Effects of HIV Infection on Gastrointestinal Function

  • Leon L. Lai
  • Tamsin A. Knox
  • Sherwood L. Gorbach


There is a close and complex relationship between the human immunodeficiency virus (HIV) and gastrointestinal function. This relationship begins with initial infection by the virus, which may be mediated through the gastrointestinal mucosa, and continues throughout disease progression. It has become clear that evolution of viral disease can lead to deteriorating gastrointestinal function. In turn, gastrointestinal dysfunction leads to nutrient malabsorption and deficiencies, which can accelerate the progression of the viral disease.


Human Immunodeficiency Virus Human Immunodeficiency Virus Type Human Immunodeficiency Virus Infection Lean Body Mass Chronic Diarrhea 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Colebunders R, Francis H, Mann JM, Bila KM, Izaley L, Kimputu L, et al (1987) Persistent diarrhea, strongly associated with HIV infection in Kinshasa, Zaire. Am J Gastroenterol 1987 82:859–864Google Scholar
  2. 2.
    Dworkin B, Wormser GP, Rosenthal WS, Heier SK, Braunstein M, Weiss L, et al (1985) Gastrointestinal manifestations of the acquired immunodeficiency syndrome: a review of 22 cases. Am J Gastroenterol 80:774–778PubMedGoogle Scholar
  3. 3.
    Simon D, Brandt LJ (1993) Diarrhea in patients with the acquired immunodeficiency syndrome. Gastroenterology 105:1238–1242PubMedGoogle Scholar
  4. 4.
    Lubeck DP, Bennett CL, Mazonson PD, Fifer SK, Fries JF (1993) Quality of life and health service use among HIV-infected patients with chronic diarrhea. J Acquir Immune Defic Syndr 6:478–484PubMedCrossRefGoogle Scholar
  5. 5.
    Watson A, Samore MH, Wanke CA (1996) Diarrhea and quality of life in ambulatory HIV-infected patients. Dig Dis Sci 41:1794–1800PubMedCrossRefGoogle Scholar
  6. 6.
    Wachtel T, Piette J, Stein M, Fleishman J, Carpenter C (1992) Quality of life in persons with human immunodeficiency virus infection: measurement by the Medical Outcomes Study instrument. Ann Intern Med 116:129–137PubMedGoogle Scholar
  7. 7.
    Knox TA, Spiegelman D, Skinner SC, Gorbach S (2000) Diarrhea and abnormalities of gastrointestinal function in a cohort of men and women with HIV infection. Am J Gastroenterol 95:3482–3489PubMedCrossRefGoogle Scholar
  8. 8.
    Chlebowski RT, Grosvenor MB, Bernhard NH, Morales LS, Bulcavage LM (1989) Nutritional status, gastrointestinal dysfunction, and survival in patients with AIDS. Am J Gastroenterol 84:1288–1293PubMedGoogle Scholar
  9. 9.
    Call SA, Heudebert G, Saag M, Wilcox CM (2000) The changing etiology of chronic diarrhea in HIV-infected patients with CD4 cell counts less than 200 cells/mm3. Am J Gastroenterol 95:3142–3146PubMedCrossRefGoogle Scholar
  10. 10.
    Fantini J, Yahi N, Baghdiguian S, Chermann JC (1992) Human colon epithelial cells productively infected with human immunodeficiency virus show impaired differentiation and altered secretion. J Virol 66:580–585PubMedGoogle Scholar
  11. 11.
    Asmuth DM, Hammer SM, Wanke CA (1994) Physiological effects of HIV infection on human intestinal epithelial cells: an in vitro model for HIV enteropathy. AIDS 8:205–211PubMedCrossRefGoogle Scholar
  12. 12.
    Lutz NW, Yahi N, Fantini J, Cozzone PJ (1997) Perturbations of glucose metabolism associated with HIV infection in human intestinal epithelial cells: a multi-nuclear magnetic resonance spectroscopy study. AIDS 11:147–155PubMedCrossRefGoogle Scholar
  13. 13.
    Meng G, Wei X, Wu X, Sellers MT, Decker JM, Mol-doveanu Z, et al (2002) Primary intestinal epithelial cells selectively transfer R5 HIV-1 to CCR5+ cells. Nat Med 8:150–156PubMedCrossRefGoogle Scholar
  14. 14.
    Meng G, Sellers MT, Mosteller-Barnum M, Rogers TS, Shaw GM, Smith PD (2000) Lamina propria lymphocytes, not macrophages, express CCR5 and CXCR4 and are the likely target cell for human immunodeficiency virus type 1 in the intestinal mucosa. J Infect Dis 182:785–791PubMedCrossRefGoogle Scholar
  15. 15.
    Delezay O, Yahi N, Tamalet C, Baghdiguian S, Boudier JA, Fantini J (1997) Direct effect of type 1 human immunodeficiency virus (HIV-1) on intestinal epithelial cell differentiation: relationship to HIV-1 enteropathy. Virology 238:231–242PubMedCrossRefGoogle Scholar
  16. 16.
    Dayanithi G, Yahi N, Baghdiguian S, Fantini J (1995) Intracellular calcium release induced by human immunodeficiency virus type 1 (HIV-1) surface envelope glycoprotein in human intestinal epithelial cells: a putative mechanism for HIV-1 enteropathy. Cell Calcium 18:9–18PubMedCrossRefGoogle Scholar
  17. 17.
    Lu SS (1997) Pathophysiology of HIV-associated diarrhea. Gastroenterol Clin North Am 26:175–189PubMedCrossRefGoogle Scholar
  18. 18.
    Smith PD, Quinn TC, Strober W, Janoff EN, Masur H (1992) NIH conference. Gastrointestinal infections in AIDS [see comments]. Ann Intern Med 116:63–77PubMedGoogle Scholar
  19. 19.
    Schieferdecker HL, Ullrich R, Hirseland H, Zeitz M (1992) T cell differentiation antigens on lymphocytes in the human intestinal lamina propria. J Immunol 149:2816–2822PubMedGoogle Scholar
  20. 20.
    Muro-Cacho CA, Pantaleo G, Fauci AS (1995) Analysis of apoptosis in lymph nodes of HIV-infected persons. Intensity of apoptosis correlates with the general state of activation of the lymphoid tissue and not with stage of disease or viral burden. J Immunol 154:5555–5566PubMedGoogle Scholar
  21. 21.
    Lee SH, Starkey PM, Gordon S (1985) Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J Exp Med 161:475–489PubMedCrossRefGoogle Scholar
  22. 22.
    Herbein G, Mahlknecht U, Batliwalla F, Gregersen P, Pappas T, Butler J, et al (1998) Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 395:189–194PubMedCrossRefGoogle Scholar
  23. 23.
    Talal AH, Irwin CE, Dieterich DT, Yee H, Zhang L (2001) Effect of HIV-1 infection on lymphocyte proliferation in gut-associated lymphoid tissue. J Acquir Immune Defic Syndr 26:208–217PubMedCrossRefGoogle Scholar
  24. 24.
    Zeitz M, Ullrich R, Schneider T, Kewenig S, Hohloch K, Riecken EO (1998) HIV/SIV enteropathy. Ann NY Acad Sci 859:139–148PubMedCrossRefGoogle Scholar
  25. 25.
    Budhraja M, Levendoglu H, Kocka F, Mangkornkanok M, Sherer R (1987) Duodenal mucosal T cell subpopulation and bacterial cultures in acquired immune deficiency syndrome. Am J Gastroenterol 82:427–431PubMedGoogle Scholar
  26. 26.
    Ellakany S, Whiteside TL, Schade RR, van Thiel DH (1987) Analysis of intestinal lymphocyte subpopulations in patients with acquired immunodeficiency syndrome (AIDS) and AIDS-related complex. Am J Clin Pathol 87:356–364PubMedGoogle Scholar
  27. 27.
    Rodgers VD, Fassett R, Kagnoff MF (1986) Abnormalities in intestinal mucosal T cells in homosexual populations including those with the lymphadeno-pathy syndrome and acquired immunodeficiency syndrome. Gastroenterology 90:552–558PubMedGoogle Scholar
  28. 28.
    Veazey RS, Tham 1C, Mansfield KG, DeMaria M, Forand AE, Shvetz DE, et al (2000) Identifying the target cell in primary simian immunodeficiency virus (SIV) infection: highly activated memory CD4(+) T cells are rapidly eliminated in early SIV infection in vivo. J Virol 74:57–64PubMedCrossRefGoogle Scholar
  29. 29.
    Schneider T, Jahn HU, Schmidt W, Riecken EO, Zeitz M, Ullrich R (1995) Loss of CD4 T lymphocytes in patients infected with human immunodeficiency virus type 1 is more pronounced in the duodenal mucosa than in the peripheral blood. Berlin Diarrhea/Wasting Syndrome Study Group. Gut 37:524–529PubMedCrossRefGoogle Scholar
  30. 30.
    Schneider T, Ullrich R, Jahn HU, Bergs C, Schmidt W, Dormann A, et al (1995) Loss of activated CD4-positive T cells and increase in activated cytotoxic CD8-positive T cells in the duodenum of patients infected with human immunodeficiency virus. Berlin Diarrhea/Wasting Syndrome Study Group. Adv Exp Med Biol 371B:1019–1021PubMedGoogle Scholar
  31. 31.
    Clayton F, Snow G, Reka S, Kotler DP (1997) Selective depletion of rectal lamina propria rather than lymphoid aggregate CD4 lymphocytes in HIV infection. Clin Exp Immunol 107:288–292PubMedCrossRefGoogle Scholar
  32. 32.
    Smith PD, Meng G, Shaw GM, Li L (1987) Infection of gastrointestinal tract macrophages by HIV-1. J Leukoc Biol 62:72–77Google Scholar
  33. 33.
    Fox CH, Kotier D, Tierney A, Wilson CS, Fauci AS (1989) Detection of HIV-i RNA in the lamina propria of patients with AIDS and gastrointestinal disease. J Infect Dis 159:467–471PubMedCrossRefGoogle Scholar
  34. 34.
    Kotier DP, Shimada T, Snow G, Winson G, Chen W, Zhao M, et al (1998) Effect of combination antiretroviral therapy upon rectal mucosal HIV RNA burden and mononuclear cell apoptosis. AIDS 12:597–604CrossRefGoogle Scholar
  35. 35.
    Talal AH, Monard S, Vesanen M, Zheng Z, Hurley A, Cao Y, et al (2001) Virologic and immunologic effect of antiretroviral therapy on HIV-1 in gut-associated lymphoid tissue. J Acquir Immune Defic Syndr 26:1–7PubMedGoogle Scholar
  36. 36.
    Poles MA, Elliott J, Vingerhoets J, Michiels L, Scholliers A, Bloor S, et al (2001) Despite high concordance, distinct mutational and phenotypic drug resistance profiles in human immunodeficiency virus type 1 RNA are observed in gastrointestinal mucosal biopsy specimens and peripheral blood mononuclear cells compared with plasma. J Infect Dis 183:143–148PubMedCrossRefGoogle Scholar
  37. 37.
    Sharpstone D, Neild P, Crane R, Taylor C, Hodgson C, Sherwood R, et al (1999) Small intestinal transit, absorption, and permeability in patients with AIDS with and without diarrhoea. Gut 45:70–76PubMedCrossRefGoogle Scholar
  38. 38.
    Patton JS, Peters PM, McCabe J, Crase D, Hansen S, Chen AB, et al (1987) Development of partial tolerance to the gastrointestinal effects of high doses of recombinant tumor necrosis factor-alpha in rodents. J Clin Invest 80:1587–1596PubMedCrossRefGoogle Scholar
  39. 39.
    Fantino M, Wieteska L (1993) Evidence for a direct central anorectic effect of tumor-necrosis-factor-alpha in the rat. Physiol Behav 53:477–483PubMedCrossRefGoogle Scholar
  40. 40.
    Lake-Bakaar G, Elsakr M, Hagag N, Lyubsky S, Ahuja J, Craddock B, et al (1996) Changes in parietal cell structure and function in HIV disease. Dig Dis Sci 41:1398–1408PubMedCrossRefGoogle Scholar
  41. 41.
    Stein TP, Koerner B, Schluter MD, Leskiw MJ, Gaprin-dachvilli T, Richards EW, et al (1997) Weight loss, the gut and the inflammatory response in aids patients. Cytokine 9:143–147PubMedCrossRefGoogle Scholar
  42. 42.
    Rene E, Marche C, Regnier B, Saimot AG, Vilde JL, Perrone C, et al (1989) Intestinal infections in patients with acquired immunodeficiency syndrome. A prospective study in 132 patients. Dig Dis Sci 34:773–780PubMedCrossRefGoogle Scholar
  43. 43.
    Desportes I, Le Charpentier Y, Galian A, Bernard F, Cochand-Priollet B, Lavergne A, et al (1985) Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. J Protozool 32:250–254PubMedGoogle Scholar
  44. 44.
    DeHovitz JA, Pape JW, Boncy M, Johnson WD Jr (1986) Clinical manifestations and therapy of Isospora belli infection in patients with the acquired immunodeficiency syndrome. N Engl J Med 315:87–90PubMedCrossRefGoogle Scholar
  45. 45.
    Kotier DP, Gaetz HP, Lange M, Klein EB, Holt PR (1984) Enteropathy associated with the acquired immunodeficiency syndrome. Ann Intern Med 101:421–428Google Scholar
  46. 46.
    Kotler DP, Weaver SC, Terzakis JA (1986) Ultrastruc-tural features of epithelial cell degeneration in rectal crypts of patients with AIDS. Am J Surg Pathol 10:531–538PubMedCrossRefGoogle Scholar
  47. 47.
    Oktedalen O, Skar V, Dahl E, Serck-Hanssen A (1998) Changes in small intestinal structure and function in HIV-infected patients with chronic diarrhoea. Scand J Infect Dis 459–463Google Scholar
  48. 48.
    Smith PD, Meng G, Sellers MT, Rogers TS, Shaw GM (2000) Biological parameters of HIV-i infection in primary intestinal lymphocytes and macrophages. J Leukoc Biol 68:360–365PubMedGoogle Scholar
  49. 49.
    Agace WW, Amara A, Roberts AI, Pablos JL, Thelen S, Uguccioni M, et al (2000) Constitutive expression of stromal derived factor-1 by mucosal epithelia and its role in HIV transmission and propagation. Curr Biol 10:325–328PubMedCrossRefGoogle Scholar
  50. 50.
    Olsson J, Poles M, Spetz AL, Elliott J, Hultin L, Giorgi J, et al (2000) Human immunodeficiency virus type 1 infection is associated with significant mucosal inflammation characterized by increased expression of CCR5, CXCR4, and beta-chemokines. J Infect Dis 182:1625–1635PubMedCrossRefGoogle Scholar
  51. 51.
    Stockmann M, Schmitz H, Fromm M, Schmidt W, Pauli G, Scholz P, et al (2000) Mechanisms of epithelial barrier impairment in HIV infection. Ann NY Acad Sci 915:293–303PubMedCrossRefGoogle Scholar
  52. 52.
    Snijders F, van Deventer SJ, Bartelsman JF, den Otter P, Jansen J, Mevissen ML, et al (1995) Diarrhoea in HIV-infected patients: no evidence of cytokine-mediated inflammation in jejunal mucosa. AIDS 9:367–373PubMedGoogle Scholar
  53. 53.
    Reka S, Garro ML, Kotler DP (1994) Variation in the expression of human immunodeficiency virus RNA and cytokine mRNA in rectal mucosa during the progression of infection. Lymphokine Cytokine Res 13:391–398PubMedGoogle Scholar
  54. 54.
    McGowan I, Radford-Smith G, Jewell DP (1994) Cytokine gene expression in HIV-infected intestinal mucosa. AIDS 8:1569–1575PubMedCrossRefGoogle Scholar
  55. 55.
    Vyakarnam A, Matear P, Meager A, Kelly G, Stanley B, Weiler I, et al (1991) Altered production of tumour necrosis factors alpha and beta and interferon gamma by HIV-infected individuals. Clin Exp Immunol 84:109–115PubMedCrossRefGoogle Scholar
  56. 56.
    Stockmann M, Schmitz H, Fromm M, Schmidt W, Rokos K, Pauli G, et al (1998) The mechanism of diarrhea in HIV is based on an impaired epithelial barrier function that could be induced by a specific cytokine pattern. Ann NY Acad Sci 859:267–270PubMedCrossRefGoogle Scholar
  57. 57.
    Madara JL, Stafford J (1989) Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J Clin Invest 83:724–727PubMedCrossRefGoogle Scholar
  58. 58.
    Agostoni C, Riva E, Esposito S, Ferraris G, Principi N, Zuccotti GV (2000) Fatty acid composition of plasma lipids in HIV-infected children. Comparison with seroreverters. Acta Paediatrica 89:172–176PubMedCrossRefGoogle Scholar
  59. 59.
    Kotier DP, Reka S, Clayton F (1993) Intestinal mucosal inflammation associated with human immunodeficiency virus infection. Dig Dis Sci 38:1119–1127CrossRefGoogle Scholar
  60. 60.
    Babameto G, Kotler DP (1997) Malnutrition in HIV infection. Gastroenterol Clin North Am 26:393–415PubMedCrossRefGoogle Scholar
  61. 61.
    Wilcox CM, Rabeneck L, Friedman S (1996) AGA technical review: malnutrition and cachexia, chronic diarrhea, and hepatobiliary disease in patients with human immunodeficiency virus infection. Gastroenterology 111:1724–1752PubMedCrossRefGoogle Scholar
  62. 62.
    Kotier DP, Francisco A, Clayton F, Scholes JV, Orenstein JM (1990) Small intestinal injury and parasitic diseases in AIDS [see comments]. Ann Intern Med 113:444–449Google Scholar
  63. 63.
    Keating J, Bjarnason I, Somasundaram S, Macpherson A, Francis N, Price AB, et al (1995) Intestinal absorptive capacity, intestinal permeability and jejunal histology in HIV and their relation to diarrhoea. Gut 37:623–629PubMedCrossRefGoogle Scholar
  64. 64.
    Greenson JK, Belitsos PC, Yardley JH, Bartlett JG (1991) AIDS enteropathy: occult enteric infections and duodenal mucosal alterations in chronic diarrhea [see comments]. Ann Intern Med 114:366–372PubMedGoogle Scholar
  65. 65.
    Ullrich R, Zeitz M, Heise W, L’age M, Hoffken G, Riecken EO (1989) Small intestinal structure and function in patients infected with human immunodeficiency virus (HIV): evidence for HIV-induced enteropathy [erratum appears in Ann Intern Med 111:954]. Ann Intern Med 111:15–21PubMedGoogle Scholar
  66. 66.
    Cummins AG, Labrooy JT, Stanley DP, Rowland R, Shearman DJ (1990) Quantitative histological study of enteropathy associated with HIV infection. Gut 31:317–321PubMedCrossRefGoogle Scholar
  67. 67.
    Belitsos PC, Greenson JK, Yardley JH, Sisler JR, Bartlett JG (1992) Association of gastric hypoacidity with opportunistic enteric infections in patients with AIDS. J Infect Dis 166:277–284PubMedCrossRefGoogle Scholar
  68. 68.
    Sharkey KA, Sutherland LR, Davison JS, Zwiers H, Gill MJ, Church DL (1992) Peptides in the gastrointestinal tract in human immunodeficiency virus infection. The GI/HIV Study Group of the University of Calgary. Gastroenterology 103:18–28PubMedGoogle Scholar
  69. 69.
    Heise C, Dandekar S, Kumar P, Duplantier R, Donovan RM, Halsted CH (1991)Human immunodeficiency virus infection of enterocytes and mononuclear cells in human jejunal mucosa. Gastroenterology 100:1521–1527PubMedGoogle Scholar
  70. 70.
    Rabeneck L, Genta RM, Risser JM, Bailey ME, Clar-ridge JE, Gyorkey F (1996) Uncertain clinical significance of duodenal mucosal abnormalities in HIV-infected individuals. Results of a case-control study. J Clin Gastroenterol 23:11–14PubMedCrossRefGoogle Scholar
  71. 71.
    Tepper RE, Simon D, Brandt LJ, Nutovits R, Lee MJ (1994) Intestinal permeability in patients infected with the human immunodeficiency virus. Am J Gastroenterology 89:878–882Google Scholar
  72. 72.
    Kotier DP, Reka S, Chow K, Orenstein JM (1993) Effects of enteric parasitoses and HIV infection upon small intestinal structure and function in patients with AIDS. J Clin Gastroenterol 16:10–15CrossRefGoogle Scholar
  73. 73.
    Taylor C, Hodgson K, Sharpstone D, Sigthorsson G, Coutts M, Sherwood R, et al (2000) The prevalence and severity of intestinal disaccharidase deficiency in human immunodeficiency virus-infected subjects. Scand J Gastroenterol 2000 35:599–606CrossRefGoogle Scholar
  74. 74.
    Bjarnason I, Sharpstone DR, Francis N, Marker A, Taylor C, Barrett M, et al (1996) Intestinal inflammation, ileal structure and function in HIV. AIDS 10:1385–1391PubMedCrossRefGoogle Scholar
  75. 75.
    Lambl BB, Federman M, Pleskow D, Wanke CA (1996) Malabsorption and wasting in AIDS patients with microsporidia and pathogen-negative diarrhea. AIDS 10:739–744PubMedCrossRefGoogle Scholar
  76. 76.
    Ehrenpreis ED, Ganger DR, Kochvar GT, Patterson BK, Craig RM (1992) D-xylose malabsorption: characteristic finding in patients with the AIDS wasting syndrome and chronic diarrhea. J Acquir Immune Defic Syndr 5:1047–1050PubMedGoogle Scholar
  77. 77.
    Ehrenpreis ED, Patterson BK, Brainer JA, Yokoo H, Rademaker AW, Glogowski W, et al (1992) Histopathologic findings of duodenal biopsy specimens in HIV-infected patients with and without diarrhea and malabsorption [see comments]. Am J Clin Pathol 97:21–28PubMedGoogle Scholar
  78. 78.
    Lim SG, Menzies IS, Lee CA, Johnson MA, Pounder RE (1993) Intestinal permeability and function in patients infected with human immunodeficiency virus. A comparison with coeliac disease. Scand J Gastroenterol 28:573–580PubMedCrossRefGoogle Scholar
  79. 79.
    Ott M, Wegner A, Caspary WF, Lembcke B (1993) Intestinal absorption and malnutrition in patients with the acquired immunodeficiency syndrome (AIDS). Zeitschrift fur Gastroenterologie 31:661–665PubMedGoogle Scholar
  80. 80.
    Ehrenpreis ED, Gulino SP, Patterson BK, Craig RM, Yokoo H, Atkinson AJ Jr (1991) Kinetics of D-xylose absorption in patients with human immunodeficiency virus enteropathy. Clin Pharmacol Ther 49:632–640PubMedCrossRefGoogle Scholar
  81. 81.
    Ullrich R, Riecken EO, Zeitz M (1991) Human immunodeficiency virus-induced enteropathy. Immunol Res 10:456–464PubMedCrossRefGoogle Scholar
  82. 82.
    Ullrich R, Heise W, Bergs C, L’age M, Riecken EO, Zeitz M (1992) Effects of zidovudine treatment on the small intestinal mucosa in patients infected with the human immunodeficiency virus. Gastroenterology 102:1483–1492PubMedGoogle Scholar
  83. 83.
    Ehrenpreis ED, Carlson SJ, Boorstein HL, Craig RM (1994) Malabsorption and deficiency of vitamin B12 in HIV-infected patients with chronic diarrhea. Dig Dis Sci 39:2159–2162PubMedCrossRefGoogle Scholar
  84. 84.
    Baum MK, Beam R, Mantero-Atienza E (1991) Predic-tors of change in immune function: longitudinal analysis of nutritional and immune status in early HIV infection [abstract]. International Conference On AIDS 7:329Google Scholar
  85. 85.
    Livrozet JM, Bourgeay-Causse M, Fayol V (1992) Vitamin status (folinic acid and vitamin B12) at the first blood test analysis in 140 HIV seropositive patients [abstract]. International Conference On AIDS 8:102Google Scholar
  86. 86.
    Bieber S, Fremont S, May T (1994) Vitamin B12 and folate in AIDS [abstract]. International Conference On AIDS 10:223Google Scholar
  87. 87.
    Harriman GR, Smith PD, Home MK, Fox CH, Koenig S, Lack EE, et al (1989) Vitamin B12 malabsorption in patients with acquired immunodeficiency syndrome. Arch Intern Med 149:2039–2041PubMedCrossRefGoogle Scholar
  88. 88.
    Sciarretta G, Bonazzi L, Monti M, Furno A, Mazzoni M, Mazzetti M, et al (1994) Bile acid malabsorption in AIDS-associated chronic diarrhea: a prospective 1-year study. Am J Gastroenterol 89:379–381PubMedGoogle Scholar
  89. 89.
    Poles MA, Fuerst M, McGowan I, Elliott J, Rezaei A, Mark D, et al (2001) HIV-related diarrhea is multifactorial and fat malabsorption is commonly present, independent of HAART. Am J Gastroenterol 96:1831–1837PubMedCrossRefGoogle Scholar
  90. 90.
    Koch J, Garcia-Shelton YL, Neal EA, Chan MF, Weaver KE, Cello JP (1996) Steatorrhea: a common manifestation in patients with HIV/AIDS. Nutrition 12:507–510PubMedCrossRefGoogle Scholar
  91. 91.
    Laine L, Garcia F, McGilligan K, Malinko A, Sinatra FR, Thomas DW (1993) Protein-losing enteropathy and hypoalbuminemia in AIDS. AIDS 7:837–8CrossRefGoogle Scholar
  92. 92.
    Batman PA, Miller AR, Sedgwick PM, Griffin GE (1991) Autonomic denervation in jejunal mucosa of homosexual men infected with HIV. AIDS 5:1247–1252PubMedCrossRefGoogle Scholar
  93. 93.
    Kartalija M, Sande MA (1999) Diarrhea and AIDS in the era of highly active antiretroviral therapy. Clin Infect Dis 28:701–705PubMedCrossRefGoogle Scholar
  94. 94.
    Shor-Posner G, Baum MK (1999) Nutritional alterations in HIV-1 seropositive and seronegative drug users [letter; comment]. Nutrition 12:555–556CrossRefGoogle Scholar
  95. 95.
    1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR Recomm Rep 1992 41:1–19Google Scholar
  96. 96.
    Tang AM, Forrester JE, Spiegelman D, Knox TA, Tchetgen E, Gorbach SL (2002) Weight loss and survival in HIV-positive patients in the era of highly active antiretroviral therapy (HAART). Acquir Immune Defic Syndr 31:230–236CrossRefGoogle Scholar
  97. 97.
    Gilbert C, Launer C, Bartsch G, et al (1995) Body weight and percent weight change as predictors of mortality in AIDS [abstract]. Proceedings of the 35th ICAACGoogle Scholar
  98. 98.
    Moore RD, Chaisson RE (1999) Natural history of HIV infection in the era of combination antiretroviral therapy. AIDS 13:1933–1942PubMedCrossRefGoogle Scholar
  99. 99.
    Wanke CA, Silva M, Knox TA, Forrester J, Speigelman D, Gorbach SL (2000) Weight loss and wasting remain common complications in individuals infected with human immunodeficiency virus in the era of highly active antiretroviral therapy. Clin Infect Dis 31:803–805PubMedCrossRefGoogle Scholar
  100. 100.
    Baum MK, Shor-Posner G, Zhang G, Lai H, Quesada JA, Campa A, et al (1997) HIV-i infection in women is associated with severe nutritional deficiencies. J Acquir Immune Defic Syndr 16:272–278CrossRefGoogle Scholar
  101. 101.
    Nahlen BL, Chu SY, Nwanyanwu OC, Berkelman RL, Martinez SA, Rullan JV (1993) HIV wasting syndrome in the United States. AIDS 7:183–188PubMedCrossRefGoogle Scholar
  102. 102.
    Schwenk A, Hoffer-Belitz E, Jung B, Kremer G, Burger B, Salzberger B, et al (1996) Resting energy expenditure, weight loss, and altered body composition in HIV infection. Nutrition 12:595–601PubMedCrossRefGoogle Scholar
  103. 103.
    Beaugerie L, Carbonnel F, Carrat F, Rached AA, Maslo C, Gendre JP, et al (1998) Factors of weight loss in patients with HIV and chronic diarrhea [see comments]. J Acquir Immune Defic Syndr 19:34–39CrossRefGoogle Scholar
  104. 104.
    Graham NM, Rubb S, Hoover DR, McCall LD, Paleni-cek JG, Saah AJ (1994) Beta 2-microglobulin and other early predictors of human immunodeficiency virus type 1-related wasting. Ann Epidemiol 4:32–39PubMedCrossRefGoogle Scholar
  105. 105.
    Zangerle R, Reibnegger G, Wachter H, Fuchs D (1993) Weight loss in HIV-1 infection is associated with immune activation. AIDS 7:175–181PubMedCrossRefGoogle Scholar
  106. 106.
    Grunfeld C, Pang M, Shimizu L, Shigenaga JK, Jensen P, Feingold KR (1992) Resting energy expenditure, caloric intake, and short-term weight change in human immunodeficiency virus infection and the acquired immunodeficiency syndrome. Am J Clin Nutr 55:455–460PubMedGoogle Scholar
  107. 107.
    Jones PD, Shelley L, Wakefield D (1992) Tumor necrosis factor-alpha in advanced HIV infection in the absence of AIDS-related secondary infections. J Acquir Immune Defic Syndr 5:1266–1271PubMedCrossRefGoogle Scholar
  108. 108.
    Ayehunie S, Sonnerborg A, Yemane-Berhan T, Zew-die DW, Britton S, Strannegard O (1993) Raised levels of tumour necrosis factor-alpha and neopterin, but not interferon-alpha, in serum of HIV-1-infected patients from Ethiopia. Clin Exp Immunol 91:37–42PubMedCrossRefGoogle Scholar
  109. 109.
    Reddy MM, Sorrell SJ, Lange M, Grieco MH (1988) Tumor necrosis factor and HIV P24 antigen levels in serum of HIV-infected populations. J Acquir Immune Defic Syndr 1:436–440PubMedGoogle Scholar
  110. 110.
    Aukrust P, Liabakk NB, Muller F, Lien E, Espevik T, Froland SS (1994) Serum levels of tumor necrosis factor-alpha (TNF alpha) and soluble TNF receptors in human immunodeficiency virus type 1 infection-correlations to clinical, immunologic, and virologic parameters. J Infect Dis 169:420–424PubMedCrossRefGoogle Scholar
  111. 111.
    Suttmann U, Selberg 0, Gallati H, Ockenga J, Deicher H, Muller MJ (1994) Tumour necrosis factor receptor levels are linked to the acute-phase response and malnutrition in human-immunodeficiency-virus-infected patients. Clin Sci (Lond) 86:461–467Google Scholar
  112. 112.
    Grunfeld C, Kotier DP, Shigenaga JK, Doerrler W, Tierney A, Wang J, et al (1991) Circulating interferon-alpha levels and hypertriglyceridemia in the acquired immunodeficiency syndrome. Am J Med 90:154–162PubMedGoogle Scholar
  113. 113.
    Coodley GO, Loveless MO, Nelson HD, Coodley MK (1994) Endocrine function in the HIV wasting syndrome. J Acquir Immune Defic Syndr 7:46–51PubMedGoogle Scholar
  114. 114.
    Roubenoff R, Grinspoon S, Skolnik P, Tchetgen E, Abad L, Spiegelman D, et al (2002) Role of cytokines and testosterone in regulating lean body mass and resting energy expenditure in HIV-infected men. Am J Physiol Endocrinol Metab 283:E138–E145PubMedGoogle Scholar
  115. 115.
    Wilson IB, Roubenoff R, Knox TA, Spiegelman D, Gorbach SL (2000) Relation of lean body mass to health-related quality of life in persons with HIV. J Acquir Immune Defic Syndr 24:137–146PubMedGoogle Scholar
  116. 116.
    Forrester JE, Spiegelman D, Woods M, Knox TA, Fauntleroy JM, Gorbach SL (2001) Weight and body composition in a cohort of HIV-positive men and women. Public Health Nutr 4:743–747PubMedCrossRefGoogle Scholar
  117. 117.
    Kim JH, Spiegelman D, Rimm E, Gorbach SL (2001) The correlates of dietary intake among HIV-positive adults. Am J Clin Nutr 74:852–861PubMedGoogle Scholar
  118. 118.
    Woods MN, Spiegelman D, Knox TA, Forrester JE, Connors JL, Skinner SC, et al (2002) Nutrient intake and body weight in a large HIV cohort that includes women and minorities. J Am Diet Assoc 102:203–211PubMedCrossRefGoogle Scholar
  119. 119.
    Semba RD, Caiaffa WT, Graham NM, Cohn S, Vlahov D (1995) Vitamin A deficiency and wasting as predictors of mortality in human immunodeficiency virus-infected injection drug users. J Infect Dis 171: 1196–1202PubMedCrossRefGoogle Scholar
  120. 120.
    Semba RD, Graham NM, Caiaffa WT, Margolick JB, Clement L, Vlahov D (1993) Increased mortality associated with vitamin A deficiency during human immunodeficiency virus type 1 infection. Arch Intern Med 153:2149–2154PubMedCrossRefGoogle Scholar
  121. 121.
    Haug C, Muller F, Aukrust P, Froland SS (1994) Subnormal serum concentration of 1,25-vitamin D in human immunodeficiency virus infection: correlation with degree of immune deficiency and survival. J Infect Dis 169:889–893PubMedCrossRefGoogle Scholar
  122. 122.
    Baum MK, Shor-Posner G, Lu Y, Rosner B, Sauberlich HE, Fletcher MA, et al (1995) Micronutrients and HIV-i disease progression. AIDS 9:1051–1056PubMedCrossRefGoogle Scholar
  123. 123.
    Liang B, Chung S, Araghiniknam M, Lane LC, Watson RR (1996) Vitamins and immunomodulation in AIDS. Nutrition 12:1–7PubMedCrossRefGoogle Scholar
  124. 124.
    Abrams B, Duncan D, Hertz-Picciotto I (1993) A prospective study of dietary intake and acquired immune deficiency syndrome in HIV-seropositive homosexual men. J Acquir Immune Defic Syndr 6:949–958PubMedGoogle Scholar
  125. 125.
    Baum MK, Shor-Posner G, Lai S, Zhang G, Lai H, Fletcher MA, et al (1997) High risk of HIV-related mortality is associated with selenium deficiency. J Acquir Immune Defic Syndr Hum Retrovirol 15:370–374PubMedCrossRefGoogle Scholar
  126. 126.
    Bauer T, Ewig S, Hasper E, Rockstroh JK, Luderitz B (1995) Predicting in-hospital outcome in HIV-associated Pneumocystis carinii pneumonia. Infection 23:272–277PubMedCrossRefGoogle Scholar
  127. 127.
    Ott M, Fischer H, Polat H, Helm EB, Frenz M, Caspary WF, et al (1995) Bioelectrical impedance analysis as a predictor of survival in patients with human immunodeficiency virus infection. J Acquir Immune Defic Syndr Hum Retrovirol 9:20–25PubMedCrossRefGoogle Scholar
  128. 128.
    Suttmann U, Ockenga J, Selberg 0, Hoogestraat L, Deicher H, Muller MJ (1995) Incidence and prognostic value of malnutrition and wasting in human immunodeficiency virus-infected outpatients. J Acquir Immune Defic Syndr Hum Retrovirol 8:239–246PubMedCrossRefGoogle Scholar
  129. 129.
    Trujillo EB, Borlase BC, Bell SJ, Guenther KJ, Swails W, Queen PM, et al (1992) Assessment of nutritional status, nutrient intake, and nutrition support in AIDS patients. J Am Diet Assoc 92:477–478PubMedGoogle Scholar
  130. 130.
    Huang CM, Ruddel M, Elin RJ (1988) Nutritional sta tus of patients with acquired immunodeficiency syndrome. Clin Chem 34:1957–1959PubMedGoogle Scholar
  131. 131.
    Shevitz AH, Knox TA (2001) Nutrition in the era of highly active antiretroviral therapy. Clin Infect Dis 32:1769–1775PubMedCrossRefGoogle Scholar
  132. 132.
    Shevitz AH, Knox TA, Spiegelman D, Roubenoff R, Gorbach SL, Skolnik PR (1999) Elevated resting energy expenditure among HIV-seropositive persons receiving highly active antiretroviral therapy. AIDS 13:1351–1357PubMedCrossRefGoogle Scholar
  133. 133.
    Melchior JC, Salmon D, Rigaud D, Leport C, Bouvet E, Detruchis P, et al (1991) Resting energy expenditure is increased in stable, malnourished HIV-infected patients. Am J Clin Nutr 53:437–441PubMedGoogle Scholar
  134. 134.
    Pernerstorfer-Schoen H, Schindler K, Parschalk B, Schindl A, Thoeny-Lampert S, Wunderer K, et al (1999) Beneficial effects of protease inhibitors on body composition and energy expenditure: a comparison between HIV-infected and AIDS patients. AIDS 13:2389–2396PubMedCrossRefGoogle Scholar
  135. 135.
    Engelson ES, Rabkin JG, Rabkin R, Kotler DP (1996) Effects of testosterone upon body composition. J Acquir Immune Defic Syndr Hum Retrovirol 11:510–511PubMedCrossRefGoogle Scholar
  136. 136.
    Mulligan K, Grunfeld C, Hellerstein MK, Neese RA, Schambelan M (1993) Anabolic effects of recombinant human growth hormone in patients with wasting associated with human immunodeficiency virus infection. J Clin Endocrinol Metab 77:956–962PubMedCrossRefGoogle Scholar
  137. 137.
    Schambelan M, Mulligan K, Grunfeld C, Daar ES, LaMarca A, Kotler DP, et al (1996) Recombinant human growth hormone in patients with HIV-associated wasting. A randomized, placebo-controlled trial. Serostim Study Group. Ann Intern Med 125:873–882PubMedGoogle Scholar
  138. 138.
    Engelson ES, PI-Sunyer FX, Kotler DP (1999) Effects of megestrol acetate and testosterone on body composition in castrated male Sprague-Dawley rats. Nutrition 15:465–473PubMedCrossRefGoogle Scholar
  139. 139.
    Von Roenn JH, Murphy RL, Wegener N (1990) Megestrol acetate for treatment of anorexia and cachexia associated with human immunodeficiency virus infection. Semin Oncol 17[Suppl 9]:13–16Google Scholar
  140. 140.
    Von Roenn JH, Armstrong D, Kotler DP, Cohn DL, Klimas NG, Tchekmedyian NS, et al (1994) Megestrol acetate in patients with AIDS-related cachexia. Ann Intern Med 121:393–399Google Scholar
  141. 141.
    Struwe M, Kaempfer SH, Geiger CJ, Pavia AT, Plasse TF, Shepard KV, et al (1993) Effect of dronabinol on nutritional status in HIV infection. Ann Pharmaco-ther 27:827–831Google Scholar
  142. 142.
    Gorter R, Seefried M, Volberding P (1992) Dronabinol effects on weight in patients with HIV infection. AIDS 6:127PubMedCrossRefGoogle Scholar
  143. 143.
    Oster MH, Enders SR, Samuels SJ, Cone LA, Hooton TM, Browder HP, et al (1994) Megestrol acetate in patients with AIDS and cachexia. Ann Intern Med 121:400–408PubMedGoogle Scholar
  144. 144.
    Beal JE, Olson R, Laubenstein L, Morales JO, Bellman P, Yangco B, et al (1995) Dronabinol as a treatment for anorexia associated with weight loss in patients with AIDS. J Pain Symptom Manage 10:89–97PubMedCrossRefGoogle Scholar
  145. 145.
    Simon DM, Cello JP, Valenzuela J, Levy R, Dickerson G, Goodgame R, et al (1995) Multicenter trial of octreotide in patients with refractory acquired immunodeficiency syndrome-associated diarrhea. Gastroenterology 108:1753–1760PubMedCrossRefGoogle Scholar
  146. 146.
    Bini EJ, Cohen J (1999) Impact of protease inhibitors on the outcome of human immunodeficiency virus-infected patients with chronic diarrhea. Am J Gastroenterol 94:3553–3559PubMedCrossRefGoogle Scholar
  147. 147.
    Canani RB, Spagnuolo MI, Cirillo P, Guarino A (1999) Ritonavir combination therapy restores intestinal function in children with advanced HIV disease. J Acquir Immune Defic Syndr 21:307–312PubMedCrossRefGoogle Scholar
  148. 148.
    Grinspoon S, Corcoran C, Parlman K, Costello M, Rosenthal D, Anderson E, et al (2000) Effects of testosterone and progressive resistance training in eugonadal men with AIDS wasting. A randomized, controlled trial. Ann Intern Med 133:348–355PubMedGoogle Scholar
  149. 149.
    Roubenoff R, Skolnik PR, Shevitz A, Snydman L, Wang A, Melanson S, et al (1999) Effect of a single bout of acute exercise on plasma human immunodeficiency virus RNA levels. J Appl Physiol 86:1197–1201PubMedGoogle Scholar

Copyright information

© Springer-Verlag Italia 2003

Authors and Affiliations

  • Leon L. Lai
  • Tamsin A. Knox
  • Sherwood L. Gorbach

There are no affiliations available

Personalised recommendations