Vaccination to protect against infection of the female reproductive tract

Expert Review of Clinical Immunology

Volumn 8, Issue 1, 2012, Pages 81-94

  Huston, Wilhelmina M ^a   Harvie, Marina ^a   Mittal, Aruna ^b   Timms, Peter ^a   Beagley, Kenneth W ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b SAFDARJUNG HOSPITAL   (India)

Author keywords

female reproductive tract; reproductive tract infection; sexually transmitted infection; vaccine

Indexed keywords

DIPHTHERIA PERTUSSIS POLIOMYELITIS TETANUS HEPATITIS B VACCINE; HEPATITIS B VACCINE; HERPES SIMPLEX VACCINE; WART VIRUS VACCINE;

CANCER IMMUNIZATION; CANCER PREVENTION; CHLAMYDIA TRACHOMATIS; CHLAMYDIASIS; FEMALE GENITAL TRACT INFECTION; HEPATITIS B; HERPES SIMPLEX; HERPES SIMPLEX VIRUS 2; HUMAN; INFECTION PREVENTION; PAPILLOMAVIRUS INFECTION; REVIEW; SEXUALLY TRANSMITTED DISEASE; UTERINE CERVIX CANCER; VACCINATION;

BACTERIAL VACCINES; CHLAMYDIA INFECTIONS; CHLAMYDIA TRACHOMATIS; FEMALE; HUMANS; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; REPRODUCTIVE TRACT INFECTIONS; VACCINATION;

EID: 83455233749     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/eci.11.80     Document Type: Review

References (160)

1. Kelleher P. HIV immunology: what lessons can we learn from recent vaccine trials? J. HIV Ther. 15(1), 2-5 (2010).
2. Mckinnon LR, Card CM. HIV vaccine efficacy trials: a brief history, and options for going forward. AIDS Rev. 12(4), 209-217 (2010).
3. WHO. Global Prevalence and Incidence Of Selected Curable Sexually Transmitted Infections Overview and Estimates. WHO, Geneva, Switzerland (2001).
4. Jarayaman G, Totten S, Perrin M, Fang L, Remes O. Report on Sexually Transmitted Infections in Canada: 2008. Public Health Agency of Canada, Ottawa, ON, Canada (2010).
5. Jindal N, Aggarwah A, Gill P, Sacharwai B, Sheevani BB. Community-based study of reproductive tract infections, including sexually transmitted infections, among the rural population of Punjab, India. India J. Comm. Med. 34, 359-361 (2009).
6. Hoare A, Wilson DP, Regan DG, Kaldor J, Law MG. Using mathematical modelling to help explain the differential increase in HIV incidence in New South Wales, Victoria and Queensland: importance of other sexually transmissible infections. Sex. Health 5, 169-187 (2008).
7. Russell MW, Mestecky J. Tolerance and protection against infection in the genital tract. Immuno. Invest. 39, 500-525 (2010).
8. Vallely A, Page A, Dias S et al. The prevalence of sexually transmitted infections in papua new Guinea: a systematic review and meta-analysis. PLoS One 5(12), e15586 (2010).
9. Guy RJ, Kong F, Goller J et al. A new national Chlamydia sentinel surveillance system in Australia: evaluation of the first stage of implementation. Comm. Dis. Intell. 319-328 (2010).
10. Blandford JM, Gift TL. The cost- effectiveness of single-dose azithromycin for treatment of incubating syphilis. Sex. Transm. Dis. 30, 502-508 (2003).
11. Anonymous. HIV vaccine failure prompts Merck to halt trial. Nature 449, 390 (2007).
12. Tawk HM, Vickery K, Bisset L, Lo SK, Selby W, Cossart YE. The current pattern of hepatitis B virus infection in Australia. J. Viral Hepat. 13, 206-215 (2006).
13. CDC. Sexually transmitted diseases treatment guidelines. Human papillomavirus (HPV) infection MMWR 59(RR-12), 69-71 (2010).
14. Moodley P, Wilkinson D, Connolly C. Trichomonas vaginalis is associated with pelvic inflammatory disease in women infected with human immunodeficiency virus. Clin. Infect. Dis. 34, 519-522 (2002).
15. Forna F, Gülmezoglu AM. Interventions for treating trichomoniasis in women. Cochrane Database Syst. Rev. 2, CD000218 (2003).
16. Petrin D, Delgaty K, Bhatt R, Garber G. Clinical and microbiological aspects of Trichomonas Vaginalis. Clin. Microbiol. Rev. 11, 300-317 (1998).
17. Org GF. Global Health Program. 2011 Bill Melinda Gates Foundation, DC, USA (2010).
18. Witkin SS, Linhares IM, Giraldo P. Bacterial flora of the female genital tract: function and immune regulation. Best Pract. Res. Clin. Obstet. Gynaecol. 21, 347-354 (2007).
19. Fahey JV, Schaefer TM, Wira CR. Sex hormone modulation of human uterine epithelial cell immune responses. Integr. Comp. Biol. 46, 1082-1087 (2006).
20. Wira CR, Rossoll RM, Kaushic C. Antigen-presenting cells in the female reproductive tract: influence of estradiol on antigen presentation by vaginal cells. Endocrinology 141, 2877-2885 (2000).
21. Ruiz RJ, Fullerton J, Brown CE, Dudley DJ. Predicting risk of preterm birth: the roles of stress, clinical risk factors, and corticotropin-releasing hormone. Biol. Res. Nurs. 4, 54-64 (2002).
22. Kawana K, Kawana Y, Schust DJ. Female steroid hormones use signal transducers and activators of transcription protein-mediated pathways to modulate the expression of T-bet in epithelial cells: a mechanism for local immune regulation in the human reproductive tract. Mol. Endocrinol. 19, 2047-2059 (2005).
23. Hickey DK, Patel MV, Fahey JV, Wira CR. Innate and adaptive immunity at mucosal surfaces of the female reproductive tract: stratification and integration of immune protection against the transmission of sexually transmitted infections. J. Reprod. Immunol. 88, 185-189 (2011).
24. Zhao C, Wang I, Lehrer RI. Widespread expression of β-defensin hBD-1 in human secretory glands and epithelial cells. FEBS Lett. 396(2-3), 319-322 (1996).
25. Wira CR, Fahey JV. The innate immune system: gatekeeper to the female reproductive tract. Immunology 111(1), 13-15 (2004).
26. Elinav E, Strowig T, Henao-Mejia J, Flavell RA. Regulation of the antimicrobial response by NLR proteins. Immunity 34, 665-679 (2011).
27. Jiang ZH, Koganty RR. Synthetic vaccines: the role of adjuvants in immune targeting. Curr. Med. Chem. 10, 1423-1439 (2003).
28. Aflatoonian R, Fazeli A. Toll-like receptors in female reproductive tract and their menstrual cycle dependent expression. J. Reprod. Immunol. 77(1), 7-13 (2008).
29. Aflatoonian R, Tuckerman E, Elliott SL et al. Menstrual cycle-dependent changes of Toll-like receptors in endometrium. Hum. Reprod. 22(2), 586-593 (2007).
30. Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum. Reprod. Update 11(4), 411-423 (2005).
31. Fish EN. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol. 8(9), 737-744 (2008).
32. Stopinska-Gluszak U, Waligora J, Grzela T et al. Effect of estrogen/progesterone hormone replacement therapy on natural killer cell cytotoxicity and immunoregulatory cytokine release by peripheral blood mononuclear cells of postmenopausal women. J. Reprod. Immunol. 69(1), 65-75 (2006).
33. Kaul R, Pettengell C, Sheth PM et al. The genital tract immune milieu: an important determinant of HIV susceptibility and secondary transmission. J. Reprod. Immunol. 77(1), 32-40 (2008).
34. Patton DL, Thwin SS, Meier A, Hooton TM, Stapleton AE, Eschenbach DA. Epithelial cell layer thickness and immune cell populations in the normal human vagina at different stages of the menstrual cycle. Am. J. Obstet. Gynecol. 183(4), 967-973 (2000).
35. + CD8+ CTL activity within the human female reproductive tract: influence of stage of the menstrual cycle and menopause. J. Immunol. 158(6), 3017-3027 (1997).
36. Yeaman GR, Collins JE, Fanger MW, Wira CR, Lydyard PM. CD8+ T cells in human uterine endometrial lymphoid aggregates: evidence for accumulation of cells by trafficking. Immunology 102, 434-440 (2001).
37. Yeaman GR, Guyre PM, Fanger MW et al. Unique CD8+ T cell-rich lymphoid aggregates in human uterine endometrium. J. Leukoc. Biol. 61(4), 427-435 (1997).
38. Lu FX, Ma Z, Moser S, Evans TG, Miller CJ. Effects of ovarian steroids on immunoglobulin-secreting cell function in healthy women. Clin. Diagn. Lab. Immunol. 10(5), 944-949 (2003).
39. Wira CR, Sullivan DA. Estradiol and progesterone regulation of immunoglobulin A and G and secretory component in cervicovaginal secretions of the rat. Biol. Reprod. 32(1), 90-95 (1985).
40. Hughes GC, Clark EA. Regulation of dendritic cells by female sex steroids: relevance to immunity and autoimmunity. Autoimmunity 40(6), 470-481 (2007).
41. Kovats S, Carreras E. Regulation of dendritic cell differentiation and function by estrogen receptor ligands. Cell Immunol. 252(1-2), 81-90 (2008).
42. Bengtsson AK, Ryan EJ, Giordano D, Magaletti DM, Clark EA. 17β-estradiol (E2) modulates cytokine and chemokine expression in human monocyte-derived dendritic cells. Blood 104(5), 1404-1410 (2004).
43. Murphy AJ, Guyre PM, Wira CR, Pioli PA. Estradiol regulates expression of estrogen receptor ERα46 in human macrophages. PLoS One 4(5), e5539 (2009).
44. Liang J, Sun L, Wang Q, Hou Y. Progesterone regulates mouse dendritic cells differentiation and maturation. Int. Immunopharmacol. 6(5), 830-838 (2006).
45. Baeten JM, Nyange PM, Richardson BA et al. Hormonal contraception and risk of sexually transmitted disease acquisition: results from a prospective study. Am. J. Obstet. Gynecol. 185, 380-385 (2001).
46. Wira CR, Fahey JV. A new strategy to understand how HIV infects women: identification of a window of vulnerability during the menstrual cycle. AIDS 22, 1909-1917 (2008).
47. Nardelli-Haefliger D, Roden R, Balmelli C, Potts A, Schiller J, De Grandi P. Mucosal but not parenteral immunization with purified human papillomavirus Type 16 virus-like particles induces neutralizing titers of antibodies throughout the estrous cycle of mice. J. Virol. 73(11), 9609-9613 (1999).
48. Johansson EL, Wassen L, Holmgren J, Jertborn M, Rudin A. Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infect. Immun. 69(12), 7481-7486 (2001).
49. Kozlowski PA, Williams SB, Lynch RM et al. Differential induction of mucosal and systemic antibody responses in women after nasal, rectal, or vaginal immunization: influence of the menstrual cycle. J. Immunol. 169(1), 566-574 (2002).
50. Decrausaz L, Domingos-Pereira S, Duc M et al. Parenteral but not mucosal immunization is able to induce regression of human papillomavirus associated genital tumors. Int. J. Cancer 129(3), 762-772 (2011).
51. Stanley, M, Lowy Dr, Fraser I. Chapter 12: prophylactic HPV vaccines: underlying mechanisms. Vaccine 24(Suppl. 3), 106-113 (2006).
52. Ulmer JB, Liu MA. Science and society-vaccines: ethical issues for vaccines and immunization. Nat. Rev. Immunol. 2, 291-296 (2002).
53. Kim JH, Rerks-Ngarm S, Excler JL, Michael NL. HIV vaccines: lessons learned and the way forward. Curr. Opin. HIV AIDS 4, 428-434 (2010).
54. Walboomers JM, Jacobs MV, Manos MM et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189(1), 12-19 (1999).
55. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus Types 16 and 18 E6 proteins with p53. Science 248, 76-79 (1990).
56. Villa LL, Costa RL, Petta CA et al. High sustained efficacy of a prophylactic quadrivalent human papillomavirus Types 6/11/16/18 L1 virus-like particle vaccine through 5 years of follow-up. Br. J. Cancer 1459-1466 (2006).
57. Future I/Ii study group, Dillner J, Kjaer SK et al. Four year efficacy of prophylactic human papillomavirus quadrivalent vaccine against low grade cervical, vulvar, and vaginal intraepithelial neoplasia and anogenital warts: randomised controlled trial. BMJ 341, 3493 (2010).
58. Brotherton JM, Fridman M, May CL, Chappell G, Saville AM, Gertig DM. Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study. Lancet 377(9783), 2085-2092 (2011).
59. Kim JJ. Focus on research: weighing the benefits and costs of HPV vaccination of young men. N. Engl. J. Med. 364, 393-395 (2011).
60. Giuliano AR, Palefsky JM, Goldstone S et al. Efficacy of quadrivalent HPV vaccine against HPV infection and disease in males. N. Engl. J. Med. 364, 401-411 (2011).
61. Greer AL, Fisman DN. Punching above their weight: males, reinfection, and the limited success of Chlamydia screening programs. Sex. Trans. Dis. 36, 9-10 (2009).
62. Anderson ME, Weese JS. Video observation of hand hygiene practices at a petting zoo and the impact of hand hygiene interventions. Epidemiol. Infect. 1-9 (2011).
63. Mast EE, Margolis HS, Fiore AE et al. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus in the United States: recommendations of the Advisory Committee on Immunization Practices (ACIP); Part 1: immunization of infants, children and adolescents. MMWR Recomm. Rep. 54, RR-16 (2005).
64. Mast EE, Weinbaum CM, Fiore AE et al. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus in the United States: recommendations of the advisroty committee on immunization practices (ACIP); Part 2: immunization of adults. MMWR Recomm. Rep. 55, RR-16 (2006).
65. Noble RC, Kirk NM, Slagel WA, Vance BJ, Somes GW. Recidivism among patients with gonococcal infection presenting to a venereal disease clinic. Sex. Transm. Dis. 4(2), 39-43 (1977).
66. Beagley KW, Timms P. Chlamydia trachomatis infection: incidence, health costs and prospects for vaccine development. J. Reprod. Immunol. 48(1), 47-68 (2000).
67. Fleming DT, Mcquillan GM, Johnson RE. Herpes simplex virus Type 2 in the United States. N. Engl. J. Med. 337, 1105-1111 (1997).
68. Bettahi I, Zhang X, Afifi RE, Benmohamed L. Protective immunity to genital herpes simplex virus Type 1 and Type 2 provided by self-adjuvanting lipopeptides that drive dendritic cell maturation and elicit a polarized Th1 immune response. Viral Immunol. 19, 220-236 (2006).
69. Aurelian L. Herpes simplex virus Type 2 vaccines: new ground for optimism? Clin. Diagn. Lab. Immunol. 11, 437-445 (2004).
70. Stanberry LR, Bernstein DI, Burke RL, Pachl C, Myers MG. Vaccination with recombinant herpes simplex virus glycoproteins: protection against initial and recurrent genital herpes. J. Infect. Dis. 155, 914-920 (1987).
71. Stanberry LR, Spruance SL, Cunningham AL et al. Glycoprotein-d-adjuvant vaccine to prevent genital herpes. N. Engl. J. Med. 347, 1652-1662 (2002).
72. Boursnell ME, Entwisle C, Blakeley D et al. A genetically inactivated herpes simplex virus Type 2 (HSV-2) vaccine provides effective protection against primary and recurrent HSV-2 disease. J. Infect. Dis. 175, 16-25 (1997).
73. Cunningham KA, Beagley KW. Male genital tract chlamydial infection: implications for pathology and infertility. Biol. Reprod. 79, 180-189 (2008).
74. Peipert JF. Clinical practice. Genital chlamydial infections. N. Engl. J. Med. 349(25), 2424-2430 (2003).
75. Grayston JT, Woolridge RL, Wang S. Trachoma vaccine studies on Taiwan. Ann. NY Acad. Sci. 98, 352-367 (1962).
76. Kelly KA. Cellular immunity and Chlamydia genital infection: induction, recruitment, and effector mechanisms. Int. Rev. Immunol. 22(1), 3-41 (2003).
77. Morrison SG, Morrison RP. A predominant role for antibody in acquired immunity to chlamydial genital tract reinfection. J. Immunol. 175, 7536-7542 (2005).
78. Morrison SG, Morrison RP. The protective effect of antibody in immunity to murine chlamydial genital tract reinfection is independent of immunoglobulin A. Infect. Immun. 73, 6183-6186 (2005).
79. Johansson M, Schon K, Ward M, Lycke N. Genital tract infection with Chlamydia trachomatis fails to induce protective immunity in gamma interferon receptor-deficient mice despite a strong local immunoglobulin A response. Infect. Immun. 73, 1032-1044 (1997).
80. Andrew DW, Hafner LM, Beagley KW, Timms P. Partial protection against chlamydial reproductive tract infection by a recombinant major outer membrane protein/CpG/cholera toxin intranasal vaccine in the guinea pig Chlamydia caviae model. J. Reprod. Immunol. 91, 9-16 (2011).
81. Cheng C, Pal S, Bettahi I, Oxford KL, Barry PA, De La Maza LM. Immunogenicity of a vaccine formulated with the Chlamydia trachomatis serovar F, native major outer membrane protein in a nonhuman primate model. Vaccine 29, 3456-3464 (2011).
82. Kari L, Whitmire WM, Crane DD et al. Chlamydia trachomatis native major outer membrane protein induces partial protection in nonhuman primates: implication for a trachoma transmission-blocking vaccine. J. Immunol. 182, 8063-8070 (2009).
83. Sun G, Pal S, Weiland J, Peterson EM, De La Maza LM. Protection against an intranasal challenge by vaccines formulated with native and recombinant preparations of the Chlamydia trachomatis major outer membrane protein. Vaccine 27, 5020-5025 (2009).
84. Lü H, Wang H, Zhao HM et al. Dendritic cells (DCs) transfected with a recombinant adenovirus carrying chlamydial major outer membrane protein antigen elicit protective immune responses against genital tract challenge infection. Biochem. Cell Biol. 88, 757-765 (2010).
85. Rockey DD, Wang J, Lei L, Zhong G. Chlamydia vaccine candidates and tools for chlamydial antigen discovery. Expert Rev. Vaccines 8(10), 1365-1377 (2009).
86. Caldwell HD, Kuo CC, Kenny GE. Antigenic analysis of Chlamydiae by two-dimensional immunoelectrophoresis. II. A trachoma-LGV-specific antigen. J. Immunol. 115, 969-975 (1975).
87. Sanchez-Campillo M, Bini L, Comanducci M et al. Identification of immunoreactive proteins of Chlamydia trachomatis by Western blot analysis of a two-dimensional electrophoresis map with patient sera. Electrophoresis 20(11), 2269-2279 (1999).
88. Murphey C, Murthy AK, Meier PA, Neal Guentzel M, Zhong G, Arulanandam BP. The protective efficacy of chlamydial protease-like activity factor vaccination is dependent upon CD4+ T cells. Cell Immunol. 242, 110-117 (2006).
89. Stemke-Hale K, Kaltenboeck B, Degraves FJ et al. Screening the whole genome of a pathogen in vivo for individual protective antigens. Vaccine 23(23), 3016-3025 (2005).
90. Starnbach MN, Loomis WP, Ovendale P et al. An inclusion membrane protein from Chlamydia trachomatis enters the MHC class I pathway and stimulates a CD8+ T cell response. J. Immunol. 171(9), 4742-4749 (2003).
91. Karunakaran KP, Rey-Ladino J, Stoynov N et al. Immunoproteomic discovery of novel T cell antigens from the obligate intracellular pathogen Chlamydia. J. Immunol. 180(4), 2459-2465 (2008).
92. Dong-JI Z, Yang X, Shen C, Lu H, Murdin A, Brunham RC. Priming with Chlamydia trachomatis major outer membrane protein (MOMP) DNA followed by MOMP ISCOM boosting enhances protection and is associated with increased immunoglobulin A and Th1 cellular immune responses. Infect. Immun. 68, 3074-3078 (2000).
93. Pal S, Peterson EM, Rappuoli R, Ratti G, De La Maza LM. Immunization with the Chlamydia trachomatis major outer membrane protein, using adjuvants developed for human vaccines, can induce partial protection in a mouse model against a genital challenge. Vaccine 24, 766-775 (2006).
94. He Q, Martinez-Sobrido L, Eko FO et al. Live-attenuated influenza viruses as delivery vectors for Chlamydia vaccines. Immunology 122(1), 28-37 (2007).
95. Macmillan L, Ifere GO, He Q et al. A recombinant multivalent combination vaccine protects against Chlamydia and genital herpes. FEMS Immunol. Med. Microbiol. 49(1), 46-55 (2007).
96. Hansen J, Jensen KT, Follmann F, Agger EM, Theisen M, Andersen P. Liposome delivery of Chlamydia muridarum major outer membrane protein primes a Th1 response that protects against genital chlamydial infection in a mouse model. J. Infect. Dis. 198, 758-767 (2008).
97. Gray RT, Beagley K, Timms P, Wilson DP. Modeling the impact of potential vaccines on epidemics of sexually transmitted Chlamydia trachomatis infection. J. Infect. Dis. 199, 1680-1688 (2009).
98. Workowski KA, Berman SM. Sexually transmitted diseases treatment guidelines. Centers for disease control and prevention. SOMMWR Recomm. Rep. 55, 1-11 (2006).
99. Zhu W, Chen C, Thomas CE, Anderson JE, Jerse AE, Sparling PF. Vaccines for gonorrhea: can we rise to the challenge? Front. Microbiol. 2, 124 (2011).
100. Liu Y, Feinen B, Russell MW. New concepts in immunity to Neisseria gonorrhoeae: innate responses and suppression of adaptive immunity favor the pathogen, not the host. Front. Microbiol. 2, 52 (2011).
101. Feinen B, Jerse AE, Gaffen SL, Russell MW. Critical role of Th17 responses in a murine model of Neisseria gonorrhoeae genital infection. Mucosal Immunol. 3(3), 312-321 (2010).
102. Boslego JW, Tramont EC, Chung RC et al. Efficacy trial of a parenteral gonococcal pilus vaccine in men. Vaccine 9, 154-162 (1991).
103. Kew OM, Wright PF, Agol VI et al. Circulating vaccine-derived polioviruses: current state of knowledge. Bull. World Health Organ. 82, 1 (2004).
104. Kew O, Morris-Glasgow V, Landaverde M et al. Outbreak of poliomyelitis in Hispaniola associated with circulating Type 1 vaccine-derived poliovirus. Science 296(5566), 356-359 (2002).
105. OConnell CM, Ingalls RR, Andrews CW Jr, Scurlock AM, Darville T. Plasmid-deficient Chlamydia muridarum fail to induce immune pathology and protect against oviduct disease. J. Immunol. 179(6), 4027-4034 (2007).
106. Halford WP, Puschel R, Rakowski B. Herpes simplex virus 2 ICP0 mutant viruses are avirulent and immunogenic: implications for a genital herpes vaccine. PLoS One 5(8), e12251 (2010).
107. Halford WP, Puschel R, Gershburg E, Wilber A, Gershburg S, Rakowski B. A live-attenuated HSV-2 ICP0 virus elicits 10 to 100 times greater protection against genital herpes than a glycoprotein D subunit vaccine. PLoS One 6(3), e17748 (2011).
108. Yinon Y, Farine D, Yudin MH. Screening, diagnosis, and management of cytomegalovirus infection in pregnancy. Obstet. Gynecol. Surv. 65, 736-743 (2010).
109. Serranti D, Buonsenso D, Valentini PC. Congenital toxoplasmosis treatment. Eur. Rev. Med. Pharmacol. Sci. 15, 193-198 (2011).
110. Sha BE, Tierney C, Cohn SE et al. Postpartum viral load rebound in HIV-1-infected women treated with highly active antiretroviral therapy: AIDS clinical trials group protocol A5150. HIV Clin. Trials 12, 9-23 (2011).
111. Bardají A, Sigauque B, Sanz S et al. Impact of malaria at the end of pregnancy on infant mortality and morbidity. J. Infect. Dis. 203, 691-699 (2011).
112. Hannachi N, Marzouk M, Harrabi I et al. Seroprevalence of rubella virus, varicella zoster virus, cytomegalovirus and parvovirus B19 among pregnant women in the Sousse region, Tunisia. Bull. Soc. Pathol. Exot. 104, 62-67 (2011).
113. Vasilcan G, Avasiloaiei A, Moscalu M, Dimitriu AG, Stamatin M. Germ circulation in neonatal units-risk factors for maternal-foetal infection. Rev. Med. Chir. Soc. Med. Nat. Iasi. 114, 1028-1034 (2010).
114. Steer PJ, Plumb J. Myth: group B streptococcal infection in pregnancy: comprehended and conquered. Semin. Fetal Neonatal Med. 16(5), 254-258 (2011).
115. Darling EK, Mcdonald H. A meta-analysis of the efficacy of ocular prophylactic agents used for the prevention of gonococcal and chlamydial ophthalmia neonatorum. J. Midwifery Womens Health 55, 319-327 (2010).
116. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JFR, Petraglia F. Inflammation and pregnancy. Reprod. Sci. 16, 206-210 (2009).
117. Pararas MV, Skevaki CL, Kafetzis DA. Preterm birth due to maternal infection: causative pathogens and modes of prevention. Eur. J. Clin. Microbiol. Infect. Dis. 25, 562-569 (2006).
118. Guaschino S, De Seta F, Piccoli M, Maso G, Alberico S. Aetiology of preterm labour: bacterial vaginosis. BJOG 113, 46-51 (2006).
119. Kirchner L, Helmer H, Heinze G et al. Amnionitis with Ureaplasma urealyticum or other microbes leads to increased morbidity and prolonged hospitalization in very low birth weight infants. Eur. J. Obstet. Gynecol. Reprod. Biol. 134, 44-50 (2007).
120. Baud D, Goy G, Jaton K et al. Role of Chlamydia trachomatis in miscarriage. Emerg. Infect. Dis. 17, 1630-1635 (2011).
121. Nickerson CW. Gonorrhea amnionitis. Obstet. Gynecol. 42, 815-817 (1973).
122. Wheetman AP. Immunity, thyroid function and pregnancy: molecular mechanisms. Nat. Rev. Endocrin. 6, 311-318 (2010).
123. Al-Safi ZA, Shavell VI, Gonik B. Vaccination in pregnancy. Womens Health 7, 109-119 (2011).
124. Fox KA, Theiler R. Vaccination in pregnancy. Curr. Pharmaceut. Biotechnol. 12, 789-796 (2011).
125. Brent RL. Immunization of pregnant women: reproductive, medical and societal risks. Vaccine 21, 3413-3421 (2003).
126. Brent RL. Risks and benefits of immunizing pregnant women: the risk of doing nothing. Reproduct. Toxicol. 21, 383-389 (2006).
127. Gilbert-Barness E. Teratogenic causes of malformations. Ann. Clin. Lab. Sci. 40, 99-114 (2010).
128. Zhou X, Brotman RM, Gajer P et al. Recent advances in understanding the microbiology of the female reproductive tract and the causes of premature birth. Infect. Dis. Obstet. Gynecol. 2010, 737425 (2010).
129. Vrachnis N, Vitoratos N, Iliodromiti Z, Sifakis S, Deligeoroglou E, Creatsas G. Intrauterine inflammation and preterm delivery. Ann. NY Acad. Sci. 1205, 118-122 (2010).
130. Randis TM. Progress toward improved understanding of infection-related preterm birth. Clin. Perinatol. 37, 677-688 (2010).
131. Smith-Mccune K, Sawaya GF. Update on quadrivalent human papillomavirus vaccination and pregnancy outcomes: is contraception advisable? Obstet. Gynecol. Surv. 114, 1168-1169 (2009).
132. Desoye M, Gauster G, Wadsack C. Placental transport in pregnancy pathologies. Am. J. Clin. Nutr. doi:10.3945/ajcn.110.000851 (2011) (Epub ahead of print).
133. Pimentel MA. Vaccination during pregnancy. Acta Med. Port. 23, 837-840 (2010).
134. Badilla X, Morice A, Avila-Aguero ML et al. Fetal risk associated with rubella vaccination during pregnancy. Pediatr. Infect. Dis. J. 26, 830-835 (2007).
135. Jordan EK, Sever JL. Fetal damage caused by parvoviral infections. Reprod. Toxicol. 8, 161-168 (1994).
136. Wacholder S, Chen BE, Wilcox A et al. Risk of miscarriage with bivalent vaccine against human papillomavirus (HPV) Types 16 and 18: pooled analysis of two randomised controlled trials. BMJ 340, 712 (2010).
137. Lopes CR, Berezin EN, Ching TH, Canuto Jde S, Costa VO, Klering EM. Ineffectiveness for infants of immunization of mothers with pneumococcal capsular polysaccharide vaccine during pregnancy. Braz. J. Infect. Dis. 13(2), 104-106 (2009).
138. Witkin SS, Linhares IM, Bongiovanni AM, Herway C, Skupskia D. Unique alterations in infection-induced immune activation during pregnancy. BJOG 118, 145-153 (2010).
139. Wilkin T, Lee JY, Lensing SY et al. Safety and immunogenicity of the quadrivalent human papillomavirus vaccine in HIV-1-infected men. J. Infect. Dis. 202(8), 1246-1253 (2010).
140. Glenny AT, Pope CG, Waddington, H et al. Immunological notes. XVII-XXIV. J. Pathol. Bacteriol. 29(1), 31-40 (1926).
141. Ohagan DT, Ugozzoli M, Barackman J et al. Microparticles in MF59, a potent adjuvant combination for a recombinant protein vaccine against HIV-1. Vaccine 18(17), 1793-1801 (2000).
142. Gluck R. Adjuvant activity of immunopotentiating reconstituted influenza virosomes (IRIVs). Vaccine 17(13-14), 1782-1787 (1999).
143. Gluck U, Gebbers JO, Gluck R. Phase 1 evaluation of intranasal virosomal influenza vaccine with and without Escherichia coli heat-labile toxin in adult volunteers. J. Virol. 73(9), 7780-7786 (1999).
144. Herrera S, Fernandez OL, Vera O et al. Phase 1 safety and immunogenicity trial of Plasmodium vivax CS derived long synthetic peptides adjuvanted with montanide ISA 720 or montanide ISA 51. Am. J. Trop. Med. Hyg. 84(Suppl. 2), S12-S20 (2011).
145. Jahrsdorfer B, Weiner GJ. CpG oligodeoxynucleotides as immunotherapy in cancer. Update Cancer Ther. 3(1), 27-32 (2008).
146. Singh M, Carlson JR, Briones M et al. A comparison of biodegradable microparticles and MF59 as systemic adjuvants for recombinant gD from HSV-2. Vaccine 16(19), 1822-1827 (1998).
147. Valensi JP, Carlson JR, Van Nest GA. Systemic cytokine profiles in BALB/c mice immunized with trivalent influenza vaccine containing MF59 oil emulsion and other advanced adjuvants. J. Immunol. 153(9), 4029-4039 (1994).
148. Xu W, Liu J, Gong W, Chen J, Zhu S, Zhang L. Protective immunity against Chlamydia trachomatis genital infection induced by a vaccine based on the major outer membrane multi-epitope human papillomavirus major capsid protein L1. Vaccine 29, 2672-2678 (2011).
149. Diniz MO, Lasaro MO, Ertl HC, Ferreira LC. Immune responses and therapeutic antitumor effects of an experimental DNA vaccine encoding human papillomavirus type 16 oncoproteins genetically fused to herpesvirus glycoprotein D. Clin. Vacc. Immunol. 17, 1576-1583 (2010).
150. Ekong EE, Okenu DN, Mania-Pramanik J et al. A Vibrio cholerae ghost-based subunit vaccine induces cross-protective chlamydial immunity that is enhanced by CTA2B, the nontoxic derivative of cholera toxin. FEMS Immunol. Med. Microbiol. 55, 280-291 (2009).
151. Eko FO, Ekong E, HE Q, Black CM, Igietseme JU. Induction of immune memory by a multisubunit chlamydial vaccine. Vaccine 29, 1472-1480 (2011).
152. Fisseha M, Chen P, Brandt C, Kijek T, Moran E, Zollinger W. Characterisation of native outer membrane vesicles from lpxL mutant strains of Neisseria meningitidis for use in parenteral vaccination. Infect. Immun. 73, 4070-4080 (2005).
153. Barker CJ, Beagley KW, Hafner LM, Timms P. In silico identification and in vivo analysis of a novel T-cell antigen from Chlamydia, NrdB. Vaccine 26(10), 1285-1296 (2008).
154. World Health Organisation. The interagency list of essential medicines for reproductive health, 2006. www.who.int/reproductivehealth/ publications/general/RHR-2006-1/en/
155. VaxGen. VaxGen announces results of its Phase 3 HIV vaccine trial in Thailand: vaccine fails to meet endpoints. http://www2.prnewswire.com/cgi-bin/ stories.pl?ACCT=104&STORY=/www/story/11-12-2003/0002056633&EDATE
156. Key Concepts: economics of vaccine production. www.who.int/immunization- financing/ options/en/briefcase-vacproduction.pdf
157. The WHO: initiative for vaccine research (IVR). www.who.int/vaccine- research/diseases/ soa-std/en/index3.html
158. BioVex initiates Phase 1 clinical trial with its genital herpes vaccine, ImmunoVEXHSV2. www.medicalnewstoday.com/ releases/181424.php
159. Herpes vaccine fails clinical Trial. www.paidclinicaltrials.org/media/ herpes-vaccine-fails-clinical-trial
160. World Health Organisation department of HIV/AIDS Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections. www.who.int/docstore/hiv/GRSTI/003.html