Bacterial vaginosis - A microbiological and immunological enigma

APMIS

Volumn 113, Issue 2, 2005, Pages 81-90

  Forsum, Urban ^a,d   Holst, E ^b   Larsson, P G ^a   Vasquez, A ^b   Jakobsson, T ^a   Mattsby Baltzer, I ^c  

^a LINKÖPING UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d LINKÖPING UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Bacterial vaginosis; Ecology; Immune response; Lactobacilli; Nugent scoring; Taxonomy

Indexed keywords

AUTACOID; CYTOKINE; VIRULENCE FACTOR;

ANAEROBIC BACTERIUM; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE COURSE; HUMAN; IMMUNE RESPONSE; INFLAMMATION; LACTOBACILLUS; MICROBIOLOGICAL EXAMINATION; PATHOGENICITY; PRIORITY JOURNAL; REVIEW; VAGINA FLORA; VAGINITIS;

ANIMALS; BACTERIA, ANAEROBIC; FEMALE; HUMANS; LACTOBACILLUS; VAGINOSIS, BACTERIAL;

EID: 14844320009     PISSN: 09034641     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0463.2005.apm1130201.x     Document Type: Review

References (68)

1. Redondo-Lopez V, Cook RL, Sobel JD. Emerging role of lactobacilli in the control and maintenance of the vaginal bacterial microflora. Rev Infect Dis 1990;12:856-72.
2. Carlsson J, Gothefors L. Transmission of Lactobacillus jensenii and Lactobacillus acidophilus from mother to child at time of delivery. J Clin Microbiol 1975;1:124-8.
3. Giorgi A, Torriani S, Dellaglio F, Bo G, Stola E, Bernuzzi L. Identification of vaginal lactobacilli from asymptomatic women. Microbiologica 1987; 10:377-84.
4. Antonio MA, Hawes SE, Hillier SL. The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 1999;180:1950-6.
5. Song YL, Kato N, Matsumiya Y, Liu CX, Kato H, Watanabe K. Identification of and hydrogen peroxide production by fecal and vaginal lactobacilli isolated from Japanese women and newborn infants. J Clin Microbiol 1999;37:3062-4.
6. Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, Holmes KK. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 1983;74:14-22.
7. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:297-301.
8. Klein G, Pack A, Bonaparte C, Reuter G. Taxonomy and physiology of probiotic lactic acid bacteria. Int J Food Microbiol 1998;41:103-25.
9. Klaenhammer T, Altermann E, Arigoni F, Bolotin A, Breidt F, Broadbent J, et al. Discovering lactic acid bacteria by genomics. Antonie Van Leeuwenhoek 2002;82:29-58.
10. Woese CR. Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 2000;97:8392-6.
11. Kullen MJ, Sanozky-Dawes RB, Crowell DC, Klaenhammer TR. Use of the DNA sequence of variable regions of the 16S rRNA gene for rapid and accurate identification of bacteria in the Lacto bacillus acidophilus complex. J Appl Microbiol 2000;89:511-6.
12. Vásquez A, Ahrne S, Pettersson B, Molin G. Temporal temperature gradient gel electrophoresis (TTGE) as a tool for identification of Lactobacillus casei, Lactobacillus paracasei, Lactobacillus zeae and Lactobacillus rhamnosus. Lett Appl Microbiol 2001;32:215-9.
13. Vásquez A, Jakobsson T, Ahrne S, Forsum U, Molin G. Vaginal lactobacillus flora of healthy Swedish women. J Clin Microbiol 2002;40:2746-9.
14. Kilic AO, Pavlova SI, Alpay S, Kilic SS, Tao L. Comparative study of vaginal Lactobacillus phages isolated from women in the United States and Turkey: prevalence, morphology, host range, and DNA homology. Clin Diagn Lab Immunol 2001;8:31-9.
15. Pavlova SI, Kilic AO, Kilic SS, So JS, Nader-Macias ME, Simoes JA, et al. Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences. J Appl Microbiol 2002;92:451-9.
16. Tärnberg M, Jakobsson T, Jonasson J, Forsum U. Identification of randomly selected colonies of lactobacilli from normal vaginal fluid by pyrosequencing of the 16S rDNA variable V1 and V3 regions. APMIS 2002;110:802-10.
17. Jakobsson T, Forsum U. Vaginal laktobacillflora vid varierande östrogennivåer. Hygiea 2003;112: 234-5.
18. Gardner HL, Dukes CD. Haemophilus vaginalis vaginitis. A newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol 1955;69:962-76.
19. Krohn MA, Hillier S, Eschenbach D Comparisons of methods for diagnosing bacterial vaginosis among pregnant women. J Clin Microbiol 1989;27:1266-71.
20. Hoist E, Goffeng A, Andersch A. Bacterial vaginosis and vaginal microorganisms in idiopathic premature labor and association with pregnancy outcome. J Clin Microbiol 1994;32:176-86.
21. Hjelm E, Hallén A, Forsum U, Wallin J. Motile anaerobic curved rods in non-specific vaginitis. Eur J Sex Transm Dis 1982;1:9-14.
22. Hoist E, Skarin A, Mårdh PA. Characteristics of comma-shaped bacteria recovered from the female genital tract. Eur J Clin Microbiol 1982;1: 310-6.
23. Spiegel CA, Eschenbach D, Amsel R, Holmes KK. Curved anaerobic bacteria in bacterial (nonspecific) vaginosis and their response to antimicrobial therapy. J Infect Dis 1983;148:817-22.
24. Holst E, Wathne B, Hovelius B, Mårdh PA. Bacterial vaginosis: microbiological and clinical findings. Eur J Clin Microbiol 1987;6:536-41.
25. Hallén A, Påhlson C, Forsum U. Bacterial vaginosis in women attending STD clinic: diagnostic criteria and prevalence of Mobiluncus spp. Genitourin Med 1987;63:386-9.
26. Hillier SL, Critchlow CW, Stevens CE, Roberts MC, Wolner-Hanssen P, Eschenbach DA, Holmes KK. Microbiological, epidemiological and clinical correlates of vaginal colonisation by Mobiluncus species. Geniturin Med 1991;67:26-31.
27. Schwebke JR, Morgan SC, Hillier SL. Humoral antibody to Mobiluncus curtisii, a potential serological marker for bacterial vaginosis. Clin Diagn Lab Immunol 1996;3:567-9.
28. Keane FE, Thomas BJ, Gilroy CB, Renton A, Taylor-Robinson D. The association of Mycoplasma hominis, Ureaplasma urealyticum and Mycoplasma genitalium with bacterial vaginosis: observations on heterosexual women and their male partners. Int J STD AIDS 2000;11:356-60.
29. Cauci S, Driussi S, Monte R, Lanzafame P, Pitzus E, Quadrifoglio F. Immunoglobulin A response against Gardnerella vaginalis hemolysin and sialidase activity in bacterial vaginosis. Am J Obstet Gynecol 1998;178:511-5.
30. Cauci S, Hitti J, Noonan C, Agnew K, Quadrifoglio F, Hillier SL, Eschenbach DA. Vaginal hydrolytic enzymes, immunoglobulin A against Gardnerella vaginalis toxin, and risk of early preterm birth among women in preterm labor with bacterial vaginosis or intermediate flora. Am J Obstet Gynecol 2002;187:877-81.
31. Olmsted SS, Meyn LA, Rohan LC, Hillier SL. Glycosidase and proteinase activity of anaerobic gram-negative bacteria isolated from women with bacterial vaginosis. Sex Transm Dis 2003;30: 257-61.
32. Eiring P, Waller K, Widmann A, Werner H. Fibronectin and laminin binding of urogenital and oral prevotella species. Zentralbl Bakteriol 1998;288:361-72.
33. Mikamo H, Kawazoe K, Sato Y, Tamaya T. Elastase activity of anaerobes isolated from amniotic fluid with preterm premature rupture of membranes. Am J Obstet Gynecol 1999;180:378-80.
34. Hitti J, Hillier SL, Agnew KJ, Krohn MA, Reisner DP, Eschenbach DA. Vaginal indicators of amniotic fluid infection in preterm labor. Obstet Gynecol 2001;97:211-9.
35. Taylor-Robinson AW, Borriello SP, Taylor-Robinson D Identification and preliminary characterization of a cytotoxin isolated from Mobiluncus spp. Int J Exp Pathol 1993;74:357-66.
36. Pybus V, Onderdonk AB. Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella bivia involving ammonia: potential significance for bacterial vaginosis. J Infect Dis 1997;175:406-13.
37. Pybus V, Onderdonk AB. A commensal symbiosis between Prevotella bivia and Peptostreptococcus anaerobius involves amino acids: potential significance to the pathogenesis of bacterial vaginosis. FEMS Immunol Med Microbiol 1998; 22:317-27.
38. Press MF, Nousek-Goebl NA, Bur M, Greene GL. Estrogen receptor localization in the female genital tract. Am J Pathol 1986;123:280-92.
39. Kutteh WH, Moldoveanu Z, Mestecky J. Mucosal immunity in the female reproductive tract: correlation of immunoglobulins, cytokines, and reproductive hormones in human cervical mucus around the time of ovulation. AIDS Res Hum Retroviruses 1998;14(Suppl 1): S51-5.
40. Quayle AJ, Porter EM, Nussbaum AA, Wang YM, Brabec C, Yip KP, et al. Gene expression, immunolocalization, and secretion of human defensin-5 in human female reproductive tract. Am J Pathol 1998;152:1247-58.
41. Gipson IK, Moccia R, Spurr-Michaud S, Argueso P, Gargiulo AR, Hill JA 3rd, et al. The amount of MUC5B mucin in cervical mucus peaks at midcycle. J Clin Endocrinol Metab 2001;86:594-600.
42. Quayle AJ. The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J Reprod Immunol 2002;57:61-79.
43. Anderson D. Quantitation of mediators of inflammation and immunity in genital tract secretions and their relevance to HIV type 1 transmission. AIDS Res Hum Retroviruses 1998;14 (Suppl 1):S43.
44. Fichorova RN, Tucker LD, Anderson DJ. The molecular basis of nonoxynol-9-induced vaginal inflammation and its possible relevance to human immunodeficiency virus type 1 transmission. J Infect Dis 2001;184:418-28.
45. Milligan GN, Bourne N, Dudley KL. Role of polymorphonuclear leukocytes in resolution of HSV-2 infection of the mouse vagina. J Reprod Immunol 2001;49:49-65.
46. Cauci S, Guaschino S, De Aloysio D, Driussi S, De Santo D, Penacchioni P, et al. Interrelationships of interleukin-8 with interleukin-1 beta and neutrophils in vaginal fluid of healthy and bacterial vaginosis positive women. Mol Hum Reprod 2003;9:53-8.
47. Donders GG, Bosnians E, Dekeersmaecker A, Vereecken A, Van Bulck B, Spitz B. Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol 2000;182:872-8.
48. Donder GG, Vereecken A, Bosnians E, Dekeersmaecker A, Salembier G, Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. Br J Obstet Gynecol 2002;109:34-43.
49. Draper DL, Landers DV, Krohn MA, Hillier SL, Wiesenfeld HC, Heine RP Levels of vaginal secretory leukocyte protease inhibitor are decreased in women with lower reproductive tract infections. Am J Obstet Gynecol 2000;183:1243-8.
50. Fichorova RN, Cronin AO, Lien E, Anderson DJ, Ingalls RR Response to Neisseria gonorrhoeae by cervicovaginal epithelial cells occurs in the absence of toll-like receptor 4-mediated signaling. J Immunol 2002;168:2424-32.
51. Rock FL, Hardiman G, Timans JC, Kastelein RA, Bazan JF A family of human receptors structurally related to Drosophila Toll. Proc Natl Acad Sci USA 1998;95:588-93.
52. Medzhitov R, Preston-Hurlburt P, Janeway CA Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 1997;388:394-7.
53. Zhang G, Ghosh S. Toll-like receptor-mediated NFkB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest, 2001; 107:13-9.
54. Fichorova RN, Desai PJ, Gibson FC 3rd, Genco CA. Distinct proinflammatory host responses to Neisseria gonorrhoeae infection in immortalized human cervical and vaginal epithelial cells. Infect Immun 2001;69:5840-8.
55. Fichorova RN, Anderson DJ. Differential expression of immunobiological mediators by immortalized human cervical and vaginal epithelial cells. Biol Reprod 1999;60:508-14.
56. Steele C, Fidel P. Cytokine and chemokine production by human oral and vaginal epithelial cells in response to Candida albicans. Infect Immun 2002;70:577-83.
57. Platz-Christensen JJ, Mattsby-Baltzer I, Thomsen P, Wiqvist N. Endotoxin and interleukin-1 alpha in the cervical mucus and vaginal fluid of pregnant women with bacterial vaginosis. Am J Obstet Gynecol 1993;169:1161-6.
58. Wennerholm UB, Holm B, Mattsby-Baltzer I, Nielsen T, Platz-Christensen JJ, Sundell G, et al. Interleukin-1alpha, interleukin-6 and interleukin-8 in cervico/vaginal secretion for screening of preterm birth in twin gestation. Acta Obstet Gynecol Scand 1998;77:508-14.
59. Mattsby-Baltzer I, Platz-Christensen JJ, Hosseini N, Rosen P IL-1beta, IL-6, TNFalpha, fetal fibronectin, and endotoxin in the lower genital tract of pregnant women with bacterial vaginosis. Acta Obstet Gynecol Scand 1998;77:701-6.
60. Yudin MH, Landers DV, Meyn L, Hillier SL. Clinical and cervical cytokine response to treatment with oral or vaginal metronidazole for bacterial vaginosis during pregnancy: a randomized trial. Obstet Gynecol 2003;102:527-34.
61. Jacobsson B, Mattsby-Baltzer I, Andersch B, Bokstrom H, Holst RM, Wennerholm UB, et al. Microbial invasion and cytokine response in amniotic fluid in a Swedish population of women in preterm labor. Acta Obstet Gynecol Scand 2003; 82:120-8.
62. Holst RM, Mattsby-Baltzer I, Wennerholm UB, Hagberg H, Jacobsson B. Interleukin-6 and interleukin 8 in cervical fluid in a population of Swedish women in preterm labor: relationship to microbial invasion of the amniotic fluid, intra-amniotic inflammation and preterm delivery. Acta Obstet Gynecol Scand 2005. In press.
63. Dudley D. Pre-term labor: an intra-uterine inflammatory response syndrome. J Reprod Immunol 1997;36:93-109.
64. Rizzo G, Capponi A, Rinaldo D, Tedeschi D, Arduini D, Romanini C. Interleukin-6 concentrations in cervical secretions identify microbial invasion of the amniotic cavity in patients with preterm labor and intact membranes Am J Obstet Gynecol 1996;175:812-7.
65. Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, Han TR. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at the age of three years. Am J Obstet Gynecol 2000;182:675-81.
66. Simhan HN, Krohn MA, Roberts JM, Zeevi A, Caritis SN. Interleukin-6 promoter -174 polymorphism and spontaneous preterm birth. Am J Obstet Gynecol 2003;189:915-8.
67. Hoist, E. Reservoir of four organisms associated with bacterial vaginosis suggests lack of sexual transmission. J Clin Microbiol 1990;28:2035-9.
68. Hallén A, Påhlson C, Forsum U. Rectal occurrence of Mobiluncus species. Genitourin Med 1988;64:273-5. 91-98