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RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1
Trigg PI, Kondrachine AV, 1998. The current global malaria situation. Sherman PW, ed. Malaria: Parasite Biology, Pathogenesis, and Protection. Washington, DC: ASM Press, 11–24.
-
2
World Health Organization, 1997. World malaria situation in 1994: population at risk. Wkly Epidemiol Rec 72 :269–276.
-
3
Muehlenbein MP, 2004. Testosterone-Mediated Immune Function: An Energetic Allocation Mechanism Evaluated in Human and Non-Human Primate Males. Ph.D. Thesis, Department of Anthropology, Yale University.
-
4
Wedekind C, Folstad I, 1994. Adaptive or nonadaptive immuno-suppression by sex-hormones. Am Nat 143 :936–938.
-
5
Sheldon BC, Verhulst S, 1996. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11 :317–321.
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6
Folstad I, Nilssen AC, Halvorsen O, Andersen J, 1989. Why do male reindeer (Rangifer tarandus tarandus) have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos 55 :87–92.
-
7
Tiuria R, Horii Y, Makimura S, Ishikawa N, Tsuchiya K, Nawa Y, 1995. Effect of testosterone on the mucosal defence against intestinal helminths in Indian soft-furred rats, Millardia meltada with reference to goblet and mast cell responses. Parasite Immunol 17 :479–484.
-
8
Olsen NJ, Kovacs WJ, 1996. Gonadal steroids and immunity. Endocr Rev 17 :369–384.
-
9
Poulin R, 1996. Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147 :287–295.
-
10
Zuk M, McKean KA, 1996. Sex differences in parasite infections: patterns and processes. Int J Parasitol 26 :1009–1023.
-
11
Moore SL, Wilson K, 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297 :2015–2018.
-
12
Weatherhead PJ, Metz KJ, Bennett GF, Irwin RE, 1993. Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 33 :13–23.
-
13
Saino N, Moller AP, 1994. Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica.Anim Behav 48 :1325–1333.
-
14
Saino N, Moller AP, Bolzern AM, 1995. Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav Ecol 6 :397–404.
-
15
Hasselquist D, Marsh JA, Sherman PW, Wingfield JC, 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45 :167–175.
-
16
Duffy DL, Ball GF, 2002. Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc R Soc Lond B Biol Sci 269 :847–852.
-
17
Weinstein Y, Bercovich Z, 1981. Testosterone effects on bone marrow, thymus and suppressor T cells in the (NZB x NZW) F1 mice: its relevance to autoimmunity. J Immunol 126 :998–1002.
-
18
Schuurs AHWM, Verheul HAM, 1990. Effects of gender and sex steroids on the immune response. J Steroid Biochem Mol Biol 35 :157–172.
-
19
Olsen NJ, Watson MB, Henderson GS, Kovacs WJ, 1991. Androgen deprivation induces phenotypic and functional changes in the thymus of adult mice. Endocrinology 129 :2471–2476.
-
20
Folstad I, Karter AJ, 1992. Parasites, bright males and the immunocompetence handicap. Am Nat 139 :603–622.
-
21
Benten WP, Wunderlich F, Herrmann R, Kuhn-Velten WN, 1993. Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. J Endocrinol 139 :487–494.
-
22
Hadid R, Spinedi E, Daneva T, Grau G, Gaillard RC, 1995. Repeated endotoxin treatment decreases immune and hypo-thalamo-pituitary-adrenal axis responses—effects of orchiectomy and testosterone therapy. Neuroendocrinology 62 :348–355.
-
23
Zuk M, Johnsten TS, Maclarty T, 1995. Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B Biol Sci 260 :205–210.
-
24
Duffy DL, Bentley GE, Drazen DL, 2000. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11 :654–662.
-
25
Grossman CJ, Roselle GA, Mendenhall CL, 1991. Sex steroid regulation of autoimunity. J Steroid Biochem Mol Biol 40 :649– 659.
-
26
Chao TC, Van Alten PJ, Walter RJ, 1994. Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am J Reprod Immunol 32 :43–52.
-
27
Chao TC, Van Alten PJ, Greager JA, Walter RJ, 1995. Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol 160 :43–49.
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28
Grossman CJ, 1995. The role of sex steroids in immune system regulation. Grossman CJ, ed. Bilateral Communication between the Endocrine and Immune Systems. New York: Springer-Verlag, 1–11.
-
29
Benten WP, Ulrich P, Kuhn-Velten WN, Vohr HW, Wunderlich F, 1997. Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. J Endocrinol 153 :275–281.
-
30
Straub RH, Cutolo M, 2001. Involvement of the hypothalamic-pituitary-adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis: viewpoint based on a systemic pathogenetic role. Arthritis Rheum 44 :493–507.
-
31
Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, Mossmann H, 2002. Testosterone signaling in T cells and macrophages. Steroids 67 :535–538.
-
32
Palmer CJ, Makler M, Klaskala WI, Lindo JF, Baum MK, Ager AL, 1998. Increased prevalence of Plasmodium falciparum malaria in Honduras, Central America. Rev Panam Salud Publica 4 :40–42.
-
33
SAS Institute Inc, 2001. SAS System for Windows. Cary, NC: SAS Institute Inc.
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34
Elenkov IJ, Papanicolaou DA, Wilder RL, Chrousos GP, 1996. Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians 108 :374–381.
-
35
Norbiato G, Bevilacqua M, Vago T, Taddei A, Clerici M, 1997. Glucocorticoids and the immune function in the human immunodeficiency virus infection: a study in hypercortisolemic and cortisol-resistant patients. J Clin Endocrinol Metab 82 :3260–3263.
-
36
Elenkov IJ, Chrousos GP, 1999. Stress, cytokine patterns and susceptibility to disease. Baillieres Best Pract Res Clin Endocrinol Metab 13 :583–595.
-
37
Turnbull AV, Rivier CL, 1999. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 79 :1–71.
-
38
Doerr P, Pirke KM, 1976. Cortisol-induced suppression of plasma testosterone in normal adult males. J Clin Endocrinol Metab 43 :622–629.
-
39
Bambino TH, Hsueh AJ, 1981. Direct inhibitory effect of gluco-corticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology 108 :2142–2148.
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40
Faul F, Erdfelder E, 1992. GPower: a priori, post-hoc, and compromise power analyses for MS-DOS. Bonn, FRG: Bonn University, Department of Psychology.
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41
Lehmann EL, 1975. Nonparametrics. Statistical Methods Based on Ranks. San Francisco: Holden-Day.
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Park JW, Park SH, Yeom JS, Huh AJ, Cho YK, Ahn JY, Min GS, Song GY, Kim YA, Ahn SY, Woo SY, Lee BE, Ha EH, Han HS, Yoo K, Seoh JY, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without thrombocytopenia. Ann Trop Med Parasitol 97 :339–344.
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Mendis KN, Carter R, 1992. The role of cytokines in Plasmodium vivax malaria. Mem Inst Oswaldo Cruz 87 :51–55.
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Seoh JY, Khan M, Park SH, Park HK, Shin MH, Ha EH, Lee BE, Yoo K, Han HS, Oh S, Wi JH, Hong CK, Oh CH, Kim YA, Park JW, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without hyperpyrexia. Am J Trop Med Hyg 68 :102–106.
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THE REPRODUCTIVE ENDOCRINE RESPONSE TO PLASMODIUM VIVAX INFECTION IN HONDURANS
MICHAEL P. MUEHLENBEIN
MICHAEL P. MUEHLENBEIN
Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin; Departamento de Laboratorios Clinicos, Hospital Escuela, Tegucigalpa, Honduras; Department of Bacteriology and Parasitology, Tulane National Primate Research Center, Covington, Louisiana; Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
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JACKELINE ALGER
JACKELINE ALGER
Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin; Departamento de Laboratorios Clinicos, Hospital Escuela, Tegucigalpa, Honduras; Department of Bacteriology and Parasitology, Tulane National Primate Research Center, Covington, Louisiana; Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
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FRANK COGSWELL
FRANK COGSWELL
Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin; Departamento de Laboratorios Clinicos, Hospital Escuela, Tegucigalpa, Honduras; Department of Bacteriology and Parasitology, Tulane National Primate Research Center, Covington, Louisiana; Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
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MARK JAMES
MARK JAMES
Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin; Departamento de Laboratorios Clinicos, Hospital Escuela, Tegucigalpa, Honduras; Department of Bacteriology and Parasitology, Tulane National Primate Research Center, Covington, Louisiana; Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
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DONALD KROGSTAD
DONALD KROGSTAD
Department of Anthropology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin; Departamento de Laboratorios Clinicos, Hospital Escuela, Tegucigalpa, Honduras; Department of Bacteriology and Parasitology, Tulane National Primate Research Center, Covington, Louisiana; Department of Tropical Medicine, Tulane University School of Public Health and Tropical Medicine, New Orleans, Louisiana
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Reproductive physiology and endocrinology change with the onset of illness and injury in a variety of species, including humans. To assess the human reproductive endocrine response to malaria, serial serum samples were collected from 8 male and 9 female residents of Honduras infected with Plasmodium vivax (plus 19 male and 23 female healthy age-matched controls) and were analyzed for associations between testosterone, parasitemia, and cytokine levels. Because testosterone has been negatively associated with measures of immune function under various circumstances, it was hypothesized that testosterone would be directly associated with P. vivax parasitemia and inversely associated with proinflammatory cytokine levels. The findings presented here suggest that 1) testosterone levels are positively associated with P. vivax parasitemia in adult males, and 2) males infected with P. vivax exhibit significantly lower testosterone levels and significantly higher cortisol levels than healthy individuals. Depressed androgen levels during physiologic perturbations may be an advantageous, adaptive host response to ameliorate immunosuppression by higher testosterone levels and to curb the use of energetic resources for metabolically expensive anabolic functions.
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-
1
Trigg PI, Kondrachine AV, 1998. The current global malaria situation. Sherman PW, ed. Malaria: Parasite Biology, Pathogenesis, and Protection. Washington, DC: ASM Press, 11–24.
-
2
World Health Organization, 1997. World malaria situation in 1994: population at risk. Wkly Epidemiol Rec 72 :269–276.
-
3
Muehlenbein MP, 2004. Testosterone-Mediated Immune Function: An Energetic Allocation Mechanism Evaluated in Human and Non-Human Primate Males. Ph.D. Thesis, Department of Anthropology, Yale University.
-
4
Wedekind C, Folstad I, 1994. Adaptive or nonadaptive immuno-suppression by sex-hormones. Am Nat 143 :936–938.
-
5
Sheldon BC, Verhulst S, 1996. Ecological immunology: costly parasite defenses and trade-offs in evolutionary ecology. Trends Ecol Evol 11 :317–321.
-
6
Folstad I, Nilssen AC, Halvorsen O, Andersen J, 1989. Why do male reindeer (Rangifer tarandus tarandus) have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos 55 :87–92.
-
7
Tiuria R, Horii Y, Makimura S, Ishikawa N, Tsuchiya K, Nawa Y, 1995. Effect of testosterone on the mucosal defence against intestinal helminths in Indian soft-furred rats, Millardia meltada with reference to goblet and mast cell responses. Parasite Immunol 17 :479–484.
-
8
Olsen NJ, Kovacs WJ, 1996. Gonadal steroids and immunity. Endocr Rev 17 :369–384.
-
9
Poulin R, 1996. Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147 :287–295.
-
10
Zuk M, McKean KA, 1996. Sex differences in parasite infections: patterns and processes. Int J Parasitol 26 :1009–1023.
-
11
Moore SL, Wilson K, 2002. Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297 :2015–2018.
-
12
Weatherhead PJ, Metz KJ, Bennett GF, Irwin RE, 1993. Parasite faunas, testosterone and secondary sexual traits in male red-winged blackbirds. Behav Ecol Sociobiol 33 :13–23.
-
13
Saino N, Moller AP, 1994. Secondary sexual characters, parasites and testosterone in the barn swallow, Hirundo rustica.Anim Behav 48 :1325–1333.
-
14
Saino N, Moller AP, Bolzern AM, 1995. Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behav Ecol 6 :397–404.
-
15
Hasselquist D, Marsh JA, Sherman PW, Wingfield JC, 1999. Is avian humoral immunocompetence suppressed by testosterone? Behav Ecol Sociobiol 45 :167–175.
-
16
Duffy DL, Ball GF, 2002. Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc R Soc Lond B Biol Sci 269 :847–852.
-
17
Weinstein Y, Bercovich Z, 1981. Testosterone effects on bone marrow, thymus and suppressor T cells in the (NZB x NZW) F1 mice: its relevance to autoimmunity. J Immunol 126 :998–1002.
-
18
Schuurs AHWM, Verheul HAM, 1990. Effects of gender and sex steroids on the immune response. J Steroid Biochem Mol Biol 35 :157–172.
-
19
Olsen NJ, Watson MB, Henderson GS, Kovacs WJ, 1991. Androgen deprivation induces phenotypic and functional changes in the thymus of adult mice. Endocrinology 129 :2471–2476.
-
20
Folstad I, Karter AJ, 1992. Parasites, bright males and the immunocompetence handicap. Am Nat 139 :603–622.
-
21
Benten WP, Wunderlich F, Herrmann R, Kuhn-Velten WN, 1993. Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. J Endocrinol 139 :487–494.
-
22
Hadid R, Spinedi E, Daneva T, Grau G, Gaillard RC, 1995. Repeated endotoxin treatment decreases immune and hypo-thalamo-pituitary-adrenal axis responses—effects of orchiectomy and testosterone therapy. Neuroendocrinology 62 :348–355.
-
23
Zuk M, Johnsten TS, Maclarty T, 1995. Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc R Soc Lond B Biol Sci 260 :205–210.
-
24
Duffy DL, Bentley GE, Drazen DL, 2000. Effects of testosterone on cell-mediated and humoral immunity in non-breeding adult European starlings. Behav Ecol 11 :654–662.
-
25
Grossman CJ, Roselle GA, Mendenhall CL, 1991. Sex steroid regulation of autoimunity. J Steroid Biochem Mol Biol 40 :649– 659.
-
26
Chao TC, Van Alten PJ, Walter RJ, 1994. Steroid sex hormones and macrophage function: modulation of reactive oxygen intermediates and nitrite release. Am J Reprod Immunol 32 :43–52.
-
27
Chao TC, Van Alten PJ, Greager JA, Walter RJ, 1995. Steroid sex hormones regulate the release of tumor necrosis factor by macrophages. Cell Immunol 160 :43–49.
-
28
Grossman CJ, 1995. The role of sex steroids in immune system regulation. Grossman CJ, ed. Bilateral Communication between the Endocrine and Immune Systems. New York: Springer-Verlag, 1–11.
-
29
Benten WP, Ulrich P, Kuhn-Velten WN, Vohr HW, Wunderlich F, 1997. Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. J Endocrinol 153 :275–281.
-
30
Straub RH, Cutolo M, 2001. Involvement of the hypothalamic-pituitary-adrenal/gonadal axis and the peripheral nervous system in rheumatoid arthritis: viewpoint based on a systemic pathogenetic role. Arthritis Rheum 44 :493–507.
-
31
Wunderlich F, Benten WP, Lieberherr M, Guo Z, Stamm O, Wrehlke C, Sekeris CE, Mossmann H, 2002. Testosterone signaling in T cells and macrophages. Steroids 67 :535–538.
-
32
Palmer CJ, Makler M, Klaskala WI, Lindo JF, Baum MK, Ager AL, 1998. Increased prevalence of Plasmodium falciparum malaria in Honduras, Central America. Rev Panam Salud Publica 4 :40–42.
-
33
SAS Institute Inc, 2001. SAS System for Windows. Cary, NC: SAS Institute Inc.
-
34
Elenkov IJ, Papanicolaou DA, Wilder RL, Chrousos GP, 1996. Modulatory effects of glucocorticoids and catecholamines on human interleukin-12 and interleukin-10 production: clinical implications. Proc Assoc Am Physicians 108 :374–381.
-
35
Norbiato G, Bevilacqua M, Vago T, Taddei A, Clerici M, 1997. Glucocorticoids and the immune function in the human immunodeficiency virus infection: a study in hypercortisolemic and cortisol-resistant patients. J Clin Endocrinol Metab 82 :3260–3263.
-
36
Elenkov IJ, Chrousos GP, 1999. Stress, cytokine patterns and susceptibility to disease. Baillieres Best Pract Res Clin Endocrinol Metab 13 :583–595.
-
37
Turnbull AV, Rivier CL, 1999. Regulation of the hypothalamic-pituitary-adrenal axis by cytokines: actions and mechanisms of action. Physiol Rev 79 :1–71.
-
38
Doerr P, Pirke KM, 1976. Cortisol-induced suppression of plasma testosterone in normal adult males. J Clin Endocrinol Metab 43 :622–629.
-
39
Bambino TH, Hsueh AJ, 1981. Direct inhibitory effect of gluco-corticoids upon testicular luteinizing hormone receptor and steroidogenesis in vivo and in vitro. Endocrinology 108 :2142–2148.
-
40
Faul F, Erdfelder E, 1992. GPower: a priori, post-hoc, and compromise power analyses for MS-DOS. Bonn, FRG: Bonn University, Department of Psychology.
-
41
Lehmann EL, 1975. Nonparametrics. Statistical Methods Based on Ranks. San Francisco: Holden-Day.
-
42
Park JW, Park SH, Yeom JS, Huh AJ, Cho YK, Ahn JY, Min GS, Song GY, Kim YA, Ahn SY, Woo SY, Lee BE, Ha EH, Han HS, Yoo K, Seoh JY, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without thrombocytopenia. Ann Trop Med Parasitol 97 :339–344.
-
43
Karunaweera ND, Carter R, Grau GE, Mendis KN, 1998. Demonstration of anti-disease immunity to Plasmodium vivax malaria in Sri Lanka using a quantitative method to assess clinical disease. Am J Trop Med Hyg 58 :204–210.
-
44
Mendis KN, Carter R, 1992. The role of cytokines in Plasmodium vivax malaria. Mem Inst Oswaldo Cruz 87 :51–55.
-
45
Seoh JY, Khan M, Park SH, Park HK, Shin MH, Ha EH, Lee BE, Yoo K, Han HS, Oh S, Wi JH, Hong CK, Oh CH, Kim YA, Park JW, 2003. Serum cytokine profiles in patients with Plasmodium vivax malaria: a comparison between those who presented with and without hyperpyrexia. Am J Trop Med Hyg 68 :102–106.
-
46
Mendis KN, Naotunne TD, Karunaweera ND, Del Giudice G, Grau GE, Carter R, 1990. Anti-parasite effects of cytokines in malaria. Immunol Lett 25 :217–220.
-
47
Stevenson MM, Tam MF, Belosevic M, Meide Pvd, Podoba JE, 1990. Role of endogenous gamma interferon in host response to infection with blood-stage Plasmodium chabaudi AS. Infect Immun 58 :3225–3232.
-
48
Artavanis-Tsakonas K, Tongren JE, Riley EM, 2003. The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol 133 :145–152.
-
49
Butcher GA, Garland T, Ajdukiewicz AB, Clark IA, 1990. Serum tumor necrosis factor associated with malaria in patients in the Solomon Islands. Trans R Soc Trop Med Hyg 84 :658–661.
-
50
Brown AE, Teja-Isavadharm P, Webster HK, 1991. Macrophage activation in vivax malaria: fever is associated with increased levels of neopterin and interferon-gamma. Parasite Immunol 13 :673–679.
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