Dysregulated energy expenditure in HIV-infected patients: A mechanistic review

Clinical Infectious Diseases

Volumn 44, Issue 11, 2007, Pages 1509-1517

  Chang, Evelyn ^a   Sekhar, Rajagopal ^a,b   Patel, Sanjeet ^a   Balasubramanyam, Ashok ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b BEN TAUB GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRETROVIRUS AGENT; C REACTIVE PROTEIN; CD4 ANTIGEN; CYTOKINE; FERRITIN; HAPTOCORRIN; HORMONE; INDINAVIR; INTERLEUKIN 1BETA; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; THRAZARINE; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 1; VIRUS PROTEIN;

ADIPOCYTE; BODY COMPOSITION; CD4 LYMPHOCYTE COUNT; CYTOKINE PRODUCTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG USE; DYSLIPIDEMIA; ENERGY BALANCE; ENERGY EXPENDITURE; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; LIPOATROPHY; LIPODYSTROPHY; MEDLINE; METABOLIC DISORDER; MORTALITY; PREDICTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SYSTEMATIC REVIEW; VIRUS LOAD; WASTING SYNDROME; WEIGHT REDUCTION;

ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CYTOKINES; ENERGY METABOLISM; HIV INFECTIONS; HUMANS; MITOCHONDRIA;

EID: 34249074522     PISSN: 10584838     EISSN: None     Source Type: Journal    
DOI: 10.1086/517501     Document Type: Review

References (96)

1. Mwamburi DM, Wilson IB, Jacobson DL, et al. Understanding the role of HIV load in determining weight change in the era of highly active antiretroviral therapy. Clin Infect Dis 2005; 40:167-73.
2. Melchior JC, Niyongabo T, Henzel D, Durack-Bown I, Henri SC, Boulier A. Malnutrition and wasting, immunodepression, and chronic inflammation as independent predictors of survival in HIV-infected patients. Nutrition 1999; 15:865-9.
3. Tang AM, Forrester J, Spiegelman D, Knox TA, Tchetgen E, Gorbach SL. Weight loss and survival in HIV-positive patients in the era of highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2002; 31:230-6.
4. Kotler DP, Tierney AR, Wang J, Pierson RN Jr. Magnitude of body-cell-mass depletion and the timing of death from wasting in AIDS. Am J Clin Nutr 1989; 50:444-7.
5. Wheeler DA, Gilbert CL, Launer CA, et al. Weight loss as a predictor of survival and disease progression in HIV infection. Terry Beirn Community Programs for Clinical Research on AIDS. J Acquir Immune Defic Syndr Hum Retroviral 1998; 18:80-5.
6. Palenicek JP, Graham NM, He YD, et al. Weight loss prior to clinical AIDS as a predictor of survival. Multicenter AIDS Cohort Study Investigators. J Acquir Immune Defic Syndr Hum Retroviral 1995; 10:366-73.
7. Neyra R, Chen KY, Sun M, Shyr Y, Hakim RM, Ikizler TA. Increased resting energy expenditure in patients with end-stage renal disease. JPEN J Parenter Enteral Nutr 2003; 27:36-42.
8. Rall LC, Roubenoff R. Rheumatoid cachexia: metabolic abnormalities, mechanisms, and interventions. Rheumatology (Oxford) 2004; 43:1219-23.
9. Lagman RL, Davis MP, LeGrand SB, Walsh D. Common symptoms in advanced cancer. Surg Clin N Am 2005; 85:237-55.
10. Creutzberg EC, Schols AM, Bothmer-Quaedvlieg FC, Wouters EF. Prevalence of an elevated resting energy expenditure in patients with chronic obstructive pulmonary disease in relation to body composition and lung function. Eur J Clin Nutr 1998; 52:396-401.
11. McDermott AY, Shevitz A, Must A, Harris S, Roubenoff R, Gorbach S. Nutrition treatment for HIV wasting: a prescription for food as medicine. Nutr Clin Pract 2003; 18:86-94.
12. Rabeneck L, Palmer A, Knowles JB, et al. A randomized controlled trial evaluating nutrition counseling with or without oral supplementation in malnourished HIV-infected patients. J Am Diet Assoc 1998; 98:434-8.
13. Williams SB, Bartsch G, Muurahaienen N, Collins G, Raghavan SS, Wheeler D. Protein intake is positively associated with body cell mass in weight-stable HIV-infected men. J Nutr 2003; 133:1143-6.
14. Berneis K, Battegay M, Bassetti S, et al. Nutrition supplements combined with dietary counseling diminish whole body protein catabolism in HIV-infected patients. Eur J Clin Invest 2000; 30:87-94.
15. Suttmann U, Ockenga J, Schneider H, et al. Weight gain and increased concentrations of receptor proteins for tumor necrosis factor after patients with symptomatic HIV infection received fortified nutrition support. J Am Diet Assoc 1996; 96:565-9.
16. O'Brien K, Nixon S, Glazier RH, Tynan AM. Progressive resistive exercise interventions for adults living with HIV/AIDS. Cochrane Database Syst Rev 2004:CD004248.
17. Lox CL, McAuley E, Tucker RS. Aerobic and resistance exercise training effects on body composition, muscular strength, and cardiovascular fitness in an HIV-1 population. Int J Behav Med 1996; 3:55-69.
18. Von Roenn JH, Armstrong D, Kotler DP, et al. Megestrol acetate in patients with AIDS-related cachexia. Ann Intern Med 1994; 121:393-9.
19. Beal JE, Olson R, Laubenstein L, et al. Drobabinol as a treatment for anorexia associated with weight loss in patients with AIDS. J Pain Symptom Manage 1995; 10:89-97.
20. Reyes-Teran G, Sierra-Madero JG, Martinez del Cerro V, et al. Effects of thalidomide on HIV-associated wasting syndrome: a randomized, double-blind, placebo-controlled clinical trial. AIDS 1996; 10:1501-7.
21. Haslett P, Hempstead M, Seidman C, et al. The metabolic and immunologic effects of short-term thalidomide treatment of patients infected with the human immunodeficiency virus. AIDS Res Hum Retroviruses 1997; 13:1047-54.
22. Paton NI, Newton PJ, Sharpstone DR, et al. Short-term growth hormone administration at the time of opportunisitic infections in HIVpositive patients. AIDS 1999; 13:1195-202.
23. Mulligan K, Tai VW, Schambelan M. Effects of chronic growth hormone treatment on energy intake and resting energy metabolism in patients with human immunodeficiency virus-associated wasting - a clinical research center study. J Clin Endocrinol Metab 1998; 83:1542-7.
24. Mulligan K, Grunfeld C, Hellerstein MK, Neese RA, Schambelan M. Anabolic effects of recombinant human growth hormone in paitents with wasting associated with human immunodeficiency virus infection. J Clin Endocrinol Metab 1993; 77:956-62.
25. Grinspoon S, Corcoran C, Askari H, et al. Effects of androgen administration in men with the AIDS wasting syndrome. Ann Intern Med 1998; 129:18-26.
26. Bhasin S, Storer TW, Asbel-Sethi N, et al. Effects of testosterone replacement with a nongenital, transdermal system, Androderm, in human immunodeficiency virus-infected men with low testosterone levels. J Clin Endocrinol Metab 1998; 83:3155-62.
27. Whitney EN, Rolfes SR. Understanding nutrition. 8th ed. Belmont, CA: Wadsworth Publishing Company, 1999.
28. Wang Z, Heshka S, Gallagher D, Boozer CN, Kotler DP, Heymsfield SB. Resting energy expenditure-fat-free mass relationship: new insights provided by body composition modeling. Am J Physiol Endocrinol Metab 2000; 270:539-45.
29. Ravussin E, Lillioja S, Anderson TE, Christin L, Bogardus C. Determinants of 24-hour energy expenditure in man: methods and results using a respiratory chamber. J Clin Invest 1986; 78:1568-78.
30. Illner K, Brinkmann G, Heller M, Bosy-Westphal A, Muller MJ. Metabolically active components of fat free mass and resting energy expenditure in nonobese adults. Am J Physiol Endocrinol Metab 2000; 278:E308-15.
31. Pi-Sunyer FX. Overnutrition and undernutrition as modifiers of metabolic processes in disease states. Am J Clin Nutr 2000; 72:533S-7S.
32. Leibel RL, Rosenbaum M, Hirsch J. Changes in energy expenditure resulting from altered body weight. N Engl J Med 1995; 332:621-8.
33. Nair KS, Webster J, Garrow JS. Effect of impaired tolerance and type II diabetes on resting metabolic rate and thermic response to a glucose meal in obese women. Metabolism 1986; 35:640-4.
34. Grunfeld C, Feingold KR. Metabolic disturbances and wasting in the acquired immunodeficiency syndrome. N Engl J Med 1992; 327:329-37.
35. Hommes MJ, Romijn JA, Godfried MH, et al. Increased resting energy expenditure in human immunodeficiency virus-infected men. Metabolism 1990; 39:1186-90.
36. Kotler DP, Tierney AR, Brenner SK, Couture S, Wang J, Pierson RN Jr. Preservation of short-term energy balance in clinically stable patients with AIDS. Am J Clin Nutr 1990; 51:7-13.
37. Melchior JC, Salmon D, Rigaud D, et al. Resting energy expenditure is increased in stable, malnourished HIV-infected patients. Am J Clin Nutr 1991; 53:437-41.
38. Crenn P, Rakotoanbinina B, Raynaud JJ, Thuillier F, Messing B, Melchior JC. Hyperphagia contributes to the normal body composition and protein-energy balance in HIV-infected asymptomatic men. J Nutr 2004; 134:2301-6.
39. Hommes MJ, Romijn JA, Endert E, Sauerwein HP. Resting energy expenditure and substrate oxidation in human immunodefiency virus (HIV)-infected asymptomatic men: HIV affects host metabolism in the early asymptomatic stage. Am J Clin Nutr 1991; 54:311-5.
40. Mulligan K, Tai VW, Schambelan M. Energy expenditure in human immunodeficiency virus infection. New Engl J Med 1997; 336:70-1.
41. Grunfeld C, Pang M, Shimizu L, Shigenaga JK, Jensen P, Feingold KR. Resting energy expenditure, caloric intake, and short-term weight change in human immunodeficiency virus infection and the acquired immunodeficiency syndrome. Am J Clin Nutr 1992; 55:455-60.
42. Melchior JC, Raguin G, Boulier A, et al. Resting energy expenditure in human immunodeficiency virus-infected patients: comparison between patients with and without secondary infections. Am J Clin Nutr 1993; 57:614-9.
43. Garcia-Lorda P, Serrano P, Jimenez-Exposito MJ, et al. Cytokine-driven inflammatory response is associated with the hypermetabolism of AIDS patients with opportunistic infections. JPEN J Parenter Enteral Nutr 2000; 24:317-22.
44. Schwenk A, Hoffer-Belitz E, Jung B, et al. Resting energy expenditure, weight loss, and altered body composition in HIV infection. Nutrition 1996; 12:595-601.
45. Jimenez-Exposito MJ, Garcia-Lorda P, Alonso-Villaverde C, et al. Effect of malabsorption on nutritional status and resting energy expenditure in HIV-infected patients. AIDS 1998; 12:1965-72.
46. Macallan DC. Wasting in HIV infection and AIDS. J Nutr 1999; 129(Suppl 1S):238S-42S.
47. Batterham MJ. Investigating heterogeneity in studies of resting energy expenditure in persons with HIV/AIDS: a meta-analysis. Am J Clin Nutr 2005; 81:702-13.
48. Grinspoon S, Corcoran C, Miller K, et al. Determinants of increased energy expenditure in HIV-infected women. Am J Clin Nutr 1998; 68:720-5.
49. Lane BJ, Provost-Craig MA. Resting energy expenditure in asymptomatic HIV-infected females. J Womens Health Gend Based Med 2000; 9:321-7.
50. Lovejoy JC, Champagne CM, Smith SM, de Jonge L, Xie H. Ethnic differences in dietary intakes, physical activity, and energy expenditure in middle-aged, premenopausal women: the Healthy Transitions Study. Am J Clin Nutr 2001; 74:90-5.
51. Kaplan AS, Zemel BS, Stallings VA. Differences in resting energy expenditure in prepubertal black children and white children. J Pediatr 1996; 129:643-7.
52. Sharpstone DR, Murray CP, Ross HM, et al. Energy balance in asymptomatic HIV infection. AIDS 1996; 10:1377-84.
53. Batterham MJ, Morgan-Jones J, Greenop P, Garsia R, Gold J, Caterson I. Calculating energy requirements for men with HIV/AIDS in the era of highly active antiretroviral therapy. Eur J Clin Nutr 2003; 57:209-17.
54. Sekhar RV, Jahoor F, White AC, et al. Metabolic basis of HIV-lipodystrophy syndrome. Am J Physiol Endocrinol Metab 2002; 283:E332-7.
55. Shevitz AH, Knox TA, Spiegelman D, Roubenoff R, Gorbach SL, Skolnik PR. Elevated resting energy expenditures among HIV-seropositive persons receiving highly active antiretroviral therapy. AIDS 1999; 13:1351-7.
56. Kosmiski LA, Kuritzkes DR, Sharp TA, et al. Total energy expenditure and carbohydrate oxidation are increased in the human immunodeficiency virus lipodystrophy syndrome. Metabolism 2003; 52:620-5.
57. Kosmiski LA, Kuritzkes DR, Lichenstein KA, et al. Fat distribution and metabolic changes are strongly correlated and energy expenditure is increased in the HIV lipodystrophy syndrome. AIDS 2001; 15:1993-2000.
58. Roubenoff R, Grinspoon S, Skilnik PR, et al. Role of cytokines and testosterone in regulating lean body mass and resting energy expenditure in HIV-infected men. Am J Physiol Endocrinol Metab 2002; 283:E138-45.
59. Pernerstorfer-Schoen H, Schindler K, Parschalk B, et al. Beneficial effects of protease inhibitors on body composition and energy expenditure: a comparison between HIV-infected and AIDS patients. AIDS 1999; 13:2389-96.
60. Carbonnel F, Maslo C, Beaugerie L, et al. Effects of indinavir on HIV-related wasting. AIDS 1998; 12:1777-84.
61. Renard E, Fabre J, Paris F, Reynes J, Bringer J. Syndrome of body fat redistribution in HIV-1-infected patients: relationships to Cortisol and catecholamines. Clin Endocrinol (Oxf) 1999; 51:223-30.
62. Hengel RL, Watts NB, Lennox JL. Benign symmetric lipomatosis associated with protease inhibitors. Lancet 1997; 350:1596.
63. Lo JC, Mulligan K, Tai VW, Algren H, Schambelan M. "Buffalo hump" in men with HIV-1 infection. Lancet 1998; 351:867-70.
64. Carr A, Samaras K, Thorisdottir A, Kauffman GR, Chisolm DJ, Cooper DA. Diagnosis, prediction, and natural course of HIV-1 protease-inhibitor-associated lipodystrophy, hyperlipidaemia, and diabetes mellitus: a cohort study. Lancet 1999; 353:2093-9.
65. Carr A, Samaras K, Burton S, et al. A syndrome of peripheral lipodystrophy, hyperlipidaemia and insulin resistance in patients receiving HIV protease inhibitors. AIDS 1998; 12:F51-8.
66. Bacchetti P, Gripshover B, Grunfeld C, et al. Fat distribution in men with HIV infection. Study of Fat Redistribution and Metabolic Change in HIV Infection (FRAM). J Acquir Immune Defic Syndr 2005; 40:121-31.
67. Carr A, Emery S, Law M, Puis R, Lundgren JD, Powderly WG. An objective case definition of lipodystrophy in HIV-infected adults: a case-control study. HIV Lipodystrophy Case Definition Study Group. Lancet 2003; 361:726-35.
68. Van der Valk M, Reiss P, van Leth FC, et al. Highly active antiretroviral therapy-induced lipodystrophy has minor effects on human immunodeficiency virus-induced changes in lipolysis, but normalizes resting energy expenditure. J Clin Endocrinol Metab 2002; 87:5066-71.
69. Sutinen J, Yki-Jarvinen H. Increased resting energy expenditure, fat oxidation and food intake in patients with highly active antiretroviral therapy-associated lipodystrophy Am J Physiol Endocrinol Metab 2006; 292:E687-92.
70. Tisdale MJ. Cancer cachexia: metabolic alterations and clinical manifestations. Nutrition 1997; 13:1-7.
71. Godfried MH, Romijn JA, van der Poll T, et al. Soluble receptors for tumor necrosis factor are markers for clinical course but not for major metabolic changes in human immunodeficiency virus infection. Metabolism 1995; 44:1564-9.
72. Hadigan C, Borgonha S, Rabe J, Young V, Grinspoon S. Increased rates of lipolysis among human immunodeficiency virus-infected men receiving highly active antiretroviral therapy. Metabolism 2002; 51:1143-7.
73. Reeds DN, Mittendorfer B, Patterson BW, Powderly WG, Yarasheski KE, Klein S. Alterations in lipid kinetics in men with HIV-dyslipidemia. Am J Physiol Endocrinol Metab 2003; 285:E490-7.
74. Oral EA, Simha V, Ruiz E, et al. Leptin-replacement therapy for lipodystrophy. N Engl J Med 2002; 346:570-8.
75. Reitman ML, Arioglu E, Gavrilova O, Taylor SI. Lipodystrophy revisited. Trends Endocrinol Metab 2000; 11:410-6.
76. Klein S, Jahoor F, Wolfe RR, Stuart CA. Generalized lipodystrophy: in vivo evidence for hypermetabolism and insulin-resistant lipid, glucose, and amino acid kinetics. Metabolism 1992; 41:893-6.
77. Cutler DL, Kaufmann S, Freidenberg GR. Insulin-resistant diabetes mellitus and hypermetabolism in mandibuloacral dysplasia: a newly recognized form of partial lipodystrophy. J Clin Endocrinol Metab 1991; 73:1056-61.
78. Marshall MK, Doerrler W, Feingold KR, Grunfeld C. Leukemia inhibitory factor induces changes in lipid metabolism in cultured adipocytes. Endocrinology 1994; 135:141-7.
79. Deniaud A, Brenner C, Kroemer G. Mitochondrial membrane permeabilization by HIV-1 Vpr. Mitochondrion 2004; 4:223-33.
80. Cote HC, Brumme ZL, Craib KJ, et al. Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients. N Engl J Med 2002; 346:811-20.
81. Pace CS, Martin AM, Hammond EL, Mamotte CD, Nolan DA, Mallal SA. Mitochondrial proliferation, DNA depletion and adipocyte differentiation in subcutaneous adipose tissue of HIV-positive HAART recipients. Antivir Ther 2003; 8:323-31.
82. Setzer B, Schlesier M, Walker UA. Effects of diadnosine-related depletion of mtDNA in human T lymphocytes. J Infect Dis 2005; 191:848-55.
83. Walker UA, Bickel M, Lutke Volksbeck SI, et al. Evidence of nucleoside analogue reverse-transcriptase inhibitor-associated genetic and structural defects of mitochondria in adipose tissue of HIV-infected patients. J Acquir Immune Defic Syndr 2002; 29:117-21.
84. Walker UA, Brinkman K. An argument for mitochondrial toxicity in highly active antiretroviral therapy-induced lipoatrophy. AIDS 2001; 15:1450-2.
85. Zaera MG, Miro O, Pedrol E, et al. Mitochondrial involvement in antiretroviral therapy-related lipodystrophy. AIDS 2001; 15:1643-51.
86. Miro O, Lopez S, Martinez E, et al. Mitochondrial effects of HIV infection on the peripheral blood mononuclear cells of HIV-infected patients who were never treated with antiretrovirals. Clin Infect Dis 2004; 39:710-6.
87. McComsey GA, Paulsen DM, Lonergan JT, et al. Improvements in lipoatrophy, mitochondrial DNA levels and fat apoptosis after replacing stavudine with abacavir or zidovudine. AIDS 2005; 19:15-23.
88. Shikuma CM, Hu N, Milne C, et al. Mitochondrial DNA decrease in subcutaneous adipose tissue of HIV-infected individuals with peripheral lipoatrophy. AIDS 2001; 15:1801-9.
89. Lloreta J, Domingo P, Pujol RM, et al. Ultrastructural features of highly active antiretroviral therapy-associated partial lipodystrophy. Virchows Arch 2002; 441:599-604.
90. Newsholme EA. Substrate cycles: their metabolic, energetic and thermic consequences in man. Biochem Soc Symp 1978; 43:183-205.
91. Sekhar RV, Jahoor F, Pownall HJ, et al. Severely dysregulated disposal of postprandial triacylglycerols exacerbates hypertriacylglycerolemia in HIV lipodystrophy syndrome. Am J Clin Nutr 2005; 81:1405-10.
92. Macallan DC, Noble C, Baldwin C, et al. Energy expenditure and wasting in human immunodeficiency virus infection. New Engl J Med 1995; 333:83-8.
93. Sheehan LA, Macallan DC. Determinants of energy intake and energy expenditure in HIV and AIDS. Nutrition 2000; 16:101-6.
94. Poizot-Martin I, Benourine K, Philibert P, et al. Diet-induced thermogenesis in HIV infection. AIDS 1994; 8:501-4.
95. Heijligenberg R, Romijn JA, Westerterp KR, Jonkers CF, Prins JM, Sauerwein HP. Total energy expenditure in human immunodeficiency virus-infected men and healthy controls. Metabolism 1997; 46:1324-6.
96. Coors M, Suttmann U, Trimborn P, Ockenga J, Muller MJ, Selberg O. Acute phase response and energy balance in stable human immunodeficiency virus-infected patients: a doubly labeled water study. J Lab Clin Med 2001; 138:94-100.