Incident Heart Failure Risk in Older Adults
Kalogeropoulos, A., Georgiopoulou, V., Psaty, B. M., Rodondi, N., Smith, A. L., Harrison, D. G., Liu, Y., Hoffmann, U., Bauer, D. C., Newman, A. B., et al. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2009.12.045 · Cited by 478 · see citing works
Pathophysiology of chronic heart failure
Packer, M. (1992) · The Lancet · doi:10.1016/0140-6736(92)90405-r · Cited by 474 · see citing works
Self-citation
Chronic Administration of Ghrelin Improves Left Ventricular Dysfunction and Attenuates Development of Cardiac Cachexia in Rats With Heart Failure
Nagaya, N., Uematsu, M., Kojima, M., Ikeda, Y., Yoshihara, F., Shimizu, W., Hosoda, H., Hirota, Y., Ishida, H., Mori, H., et al. (2001) · Circulation · doi:10.1161/hc3601.095575 · Cited by 471 · see citing works
Medical Therapy Can Improve the Biological Properties of the Chronically Failing Heart
Eichhorn, E. J., & Bristow, M. R. (1996) · Circulation · doi:10.1161/01.cir.94.9.2285 · Cited by 468 · see citing works
Adaptation and Maladaptation of the Heart in Diabetes: Part II
Young, M. E., McNulty, P. H., & Taegtmeyer, H. (2002) · Circulation · doi:10.1161/01.cir.0000012467.61045.87 · Cited by 465 · see citing works
The severe cardiorenal syndrome: ‘Guyton revisited’
Bongartz, L. G., Cramer, M. J., Doevendans, P. A., Joles, J. A., & Braam, B. G. (2004) · European Heart Journal · doi:10.1093/eurheartj/ehi020 · Cited by 459 · see citing works
C-Reactive Protein in Heart Failure
Anand, I. S., Latini, R., Florea, V. G., Kuskowski, M. A., Rector, T. S., Masson, S., Signorini, S. G., Mocarelli, P., Hester, A., Glazer, R. D., et al. (2005) · Circulation · doi:10.1161/circulationaha.104.508465 · Cited by 457 · see citing works
Case Reports of Heart Failure after Therapy with a Tumor Necrosis Factor Antagonist
Kwon, H., Cot, T. R., Cuffe, M. S., Kramer, J. M., & Braun, M. M. (2003) · Annals of Internal Medicine · doi:10.7326/0003-4819-138-10-200305200-00008 · Cited by 455 · see citing works
“More than a decade ago, Levine and colleagues (1) demonstrated increased serum levels of tumor necrosis factor (TNF) in patients with advanced heart failure.”
Background
Cytokine network in congestive heart failure secondary to ischemic or idiopathic dilated cardiomyopathy
Aukrust, P., Ueland, T., Lien, E., Bendtzen, K., Müller, F., Andreassen, A. K., Nordøy, I., Aass, H., Espevik, T., Simonsen, S., et al. (1999) · The American Journal of Cardiology · doi:10.1016/s0002-9149(98)00872-8 · Cited by 454 · see citing works
Stress, depression and cardiovascular dysregulation: A review of neurobiological mechanisms and the integration of research from preclinical disease models
Grippo, A. J., & Johnson, A. K. (2009) · Stress · doi:10.1080/10253890802046281 · Cited by 451 · see citing works
“2004) and may be increased in humans with CHF associated with ischemic heart disease (Levine et al. 1990).”
Background
Basic mechanisms in heart failure: The cytokine hypothesis
Seta, Y., Shan, K., Bozkurt, B., Oral, H., & Mann, D. L. (1996) · Journal of Cardiac Failure · doi:10.1016/s1071-9164(96)80047-9 · Cited by 444 · see citing works
Troponin Elevation in Heart Failure
Kociol, R. D., Pang, P. S., Gheorghiade, M., Fonarow, G. C., O’Connor, C. M., & Felker, G. M. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2010.06.016 · Cited by 444 · see citing works
Prevalence and etiology of idiopathic dilated cardiomyopathy (summary of a National Heart, Lung, and Blood Institute Workshop)
Manolio, T. A., Baughman, K. L., Rodeheffer, R. R., Pearson, T. A., Bristow, J. D., Michels, V. V., Abelmann, W. H., & Harlan, W. R. (1992) · The American Journal of Cardiology · doi:10.1016/0002-9149(92)90901-a · Cited by 432 · see citing works
Pathogenic Gut Flora in Patients With Chronic Heart Failure
Pasini, E., Aquilani, R., Testa, C., Baiardi, P., Angioletti, S., Boschi, F., Verri, M., & Dioguardi, F. S. (2015) · JACC Heart Failure · doi:10.1016/j.jchf.2015.10.009 · Cited by 440 · see citing works
Congestive Heart Failure: Fifty Years of Progress
D, E. B. M., & Bristow, M. R. (2000) · Circulation · doi:10.1161/01.cir.102.suppl_4.iv-14 · Cited by 474 · see citing works
Interplay of matrix metalloproteinases, tissue inhibitors of metalloproteinases and their regulators in cardiac matrix remodeling
Li, Y. (2000) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00003-1 · Cited by 434 · see citing works
Elevated circulating level of ghrelin in cachexia associated with chronic heart failure: relationships between ghrelin and anabolic/catabolic factors.
Nagaya, N., Uematsu, M., Kojima, M., Date, Y., Nakazato, M., Okumura, H., Hosoda, H., Shimizu, W., Yamagishi, M., Oya, H., et al. (2001) · PubMed · doi:10.1161/hc4201.097836 · Cited by 434 · see citing works
“A maleimide activated mariculture keyhole limpet hemocyanin (mcKLH)-[Cys 0]-ghrelin [13-28] conjugate was used for immunization.”
BackgroundMethod
Cardiovascular Disease, Interleukin-6, and Risk of Mortality in Older Women
Volpato, S., Guralnik, J. M., Ferrucci, L., Balfour, J. L., Chaves, P. H. M., Fried, L. P., & Harris, T. B. (2001) · Circulation · doi:10.1161/01.cir.103.7.947 · Cited by 434 · see citing works
The malnutrition, inflammation, and atherosclerosis (MIA) syndrome - the heart of the matter
Pecoits‐Filho, R., Lindholm, B., & Stenvinkel, P. (2002) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/17.suppl_11.28 · Cited by 430 · see citing works
“In the general population, CHF is associated with both malnutrition (cardiac cachexia) and increased levels of pro-inflammatory cytokines [30].”
Background
Meta-Analysis of the Relation of Body Mass Index to All-Cause and Cardiovascular Mortality and Hospitalization in Patients With Chronic Heart Failure
Sharma, A., Lavie, C. J., BORER, J. S., Vallakati, A., Goel, S., López-Jiménez, F. A., Arbab‐Zadeh, A., Mukherjee, D., & Lazar, J. (2015) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2015.02.024 · Cited by 425 · see citing works
“Higher levels of circulating lipoproteins found in overweight/obese HF patients may bind and then detoxify lipopolysaccharides and have a potential anti-inflammatory effect [15, 14, 21].”
Muscle wasting and cachexia in heart failure: mechanisms and therapies
von Haehling, S., Ebner, N., dos Santos, M. R., Springer, J., & Anker, S. D. (2017) · Nature Reviews Cardiology · doi:10.1038/nrcardio.2017.51 · Cited by 427 · see citing works
Cardiorenal Syndrome Type 1
Ronco, C., Cicoira, M., & McCullough, P. A. (2012) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2012.01.077 · Cited by 423 · see citing works
Angiotensin II regulates the synthesis of proinflammatory cytokines and chemokines in the kidney
Ruiz‐Ortega, M., Rupérez, M., Lorenzo, Ó., Esteban, V., Blanco, J., Mezzano, S. A., & Egido, J. (2002) · Kidney International · doi:10.1046/j.1523-1755.62.s82.4.x · Cited by 420 · see citing works
“In patients with end-stage cardiac disease, circulating TNF-a concentrations are increased associated with marked activation of RA”
Background
Tumor necrosis factor-alpha and interleukin-1 beta synergistically depress human myocardial function
Cain, B. S., Meldrum, D. R., Dinarello, C. A., Meng, X., Joo, K. S., Banerjee, A. M., & Harken, A. H. (1999) · Critical Care Medicine · doi:10.1097/00003246-199907000-00018 · Cited by 420 · see citing works
Inflammatory Cytokines and Chemokines as Therapeutic Targets in Heart Failure
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Authors: Levine, B., Kalman, J., Mayer, L., Fillit, H. M., & Packer, M.
Affiliations: City University of New York (US)
ORCID: Levine, Beth
Fillit, Howard M.
Packer, Milton
Venue: New England Journal of Medicine
Publisher: Massachusetts Medical Society
Published: 1990-07-26
Volume: 323
Issue: 4
Pages: 236-241
ISSN: 0028-4793 (ISSN-L)
1533-4406
DOI: 10.1056/nejm199007263230405
OpenAlex: W2324476825
Cited by: 2,582
References: 55
Citations by year: 2026: 21 · 2025: 43 · 2024: 49 · 2023: 34 · 2022: 70 · 2021: 63 · 2020: 64 · 2019: 64 · 2018: 59 · 2017: 64 · 2016: 58 · 2015: 70 · 2014: 75 · 2013: 73 · 2012: 79
FWCI: 29.44
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: New England Journal of Medicine (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (7r01hl025055-11, 5r01ca041583-06, 5k04hl001229-02)
National Heart, Lung, and Blood Institute (KO4-HL-01229, R01-HL-25055)
National Cancer Institute (R01-CA41583)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Failure Treatment and Management
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Fibrosis and Remodeling
Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
Keywords: TNF-α, chronic heart failure, cardiac cachexia, serum cytokines, plasma renin activity, serum sodium, hemoglobin, blood urea nitrogen, chronic kidney disease, cytokine clearance, advanced heart failure, weight loss, inflammation in heart failure, anemia of heart failure, hyperuricemia, hyperkalemia
MeSH terms: Adult, Aged, Aged, 80 and over, Chronic Disease, Female, Heart Failure, Hemoglobins, Humans, Male, Middle Aged, Renin, Sodium, Tumor Necrosis Factor-alpha

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Elevated Circulating Levels of Tumor Necrosis Factor in Severe Chronic Heart Failure

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