Gender Specific Differences in the Immune Response to Infection

REVIEW

Abstract

There are many instances where males and females differ in the susceptibility to infections. The reason for these differences in susceptibility is multifactorial. The primary cause is thought to be due to differences induced by sex hormones and their effects on gene expression as well as the immune system, but may also be due to innate physiological differences between males and females. This review summarizes gender specific differences seen in infections caused by bacteria, fungi, parasites and viruses. Ultimately, gender specific differences appear to be dependent on the microbe causing the infection, as not every infection with a specific microbial type results in increased susceptibility of one gender over the other. This suggests that there is an interaction between gender specific immune differences and the specific immune response to individual microbes.

Keywords

Gender differences Microbial infection Immune response 

Abbreviations

IFN-γ

Interferon γ

IL-4

Interleukin-4

TNF-α

Tumor necrosis factor α

TH1

T helper 1

DES

Diethylstilbestrol

LTA

Lipotechoic acid

LPS

Lipopolysaccharide

AIDS

Acquired immune deficiency syndrome

HIV

Human immunodeficiency virus

RSV

Respiratory syncytial virus

HSV-2

Herpes simplex virus-2

CMV

Cytomegalovirus

CD38

Cluster of differentiation 38

TLR7

Toll-like receptor 7

CCR5

C-C chemokine receptor type 5

References

  1. Abebe F, Gaarder PI, Petros B et al (2001) Age- and sex-related differences in antibody responses against Schistosoma mansoni soluble egg antigen in a cohort of school children in Ethiopia. APMIS 109:816–824PubMedGoogle Scholar
  2. Alexander J (1988) Sex differences and cross-immunity in DBA/2 mice infected with L. mexicana and L. major. Parasitology 96(Pt 2):297–302PubMedGoogle Scholar
  3. Al-Hasan MN, Wilson JW, Lahr BD et al (2008) Incidence of Pseudomonas aeruginosa bacteremia: a population-based study. Am J Med 121:702–708PubMedGoogle Scholar
  4. Allard C, Carignan A, Bergevin M et al (2008) Secular changes in incidence and mortality associated with Staphylococcus aureus bacteraemia in Quebec, Canada, 1991–2005. Clin Microbiol Infect 14:421–428PubMedGoogle Scholar
  5. Aly R (1994) Ecology and epidemilogy of dermatophyte infections. J Am Acad Dermatol 31(3 Pt 2):S21–S25PubMedGoogle Scholar
  6. Amornkul PN, Hu DJ, Tansuphasawadikul S et al (2003) Human immunodeficiency virus type 1 subtype and other factors associated with extrapulmonary Cryptococcosis among patients in Thailand with AIDS. AIDS Res Hum Retroviruses 19:85–90PubMedGoogle Scholar
  7. Anastos K, Gange SJ, Lau B et al (2000) Association of race and gender with HIV-1 RNA levels and immunologic progression. J Acquir Immune Defic Syndr 24:218–226PubMedGoogle Scholar
  8. Aoyama M, Kotani J, Usami M (2009) Gender difference in granulocyte dynamics and apoptosis and the role of IL-18 during endotoxin-induced systemic inflammation. Shock 32:401–409PubMedGoogle Scholar
  9. Aulock SV, Deininger S, Draing C et al (2006) Gender difference in cytokine secretion on immune stimulation with LPS and LTA. J Interferon Cytokine Res 26:887–892PubMedGoogle Scholar
  10. Barna M, Komatsu T, Bi Z et al (1996) Sex differences in susceptibility to viral infection of the central nervous system. J Neuroimmunol 67:31–39PubMedGoogle Scholar
  11. Bava AJ, Negroni R (1992) [The epidemiological characteristics of 105 cases of cryptococcosis diagnosed in the Republic of Argentina between 1981–1990]. In Spanish. Rev Inst Med Trop Sao Paulo 34:335–340PubMedGoogle Scholar
  12. Benfield T, Espersen F, Frimodt-Moller N et al (2007) Increasing incidence but decreasing in-hospital mortality of adult Staphylococcus aureus bacteraemia between 1981 and 2000. Clin Microbiol Infect 13:257–263PubMedGoogle Scholar
  13. Benten WP, Wunderlich F, Mossmann H (1992) Testosterone-induced suppression of self-healing Plasmodium chabaudi malaria: an effect not mediated by androgen receptors? J Endocrinol 135:407–413PubMedGoogle Scholar
  14. Benten WP, Wunderlich F, Herrmann R et al (1993) Testosterone-induced compared with oestradiol-induced immunosuppression against Plasmodium chabaudi malaria. J Endocrinol 139:487–494PubMedGoogle Scholar
  15. Benten WP, Ulrich P, Kuhn-Velten WN et al (1997) Testosterone-induced susceptibility to Plasmodium chabaudi malaria: persistence after withdrawal of testosterone. J Endocrinol 153:275–281Google Scholar
  16. Berman J, Sudbery PE (2002) Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3:918–930PubMedGoogle Scholar
  17. Bhavanam S, Snider DP, Kaushic C (2008) Intranasal and subcutaneous immunization under the effect of estradiol leads to better protection against genital HSV-2 challenge compared to progesterone. Vaccine 26:6165–6172PubMedGoogle Scholar
  18. Brown IN, Glynn AA (1987) The Ity/Lsh/Bcg gene significantly affects mouse resistance to Mycobacterium lepraemurium. Immunology 62:587–591PubMedGoogle Scholar
  19. Camara M, Dieye TN, Seydi M et al (2010) Low-level CD4+ T cell activation in HIV-exposed seronegative subjects: influence of gender and condom use. J Infect Dis 201:835–842PubMedGoogle Scholar
  20. Casadevall A, Perfect JR (1998) Cryptococcus neoformans. ASM Press, Washington, DCGoogle Scholar
  21. Chaisson RE, Keruly JC, Moore RD (1995) Race, sex, drug use, and progression of human immunodeficiency virus disease. N Engl J Med 333:751–756PubMedGoogle Scholar
  22. Chavarria A, Fleury A, Garcia E et al (2005) Relationship between the clinical heterogeneity of neurocysticercosis and the immune-inflammatory profiles. Clin Immunol 116:271–278PubMedGoogle Scholar
  23. Chuang YM, Ho YC, Chang HT et al (2008) Disseminated cryptococcosis in HIV-uninfected patients. Eur J Clin Microbiol Infect Dis 27:307–310PubMedGoogle Scholar
  24. Colocho Zelaya EA, Orvell C, Strannegard O (1994) Eosinophil cationic protein in nasopharyngeal secretions and serum of infants infected with respiratory syncytial virus. Pediatr Allergy Immunol 5:100–106PubMedGoogle Scholar
  25. Cook IF (2009) Sex differences in injection site reactions with human vaccines. Hum Vaccine 5:441–449Google Scholar
  26. Cozzi Lepri A, Pezzotti P, Dorrucci M et al (1994) HIV disease progression in 854 women and men infected through injecting drug use and heterosexual sex and followed for up to nine years from seroconversion. Italian Seroconversion Study. BMJ 309:1537–1542PubMedGoogle Scholar
  27. Curtis J, Turk JL (1984) Resistance to subcutaneous infection with Mycobacterium lepraemurium is controlled by more than one gene. Infect Immun 43:925–930PubMedGoogle Scholar
  28. Degu G, Mengistu G, Jones J (2002) Some factors affecting prevalence of and immune responses to Schistosoma mansoni in schoolchildren in Gorgora, northwest Ethiopia. Ethiop Med J 40:345–352PubMedGoogle Scholar
  29. Demkow U, Filewska M, Michalowska-Mitczuk D et al (2007) Heterogeneity of antibody response to myobacterial antigens in different clinical manifestations of pulmonary tuberculosis. J Physiol Pharmacol 58(suppl 5):117–127PubMedGoogle Scholar
  30. Diamond RD (1983) Inhibition of monocyte-mediated damage to fungal hyphae by steroid hormones. J Infect Dis 147:160PubMedGoogle Scholar
  31. Dromer F, Mathoulin S, Dupont B et al (1996a) Epidemiology of cryptococcosis in France: a 9-year survey (1985–1993). French Cryptococcosis Study Group. Clin Infect Dis 23:82–90PubMedGoogle Scholar
  32. Dromer F, Mathoulin S, Dupont B et al (1996b) Individual and environmental factors associated with infection due to Cryptococcus neoformans serotype D. French Cryptococcosis Study Group. Clin Infect Dis 23:91–96PubMedGoogle Scholar
  33. Ellabib MS, Agaj M, Khalifa Z et al (2002) Yeasts of the genus Candida are the dominant cause of onychomycosis in Libyan women but not men: results of a 2-year surveillance study. Br J Dermatol 146:1038–1041PubMedGoogle Scholar
  34. European Paediatric Hepatitis C Virus Network (2001) Effects of mode of delivery and infant feeding on the risk of mother-to-child transmission of hepatitis C virus. BJOG 108:371–377Google Scholar
  35. Eyster ME, Goedert JJ, Poon MC et al (1983) Acid-labile alpha interferon. A possible preclinical marker for the acquired immunodeficiency syndrome in hemophilia. N Engl J Med 309:583–586PubMedGoogle Scholar
  36. Fahey JL, Taylor JM, Detels R et al (1990) The prognostic value of cellular and serologic markers in infection with human immunodeficiency virus type 1. N Engl J Med 322:166–172PubMedGoogle Scholar
  37. Fahey JL, Taylor JM, Manna B et al (1998) Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS 12:1581–1590PubMedGoogle Scholar
  38. Farzadegan H, Hoover DR, Astemborski J et al (1998) Sex differences in HIV-1 viral load and progression to AIDS. Lancet 352:1510–1514PubMedGoogle Scholar
  39. Faulkner L, Altmann DM, Ellmerich S et al (2007) Sexual dimorphism in superantigen shock involves elevated TNF-alpha and TNF-alpha induced hepatic apoptosis. Am J Respir Crit Care Med 176:473–482PubMedGoogle Scholar
  40. Fleming PL, Ciesielski CA, Byers RH et al (1993) Gender differences in reported AIDS-indicative diagnoses. J Infect Dis 168:61–67PubMedGoogle Scholar
  41. Friedland GH, Saltzman B, Vileno J et al (1991) Survival differences in patients with AIDS. J Acquir Immune Defic Syndr 4:144–153PubMedGoogle Scholar
  42. Gandhi M, Bacchetti P, Miotti P et al (2002) Does patient sex affect human immunodeficiency virus levels? Clin Infect Dis 35:313–322PubMedGoogle Scholar
  43. Gillgrass AE, Ashkar AA, Rosenthal KL et al (2003) Prolonged exposure to progesterone prevents induction of protective mucosal responses following intravaginal immunization with attenuated herpes simplex virus type 2. J Virol 77:9845–9851PubMedGoogle Scholar
  44. Gillgrass AE, Fernandez SA, Rosenthal KL et al (2005) Estradiol regulates susceptibility following primary exposure to genital herpes simplex virus type 2, while progesterone induces inflammation. J Virol 79:3107–3116PubMedGoogle Scholar
  45. Giorgi JV, Hultin LE, McKeating JA et al (1999) Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179:859–870PubMedGoogle Scholar
  46. Giron-Gonzalez JA, Moral FJ, Elvira J et al (2000) Consistent production of a higher TH1:TH2 cytokine ratio by stimulated T cells in men compared with women. Eur J Endocrinol 143:31–36PubMedGoogle Scholar
  47. Glynn JR, Crampin AC, Ngwira BM et al (2008) Herpes simplex virus type 2 trends in relation to the HIV epidemic in northern Malawi. Sex Transm Infect 84:356–360PubMedGoogle Scholar
  48. Goble FC, Konopka EA (1973) Sex as a factor in infectious disease. Trans NY Acad Sci 35:325–346Google Scholar
  49. Greenblatt RM, Ameli N, Grant RM et al (2000) Impact of the ovulatory cycle on virologic and immunologic markers in HIV-infected women. J Infect Dis 181:82–90PubMedGoogle Scholar
  50. Guzman C, Camacho-Arroyo I, De Leon-Nava MA et al (2009) Neonatal exposure to estradiol induces resistance to helminth infection and changes in the expression of sex steroid hormone receptors in the brain and spleen in adult mice of both sexes. Brain Behav Immun 23:709–715PubMedGoogle Scholar
  51. Hajjeh RA, Conn LA, Stephens DS et al (1999) Cryptococcosis: population-based multistate active surveillance and risk factors in human immunodeficiency virus-infected persons. Cryptococcal Active Surveillance Group. J Infect Dis 179:449–454PubMedGoogle Scholar
  52. Han X, Lundberg P, Tanamachi B et al (2001) Gender influences herpes simplex virus type 1 infection in normal and gamma interferon-mutant mice. J Virol 75:3048–3052PubMedGoogle Scholar
  53. Hlady WG, Klontz KC (1996) The epidemiology of Vibrio infections in Florida, 1981–1993. J Infect Dis 173:1176–1183PubMedGoogle Scholar
  54. Hoover DR, Peng Y, Saah A et al (1996) Occurrence of cytomegalovirus retinitis after human immunodeficiency virus immunosuppression. Arch Ophthalmol 114:821–827PubMedGoogle Scholar
  55. Howard M, Sellors JW, Jang D et al (2003) Regional distribution of antibodies to herpes simplex virus type 1 (HSV-1) and HSV-2 in men and women in Ontario, Canada. J Clin Microbiol 41:84–89PubMedGoogle Scholar
  56. Hsia S, Howell DN, Amos DB et al (1977) Studies of viral antibody responses among Amish families. J Immunol 118:1659–1664PubMedGoogle Scholar
  57. Hughes GC, Thomas S, Li C et al (2008) Cutting edge: progesterone regulates IFN-alpha production by plasmacytoid dendritic cells. J Immunol 180:2029–2033PubMedGoogle Scholar
  58. Istas AS, Demmler GJ, Dobbins JG et al (1995) Surveillance for congenital cytomegalovirus disease: a report from the National Congenital Cytomegalovirus Disease Registry. Clin Infect Dis 20:665–670PubMedGoogle Scholar
  59. Jarefors S, Bennet L, You E et al (2006) Lyme borreliosis reinfection: might it be explained by a gender difference in immune response? Immunology 118:224–232PubMedGoogle Scholar
  60. Jean SS, Fang CT, Shau WY et al (2002) Cryptococcaemia: clinical features and prognostic factors. QJM 95:511–518PubMedGoogle Scholar
  61. Jones TC, Johnson WD Jr, Barretto AC et al (1987) Epidemiology of American cutaneous leishmaniasis due to Leishmania braziliensis braziliensis. J Infect Dis 156:73–83PubMedGoogle Scholar
  62. Kaushic C, Ashkar AA, Reid LA et al (2003) Progesterone increases susceptibility and decreases immune responses to genital herpes infection. J Virol 77:4558–4565PubMedGoogle Scholar
  63. Kelvin EA, Carpio A, Bagiella E et al (2009) The association of host age and gender with inflammation around neurocysticercosis cysts. Ann Trop Med Parasitol 103:487–499PubMedGoogle Scholar
  64. Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264PubMedGoogle Scholar
  65. Krown SE, Niedzwiecki D, Bhalla RB et al (1991) Relationship and prognostic value of endogenous interferon-alpha, beta 2-microglobulin, and neopterin serum levels in patients with Kaposi sarcoma and AIDS. J Acquir Immune Defic Syndr 4:871–880PubMedGoogle Scholar
  66. Kuo Chou TN, Chao WN, Yang C et al (2010) Predictors of mortality in skin and soft-tissue infections caused by Vibrio vulnificus. World J Surg 34:1669–1675PubMedGoogle Scholar
  67. Laupland KB, Gregson DB, Church DL et al (2008) Incidence, risk factors and outcomes of Escherichia coli bloodstream infections in a large Canadian region. Clin Microbiol Infect 14:1041–1047PubMedGoogle Scholar
  68. Lawn SD, Butera ST, Folks TM (2001) Contribution of immune activation to the pathogenesis and transmission of human immunodeficiency virus type 1 infection. Clin Microbiol Rev 14:753–777PubMedGoogle Scholar
  69. Lemp GF, Hirozawa AM, Cohen JB et al (1992) Survival for women and men with AIDS. J Infect Dis 166:74–79PubMedGoogle Scholar
  70. Lezama-Davila CM, Isaac-Marquez AP, Barbi J et al (2007a) 17Beta-estradiol increases Leishmania mexicana killing in macrophages from DBA/2 mice by enhancing production of nitric oxide but not pro-inflammatory cytokines. Am J Trop Med Hyg 76:1125–1127PubMedGoogle Scholar
  71. Lezama-Davila CM, Oghumu S, Satoskar AR et al (2007b) Sex-associated susceptibility in humans with chiclero’s ulcer: resistance in females is associated with increased serum-levels of GM-CSF. Scand J Immunol 65:210–211PubMedGoogle Scholar
  72. Lortholary O, Improvisi L, Fitting C et al (2002) Influence of gender and age on course of infection and cytokine responses in mice with disseminated Cryptococcus neoformans infection. Clin Microbiol Infect 8:31–37PubMedGoogle Scholar
  73. Lynch NR, Yarzabal L, Verde O et al (1982) Delayed-type hypersensitivity and immunoglobulin E in American cutaneous leishmaniasis. Infect Immun 38:877–881PubMedGoogle Scholar
  74. MacDonald EM, Savoy A, Gillgrass A et al (2007) Susceptibility of human female primary genital epithelial cells to herpes simplex virus, type-2 and the effect of TLR3 ligand and sex hormones on infection. Biol Reprod 77:1049–1059PubMedGoogle Scholar
  75. Marguerite M, Gallissot MC, Diagne M et al (1999) Cellular immune responses of a Senegalese community recently exposed to Schistosoma mansoni: correlations of infection level with age and inflammatory cytokine production by soluble egg antigen-specific cells. Trop Med Int Health 4:530–543PubMedGoogle Scholar
  76. May RC (2007) Gender, immunity and the regulation of longevity. Bioessays 29:795–802PubMedGoogle Scholar
  77. Meier A, Chang JJ, Chan ES et al (2009) Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat Med 15:955–959PubMedGoogle Scholar
  78. Mellors JW, Griffith BP, Ortiz MA et al (1991) Tumor necrosis factor-alpha/cachectin enhances human immunodeficiency virus type 1 replication in primary macrophages. J Infect Dis 163:78–82PubMedGoogle Scholar
  79. Melnick SL, Sherer R, Louis TA et al (1994) Survival and disease progression according to gender of patients with HIV infection. The Terry Beirn Community Programs for Clinical Research on AIDS. JAMA 272:1915–1921PubMedGoogle Scholar
  80. Merkel SM, Alexander S, Zufall E et al (2001) Essential role for estrogen in protection against Vibrio vulnificus-induced endotoxic shock. Infect Immun 69:6119–6122PubMedGoogle Scholar
  81. Micol R, Lortholary O, Sar B et al (2007) Prevalence, determinants of positivity, and clinical utility of cryptococcal antigenemia in Cambodian HIV-infected patients. J Acquir Immune Defic Syndr 45:555–559PubMedGoogle Scholar
  82. Mildvan D, Machado SG, Wilets I et al (1992) Endogenous interferon and triglyceride concentrations to assess response to zidovudine in AIDS and advanced AIDS-related complex. Lancet 339:453–456PubMedGoogle Scholar
  83. Mitchell TG, Perfect JR (1995) Cryptococcosis in the era of AIDS—100 years after the discovery of Cryptococcus neoformans. Clin Microbiol Rev 8:515–548PubMedGoogle Scholar
  84. Mock BA, Nacy CA (1988) Hormonal modulation of sex differences in resistance to Leishmania major systemic infections. Infect Immun 56:3316–3319PubMedGoogle Scholar
  85. Moore RD, Hidalgo J, Sugland BW et al (1991) Zidovudine and the natural history of the acquired immunodeficiency syndrome. N Engl J Med 324:1412–1416PubMedGoogle Scholar
  86. Muller D, Chen M, Vikingsson A et al (1995) Oestrogen influences CD4+ T-lymphocyte activity in vivo and in vitro in beta 2-microglobulin-deficient mice. Immunology 86:162–167PubMedGoogle Scholar
  87. Munoz G, Davies CR (2006) Leishmania panamensis transmission in the domestic environment: the results of a prospective epidemiological survey in Santander, Colombia. Biomedica 26(suppl 1):131–144PubMedGoogle Scholar
  88. Nagayama Y, Tsubaki T, Nakayama S et al (2006) Gender analysis in acute bronchiolitis due to respiratory syncytial virus. Pediatr Allergy Immunol 17:29–36PubMedGoogle Scholar
  89. Naidu J (1993) Growing incidence of cutaneous and ungual infections by non-dermatophyte fungi at Jabalpur (M.P.). Indian J Pathol Microbiol 36:113–118PubMedGoogle Scholar
  90. Naus CW, Booth M, Jones FM et al (2003) The relationship between age, sex, egg-count and specific antibody responses against Schistosoma mansoni antigens in a Ugandan fishing community. Trop Med Int Health 8:561–568PubMedGoogle Scholar
  91. Nazli A, Yao XD, Smieja M et al (2009) Differential induction of innate anti-viral responses by TLR ligands against Herpes simplex virus, type 2, infection in primary genital epithelium of women. Antiviral Res 81:103–112PubMedGoogle Scholar
  92. Nebavi F, Ayala FJ, Renaud F et al (2006) Clonal population structure and genetic diversity of Candida albicans in AIDS patients from Abidjan (Cote d’Ivoire). Proc Natl Acad Sci USA 103:3663–3668PubMedGoogle Scholar
  93. Oliver JD (2005) Wound infections caused by Vibrio vulnificus and other marine bacteria. Epidemiol Infect 133:383–391PubMedGoogle Scholar
  94. Pembrey L, Newell ML, Tovo PA (2008) Age-related lymphocyte and neutrophil levels in children of hepatitis C-infected women. Pediatr Infect Dis J 27:800–807PubMedGoogle Scholar
  95. Penaloza C, Estevez B, Orlanski S et al (2009) Sex of the cell dictates its response: differential gene expression and sensitivity to cell death inducing stress in male and female cells. FASEB J 23:1869–1879PubMedGoogle Scholar
  96. Pereira AJCS (1988) Inquerito intradermico para paracoccidioidomicose em Goiania. Rev Pat Trop 17:157–186Google Scholar
  97. Pinzan CF, Ruas LP, Casabona-Fortunato AS et al (2010) Immunological basis for the gender differences in murine Paracoccidioides brasiliensis infection. PLoS One 5:e10757PubMedGoogle Scholar
  98. Pope V, Larsen SA, Rice RJ et al (1994) Flow cytometric analysis of peripheral blood lymphocyte immunophenotypes in persons infected with Treponema pallidum. Clin Diagn Lab Immunol 1:121–124PubMedGoogle Scholar
  99. Portales P, Clot J, Corbeau P (2001) Sex differences in HIV-1 viral load due to sex difference in CCR5 expression. Ann Intern Med 134:81–82PubMedGoogle Scholar
  100. Poynard T, Bedossa P, Opolon P (1997) Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 349:825–832PubMedGoogle Scholar
  101. Pung OJ, Luster MI, Hayes HT et al (1984) Resistance in mice: increased susceptibility to Listeria monocytogenes after exposure to estrogenic hormones. Infect Immun 46:301–307PubMedGoogle Scholar
  102. Pung OJ, Tucker AN, Vore SJ et al (1985) Influence of estrogen on host resistance: increased susceptibility of mice to Listeria monocytogenes correlates with depressed production of interleukin 2. Infect Immun 50:91–96PubMedGoogle Scholar
  103. Quach C, Piche-Walker L, Platt R et al (2003) Risk factors associated with severe influenza infections in childhood: implication for vaccine strategy. Pediatrics 112(3 Pt 1):e197–e201PubMedGoogle Scholar
  104. Rabenau HF, Buxbaum S, Preiser W et al (2002) Seroprevalence of herpes simplex virus types 1 and type 2 in the Frankfurt am Main area, Germany. Med Microbiol Immunol 190:153–160PubMedGoogle Scholar
  105. Reithinger R, Mohsen M, Aadil K et al (2003) Anthroponotic cutaneous leishmaniasis, Kabul, Afghanistan. Emerg Infect Dis 9:727–729PubMedGoogle Scholar
  106. Remoue F, To Van D, Schacht AM et al (2001) Gender-dependent specific immune response during chronic human Schistosomiasis haematobia. Clin Exp Immunol 124:62–68PubMedGoogle Scholar
  107. Restrepo A, Benard G, de Castro CC et al (2008) Pulmonary paracoccidioidomycosis. Semin Respir Crit Care Med 29:182–197PubMedGoogle Scholar
  108. Reynes J, Portales P, Segondy M et al (2000) CD4+ T cell surface CCR5 density as a determining factor of virus load in persons infected with human immunodeficiency virus type 1. J Infect Dis 181:927–932PubMedGoogle Scholar
  109. Rezza G, Lepri AC, d’Arminio Monforte A et al (2000) Plasma viral load concentrations in women and men from different exposure categories and with known duration of HIV infection. I.CO.N.A. Study Group. J Acquir Immune Defic Syndr 25:56–62PubMedGoogle Scholar
  110. Rodriguez B, Lederman MM, Jiang W et al (2006) Interferon-alpha differentially rescues CD4 and CD8 T cells from apoptosis in HIV infection. AIDS 20:1379–1389PubMedGoogle Scholar
  111. Rothenberg R, Woelfel M, Stoneburner R et al (1987) Survival with the acquired immunodeficiency syndrome. Experience with 5833 cases in New York City. N Engl J Med 317:1297–1302PubMedGoogle Scholar
  112. Ruiz-Herrera J, Elorza MV, Valentin E et al (2006) Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res 6:14–29PubMedGoogle Scholar
  113. Sato N (1972) Mycobacterium marnium isolated from skin lesions of a patient. Jpn J Bacteriol 27:775–779Google Scholar
  114. Satoskar A, Alexander J (1995) Sex-determined susceptibility and differential IFN-gamma and TNF-alpha mRNA expression in DBA/2 mice infected with Leishmania mexicana. Immunology 84:1–4PubMedGoogle Scholar
  115. Satoskar A, Al-Quassi HH, Alexander J (1998) Sex-determined resistance against Leishmania mexicana is associated with the preferential induction of a Th1-like response and IFN-gamma production by female but not male DBA/2 mice. Immunol Cell Biol 76:159–166PubMedGoogle Scholar
  116. Schott E, Witt H, Hinrichsen H et al (2007) Gender-dependent association of CTLA4 polymorphisms with resolution of hepatitis C virus infection. J Hepatol 46:372–380PubMedGoogle Scholar
  117. Shanker G, Sorci-Thomas M, Adams MR (1994) Estrogen modulates the expression of tumor necrosis factor alpha mRNA in phorbol ester-stimulated human monocytic THP-1 cells. Lymphokine Cytokine Res 13:377–382PubMedGoogle Scholar
  118. Shapira-Nahor O, Kalinkovich A, Weisman Z et al (1998) Increased susceptibility to HIV-1 infection of peripheral blood mononuclear cells from chronically immune-activated individuals. AIDS 12:1731–1733PubMedGoogle Scholar
  119. Shi WM, Mei XY, Gao F et al (2007) Analysis of genital Candida albicans infection by rapid microsatellite markers genotyping. Chin Med J 120:975–980PubMedGoogle Scholar
  120. Shiddo SA, Aden Mohamed A, Akuffo HO et al (1995) Visceral leishmaniasis in Somalia: prevalence of markers of infection and disease manifestations in a village in an endemic area. Trans R Soc Trop Med Hyg 89:361–365PubMedGoogle Scholar
  121. Sorvillo F, Beall G, Turner PA et al (1997) Incidence and factors associated with extrapulmonary cryptococcosis among persons with HIV infection in Los Angeles County. AIDS 11:673–679PubMedGoogle Scholar
  122. Stanley SK, Ostrowski MA, Justement JS et al (1996) Effect of immunization with a common recall antigen on viral expression in patients infected with human immunodeficiency virus type 1. N Engl J Med 334:1222–1230PubMedGoogle Scholar
  123. Sterling TR, Lyles CM, Vlahov D et al (1999) Sex differences in longitudinal human immunodeficiency virus type 1 RNA levels among seroconverters. J Infect Dis 180:666–672PubMedGoogle Scholar
  124. Sterling TR, Vlahov D, Astemborski J et al (2001) Initial plasma HIV-1 RNA levels and progression to AIDS in women and men. N Engl J Med 344:720–725PubMedGoogle Scholar
  125. Taubenberger JK, Kash JC (2010) Influenza virus evolution, host adaptation, and pandemic formation. Cell Host Microbe 7:440–451PubMedGoogle Scholar
  126. Tovo PA, Palomba E, Ferraris G et al (1997) Increased risk of maternal-infant hepatitis C virus transmission for women coinfected with human immunodeficiency virus type 1. Italian Study Group for HCV Infection in Children. Clin Infect Dis 25:1121–1124PubMedGoogle Scholar
  127. Tovo PA, Pembrey L, Newell ML (2005) A significant sex—but not elective cesarean section—effect on mother-to-child transmission of hepatitis C virus infection. J Infect Dis 192:1872–1879Google Scholar
  128. Travi BL, Osorio Y, Melby PC et al (2002) Gender is a major determinant of the clinical evolution and immune response in hamsters infected with Leishmania spp. Infect Immun 70:2288–2296PubMedGoogle Scholar
  129. Turner BJ, Markson LE, McKee LJ et al (1994) Health care delivery, zidovudine use, and survival of women and men with AIDS. J Acquir Immune Defic Syndr 7:1250–1262PubMedGoogle Scholar
  130. Vassiliadou N, Tucker L, Anderson DJ (1999) Progesterone-induced inhibition of chemokine receptor expression on peripheral blood mononuclear cells correlates with reduced HIV-1 infectability in vitro. J Immunol 162:7510–7518PubMedGoogle Scholar
  131. Villacres MC, Longmate J, Auge C et al (2004) Predominant type 1 CMV-specific memory T-helper response in humans: evidence for gender differences in cytokine secretion. Hum Immunol 65:476–485PubMedGoogle Scholar
  132. Wainwright C (2010) Acute viral bronchiolitis in children—a very common condition with few therapeutic options. Paediatr Respir Rev 11:39–45PubMedGoogle Scholar
  133. Webster M, Libranda-Ramirez BD, Aligui GD et al (1997) The influence of sex and age on antibody isotype responses to Schistosoma mansoni and Schistosoma japonicum in human populations in Kenya and the Philippines. Parasitology 114(Pt 4):383–393PubMedGoogle Scholar
  134. Weigle KA, Santrich C, Martinez F et al (1993) Epidemiology of cutaneous leishmaniasis in Colombia: environmental and behavioral risk factors for infection, clinical manifestations, and pathogenicity. J Infect Dis 168:709–714PubMedGoogle Scholar
  135. White S, Larsen B (1997) Candida albicans morphogenesis is influenced by estrogen. Cell Mol Life Sci 53:744–749PubMedGoogle Scholar
  136. Wunderlich F, Marinovski P, Benten WP et al (1991) Testosterone and other gonadal factor(s) restrict the efficacy of genes controlling resistance to Plasmodium chabaudi malaria. Parasite Immunol 13:357–367PubMedGoogle Scholar
  137. Yamamoto Y, Tomioka H, Sato K et al (1990) Sex differences in the susceptibility of mice to infection induced by Mycobacterium intracellulare. Am Rev Respir Dis 142:430–433PubMedGoogle Scholar
  138. Zanetti AR, Tanzi E, Romano L et al (1998) A prospective study on mother-to-infant transmission of hepatitis C virus. Intervirology 41:208–212PubMedGoogle Scholar
  139. Zegarelli DJ (1993) Fungal infections of the oral cavity. Otolaryngol Clin North Am 26:1069–1089PubMedGoogle Scholar
  140. Zhang X, Essmann M, Burt ET et al (2000a) Estrogen effects on Candida albicans: a potential virulence-regulating mechanism. J Infect Dis 181:1441–1446PubMedGoogle Scholar
  141. Zhang Z, Chen L, Saito S et al (2000b) Possible modulation by male sex hormone of Th1/Th2 function in protection against Plasmodium chabaudi chabaudi AS infection in mice. Exp Parasitol 96:121–129PubMedGoogle Scholar

Copyright information

© L. Hirszfeld Institute of Immunology and Experimental Therapy, Wroclaw, Poland 2011

Authors and Affiliations

  1. 1.Department of Basic SciencesThe Commonwealth Medical CollegeScrantonUSA

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