The microbiological context of hiv resistance: Vaginal microbiota and mucosal inflammation at the viral point of entry

International Journal of Inflammation

Volumn 2012, Issue , 2012, Pages

  Schellenberg, John J ^a   Plummer, Francis A ^a,b,c  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Public Health Agency of Canada   (Canada)

^c UNIVERSITY OF NAIROBI   (Kenya)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ANTIGEN PRESENTING CELL; BACTERIAL COLONIZATION; BACTERIAL LOAD; CD8+ T LYMPHOCYTE; DISEASE PREDISPOSITION; HELPER CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; IMMUNOREGULATION; KENYA; LACTOBACILLUS; MICROBIAL COMMUNITY; MUCOSA INFLAMMATION; PHENOTYPE; PRIORITY JOURNAL; PROSTITUTION; REVIEW; RISK FACTOR; SEXUALLY TRANSMITTED DISEASE; SIGNAL TRANSDUCTION; VAGINA FLORA; VAGINITIS; VIRUS ENTRY; VIRUS RESISTANCE; VIRUS TRANSMISSION;

EID: 84872132005     PISSN: 20908040     EISSN: 20420099     Source Type: Journal    
DOI: 10.1155/2012/131243     Document Type: Review

References (74)

1. Gottlieb M. S., Schroff R., Schanker H. M., Pneumocystis carinii pneumonia and mucosal candidiasis in previously healthy homosexual men. Evidence of a new acquired cellular immunodeficiency. New England Journal of Medicine 1981 305 24 1425 1431 2-s2.0-0019782357 (Pubitemid 12240076)
2. Kreiss J. K., Koech D., Plummer F. A., AIDS virus infection in Nairobi prostitutes. Spread of the epidemic to East Africa. New England Journal of Medicine 1986 314 7 414 418 (Pubitemid 16161887)
3. Fowke K. R., Nagelkerke N. J. D., Kimani J., Simonsen J. N., Anzala A. O., Bwayo J. J., MacDonald K. S., Ngugi E. N., Plummer F. A., Resistance to HIV-1 infection among persistently seronegative prostitutes in Nairobi, Kenya. Lancet 1996 348 9038 1347 1351 2-s2.0-0030590749 10.1016/S0140-6736(95)12269-2 (Pubitemid 26383775)
4. Brenchley J. M., Douek D. C., The mucosal barrier and immune activation in HIV pathogenesis. Current Opinion in HIV and AIDS 2008 3 3 356 361 2-s2.0-42049095290 10.1097/COH.0b013e3282f9ae9c (Pubitemid 351521021)
5. Brenchley J. M., Price D. A., Douek D. C., HIV disease: fallout from a mucosal catastrophe? Nature Immunology 2006 7 3 235 239 2-s2.0-33645924682 10.1038/ni1316
6. Haase A. T., The pathogenesis of sexual mucosal transmission and early stages of infection: obstacles and a narrow window of opportunity for prevention. AIDS 2001 15, supplement 1 S10 S11 2-s2.0-0001968540
7. Haase A. T., Perils at mucosal front lines for HIV and SIV and their hosts. Nature Reviews Immunology 2005 5 10 783 792 2-s2.0-25844482131 10.1038/nri1706 (Pubitemid 41400852)
8. Peng B., Voltan R., Lim L., Edghill-Smith Y., Phogat S., Dimitrov D. S., Arora K., Leno M., Than S., Woodward R., Markham P. D., Cranage M., Robert-Guroff M., Rhesus macaque resistance to mucosal simian immunodeficiency virus infection is associated with a postentry block in viral replication. Journal of Virology 2002 76 12 6016 6026 2-s2.0-0036113509 10.1128/JVI.76.12. 6016-6026.2002 (Pubitemid 34556296)
9. Horton R. E., McLaren P. J., Fowke K., Kimani J., Ball T. B., Cohorts for the study of HIV-1-exposed but uninfected individuals: benefits and limitations. Journal of Infectious Diseases 2010 202 supplement 3 S377 S381 2-s2.0-78049423723 10.1086/655971
10. Marmor M., Hertzmark K., Thomas S. M., Halkitis P. N., Vogler M., Resistance to HIV Infection. Journal of Urban Health 2006 83 1 5 17 2-s2.0-33745054989 10.1007/s11524-005-9003-8 (Pubitemid 44337039)
11. Plummer F. A., Ball T. B., Kimani J., Fowke K. R., Resistance to HIV-1 infection among highly exposed sex workers in Nairobi: what mediates protection and why does it develop? Immunology Letters 1999 66 13 27 34 2-s2.0-0033046014 10.1016/S0165-2478(98)00182-5 (Pubitemid 29136815)
12. Kaul R., Rowland-Jones S. L., Kimani J., Dong T., Yang H. B., Kiama P., Rostron T., Njagi E., Bwayo J. J., MacDonald K. S., McMichael A. J., Plummer F. A., Late seroconversion in HIV-resistant Nairobi prostitutes despite pre-existing HIV-specific CD8+ responses. Journal of Clinical Investigation 2001 107 3 341 349 2-s2.0-0035134669 (Pubitemid 32157966)
13. Ball T. B., Ji H., Kimani J., McLaren P., Marlin C., Hill A. V. S., Plummer F. A., Polymorphisms in IRF-1 associated with resistance to HIV-1 infection in highly exposed uninfected Kenyan sex workers. AIDS 2007 21 9 1091 1101 2-s2.0-34248531947 10.1097/QAD.0b013e3280ef6ae1 (Pubitemid 46763279)
14. McLaren P. J., B. Ball T., Wachihi C., Jaoko W., Kelvin D. J., Danesh A., Kimani J., Plummer F. A., Fowke K. R., HIV-exposed seronegative commercial sex workers show a quiescent phenotype in the CD4+ T cell compartment and reduced expression of HIV-dependent host factors. Journal of Infectious Diseases 2010 202 3 S339 S344 2-s2.0-78049448608 10.1086/655968
15. + Regulatory T Cells. Journal of Infectious Diseases 2009 199 9 1318 1322 2-s2.0-65649106139 10.1086/597801
16. Iqbal S. M., Ball T. B., Levinson P., Maranan L., Jaoko W., Wachihi C., Pak B. J., Podust V. N., Broliden K., Hirbod T., Kaul R., Plummer F. A., Elevated elafin/trappin-2 in the female genital tract is associated with protection against HIV acquisition. AIDS 2009 23 13 1669 1677 2-s2.0-69449092614 10.1097/QAD.0b013e32832ea643
17. Ghosh M., Shen Z., Fahey J. V., Cu-Uvin S., Mayer K., Wira C. R., Trappin-2/Elafin: a novel innate anti-human immunodeficiency virus-1 molecule of the human female reproductive tract. Immunology 2010 129 2 207 219 2-s2.0-73949143527 10.1111/j.1365-2567.2009.03165.x
18. Burgener A., Boutilier J., Wachihi C., Kimani J., Carpenter M., Westmacott G., Cheng K., Ball T. B., Plummer F., Identification of differentially expressed proteins in the cervical mucosa of HIV-1-resistant sex workers. Journal of Proteome Research 2008 7 10 4446 4454 2-s2.0-55949121329 10.1021/pr800406r
19. Hladik F., McElrath M. J., Setting the stage: host invasion by HIV. Nature Reviews Immunology 2008 8 6 447 457 2-s2.0-44349159423 10.1038/nri2302 (Pubitemid 351735878)
20. Wilson M., Microbial Inhabitants of Humans: Their Ecology and Role in Health and Disease 2005 Cambridge, UK Cambridge University Press
21. Olmsted S. S., Khanna K. V., Ng E. M., Whitten S. T., Johnson O. N., Markham R. B., Cone R. A., Moench T. R., Low pH immobilizes and kills human leukocytes and prevents transmission of cell-associated HIV in a mouse model. BMC Infectious Diseases 2005 5, article no. 79 2-s2.0-27644435540 10.1186/1471-2334-5-79 (Pubitemid 41554910)
22. Levy J. A., HIV pathogenesis: 25 years of progress and persistent challenges. AIDS 2009 23 2 147 160 2-s2.0-59049094482 10.1097/QAD. 0b013e3283217f9f
23. Pudney J., Quayle A. J., Anderson D. J., Immunological microenvironments in the human vagina and cervix: mediators of cellular immunity are concentrated in the cervical transformation zone. Biology of Reproduction 2005 73 6 1253 1263 2-s2.0-28144449069 10.1095/biolreprod.105.043133 (Pubitemid 41698616)
24. Furuta Y., Eriksson K., Svennerholm B., Fredman P., Horal P., Jeansson S., Vahlne A., Holmgren J., Czerkinsky C., Infection of vaginal and colonic epithelial cells by the human immunodeficiency virus type 1 is neutralized by antibodies raised against conserved epitopes in the envelope glycoprotein gp120. Proceedings of the National Academy of Sciences of the United States of America 1994 91 26 12559 12563 2-s2.0-0028596516 10.1073/pnas.91.26.12559
25. Zheng J., Xie Y., Campbell R., Song J., Wang R. Q., Chiu R., Berenson J., Razi M., Massachi S., Yang O. O., Chen I. S. Y., Pang S., gp120-independent HIV infection of cells derived from the female reproductive tract, brain, and colon. Journal of Acquired Immune Deficiency Syndromes 2006 43 2 127 136 2-s2.0-33748999991 10.1097/01.qai.0000228149.17669.08 (Pubitemid 44454805)
26. De Jong M. A. W. P., Geijtenbeek T. B. H., Human immunodeficiency virus-1 acquisition in genital mucosa: langerhans cells as key-players. Journal of Internal Medicine 2009 265 1 18 28 2-s2.0-57449084696 10.1111/j.1365-2796.2008. 02046.x
27. Kaul R., Pettengell C., Sheth P. M., Sunderji S., Biringer A., MacDonald K., Walmsley S., Rebbapragada A., The genital tract immune milieu: an important determinant of HIV susceptibility and secondary transmission. Journal of Reproductive Immunology 2008 77 1 32 40 2-s2.0-38149074165 10.1016/j.jri.2007. 02.002
28. Douek D. C., Roederer M., Koup R. A., Emerging concepts in the immunopathogenesis of AIDS. Annual Review of Medicine 2009 60 471 484 2-s2.0-63449124466 10.1146/annurev.med.60.041807.123549
29. Brenchley J. M., Price D. A., Schacker T. W., Asher T. E., Silvestri G., Rao S., Kazzaz Z., Bornstein E., Lambotte O., Altmann D., Blazar B. R., Rodriguez B., Teixeira-Johnson L., Landay A., Martin J. N., Hecht F. M., Picker L. J., Lederman M. M., Deeks S. G., Douek D. C., Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nature Medicine 2006 12 12 1365 1371 2-s2.0-33845532053 10.1038/nm1511 (Pubitemid 44924494)
30. Liovat A. S., Jacquelin B., Ploquin M. J., Barré-Sinoussi F., Müller-Trutwin M. C., African non human primates infected by SIVwhy don't they get sick? Lessons from studies on the early phase of non-pathogenic SIV infection. Current HIV Research 2009 7 1 39 50 2-s2.0-59649097925 10.2174/157016209787048546
31. Pandrea I., Sodora D. L., Silvestri G., Apetrei C., Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends in Immunology 2008 29 9 419 428 2-s2.0-49849088558 10.1016/j.it.2008.05.004
32. Kornfeld C., Ploquin M. J. Y., Pandrea I., Faye A., Onanga R., Apetrei C., Poaty-Mavoungou V., Rouquet P., Estaquier J., Mortara L., Desoutter J. -F., Butor C., Le Grand R., Roques P., Simon F., Barré-Sinoussi F., Diop O. M., Müller-Trutwin M. C., mmuller@pasteur.fr Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. Journal of Clinical Investigation 2005 115 4 1082 1091 10.1172/JCI200523006 (Pubitemid 40489413)
33. Favre D., Lederer S., Kanwar B., Ma Z. M., Proll S., Kasakow Z., Mold J., Swainson L., Barbour J. D., Baskin C. R., Palermo R., Pandrea I., Miller C. J., Katze M. G., McCune J. M., Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathogens 2009 5 2 2-s2.0-61449115882 10.1371/journal.ppat.1000295 e1000295
34. Brenchley J. M., Paiardini M., Knox K. S., Asher A. I., Cervasi B., Asher T. E., Scheinberg P., Price D. A., Hage C. A., Kholi L. M., Khoruts A., Frank I., Else J., Schacker T., Silvestri G., Douek D. C., Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008 112 7 2826 2835 2-s2.0-53449093632 10.1182/blood-2008-05-159301
35. Acosta-Rodriguez E. V., Napolitani G., Lanzavecchia A., Sallusto F., Interleukins 1 β and 6 but not transforming growth factor- β are essential for the differentiation of interleukin 17-producing human T helper cells. Nature Immunology 2007 8 9 942 949 2-s2.0-34548125305 10.1038/ni1496 (Pubitemid 47300008)
36. + memory T cells harbor most Th-17 cells and are preferentially infected during acute SIV infection. Mucosal Immunology 2009 2 5 439 449 2-s2.0-69249153068 10.1038/mi.2009.90
37. Bernstein K. T., kyle.bernstein@sfdph.org Marcus J. L., Nieri G., Philip S. S., Klausner J. D., Rectal gonorrhea and chlamydia reinfection is associated with increased risk of HIV seroconversion. Journal of Acquired Immune Deficiency Syndromes 2010 53 4 537 543 10.1097/QAI.0b013e3181c3ef29
38. Fleming D. T., Wasserheit J. N., From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sexually Transmitted Infections 1999 75 1 3 17 2-s2.0-0033017798 (Pubitemid 29117474)
39. T. Kane C., Diawara S., Ndiaye H. D., Diallo P. A. N., Wade A. S., Diallo A. G., Belec L., Mboup S., Concentrated and linked epidemics of both HSV-2 and HIV-1/HIV-2 infections in Senegal: public health impacts of the spread of HIV. International Journal of STD and AIDS 2009 20 11 793 796 2-s2.0-73949089028 10.1258/ijsa.2008.008414
40. Shafir S. C., sshaflr@ucla.edu Sorvillo F. J., Smith L., Current issues and considerations regarding trichomoniasis and human immunodeficiency virus in African-Americans. Clinical Microbiology Reviews 2009 22 1 37 45 10.1128/CMR.00002-08
41. Larsson P. G., Bergström M., Forsum U., Jacobsson B., Strand A., Wölner-Hanssen P., Bacterial vaginosis transmission, role in genital tract infection and pregnancy outcome: an enigma. APMIS 2005 113 4 233 245 2-s2.0-18744400231 10.1111/j.1600-0463.2005.apm01.x (Pubitemid 40676804)
42. Westrom L., Evaldson G., K. Holmes K., Taxonomy of vaginosis: bacterial vaginosisa definition. Scandinavian Journal of Urology and Nephrology Supplement 1984 86 259 264
43. Atashili J., Poole C., Ndumbe P. M., Adimora A. A., Smith J. S., Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS 2008 22 12 1493 1501 2-s2.0-49849099241 10.1097/QAD.0b013e3283021a37
44. Forsum U., Hallén A., Larsson P. G., Bacterial vaginosisa laboratory and clinical diagnostics enigma: review article II. APMIS 2005 113 3 153 161 2-s2.0-17144429636 10.1111/j.1600-0463.2005.apm1130301.x (Pubitemid 40524098)
45. Forsum U., Holst E., Larsson P. G., Vasquez A., Jakobsson T., Mattsby-Baltzer I., Bacterial vaginosisa microbiological and immunological enigma. APMIS 2005 113 2 81 90 2-s2.0-14844320009 10.1111/j.1600-0463.2005. apm1130201.x (Pubitemid 40343577)
46. Amsel R., Totten P. A., Spiegel C. A., Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. American Journal of Medicine 1983 74 1 14 22 2-s2.0-0020665888 (Pubitemid 13221599)
47. Nugent R. P., Krohn M. A., Hillier S. L., Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. Journal of Clinical Microbiology 1991 29 2 297 301 2-s2.0-0026088584
48. Thorsen P., Jensen I. P., Jeune B., Ebbesen N., Arpi M., Bremmelgaard A., Moller B. R., Few microorganisms associated with bacterial vaginosis may constitute the pathologic core: a population-based microbiologic study among 3596 pregnant women. American Journal of Obstetrics and Gynecology 1998 178 3 580 587 2-s2.0-0031980368 10.1016/S0002-9378(98)70442-9 (Pubitemid 28207514)
49. Huth E. J., Style notes: bacterial vaginosis or vaginal bacteriosis? Annals of Internal Medicine 1989 111 7 553 554 2-s2.0-0024358952 (Pubitemid 19244554)
50. Losikoff P., Fichorova R., Snyder B., Rodriguez I., Cu-Uvin S., Harwell J., Mayer K. H., Genital tract interleukin-8 but not interleukin-1 β or interleukin-6 concentration is associated with bacterial vaginosis and its clearance in HIV-infected and HIV-uninfected women. Infectious Diseases in Obstetrics and Gynecology 2007 2007 6 2-s2.0-36249031500 10.1155/2007/92307 92307 (Pubitemid 350134983)
51. Mares D., Simoes J. A., Novak R. M., Spear G. T., TLR2-mediated cell stimulation in bacterial vaginosis. Journal of Reproductive Immunology 2008 77 1 91 99 2-s2.0-38149073388 10.1016/j.jri.2007.04.004
52. Mitchell C. M., Balkus J., Agnew K. J., Cohn S., Luque A., Lawler R., Coombs R. W., Hitti J. E., Bacterial vaginosis, not HIV, is primarily responsible for increased vaginal concentrations of proinflammatory cytokines. AIDS Research and Human Retroviruses 2008 24 5 667 671 2-s2.0-44349092065 10.1089/aid.2008.0268 (Pubitemid 351748782)
53. Roberton A. M., Wiggins R., Horner P. J., Greenwood R., Crowley T., Fernandes A., Berry M., Corfield A. P., A novel bacterial mucinase, glycosulfatase, is associated with bacterial vaginosis. Journal of Clinical Microbiology 2005 43 11 5504 5508 2-s2.0-27744606928 10.1128/JCM.43.11.5504- 5508.2005 (Pubitemid 41612321)
54. Pybus V., Onderdonk A. B., Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella bivia involving ammonia: potential significance for bacterial vaginosis. Journal of Infectious Diseases 1997 175 2 406 413 2-s2.0-0031016837 (Pubitemid 27052247)
55. Cauci S., Guaschino S., Driussi S., De Santo D., Lanzafame P., Quadrifoglio F., Correlation of local interleukin-8 with immunoglobulin A against Gardnerella vaginalis hemolysin and with prolidase and sialidase levels in women with bacterial vaginosis. Journal of Infectious Diseases 2002 185 11 1614 1620 2-s2.0-0036605510 10.1086/340417 (Pubitemid 34587523)
56. Hay P., Life in the littoral zone: lactobacilli losing the plot. Sexually Transmitted Infections 2005 81 2 100 102 2-s2.0-17144378227 10.1136/sti.2003.007161 (Pubitemid 40523817)
57. Anukam K. C., Osazuwa E. O., Ahonkhai I., Reid G., Lactobacillus vaginal microbiota of women attending a reproductive health care service in Benin City, Nigeria. Sexually Transmitted Diseases 2006 33 1 59 62 2-s2.0-29944447546 10.1097/01.olq.0000175367.15559.c4 (Pubitemid 43042823)
58. Hillier S. L., The vaginal microbial ecosystem and resistance to HIV. AIDS Research and Human Retroviruses 1998 14 supplement 1 S17 S21 2-s2.0-0031970450 (Pubitemid 28208884)
59. Boskey E. R., Cone R. A., Whaley K. J., Moench T. R., Origins of vaginal acidity: high D/L lactate ratio is consistent with bacteria being the primary source. Human Reproduction 2001 16 9 1809 1813 2-s2.0-0034817210 (Pubitemid 32916204)
60. Boskey E. R., Telsch K. M., Whaley K. J., Moench T. R., Cone R. A., Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infection and Immunity 1999 67 10 5170 5175 2-s2.0-0032879164 (Pubitemid 29455288)
61. Daniel Johannes Rönnqvist P., daniel.ronnqvist@essum.se Birgitta Forsgren-Brusk U., Elisabeth Grahn-Håkansson E., Lactobacilli in the female genital tract in relation to other genital microbes and vaginal pH. Acta Obstetricia et Gynecologica Scandinavica 2006 85 6 726 735 10.1080/ 00016340600578357 (Pubitemid 43995054)
62. Klebanoff S. J., Coombs R. W., Viricidal effect of Lactobacillus acidophilus on human immunodeficiency virus type 1: possible role in heterosexual transmission. Journal of Experimental Medicine 1991 174 1 289 292 2-s2.0-0025847568
63. Fontaine E. A., Taylor-Robinson D., Comparison of quantitative and qualitative methods of detecting hydrogen peroxide produced by human vaginal strains of lactobacilli. Journal of Applied Bacteriology 1990 69 3 326 331 2-s2.0-0025039231 (Pubitemid 20329544)
64. Tao L., Pavlova S., Anzinger J., Carlson S., Jacobs A., Caffrey M., Spear G., Fighting HIV with its natural enemy: mannose-specific capture of HIV by Lactobacillus. Beneficial Microbes Conference, Poster Abstract #5B, 2005
65. Buffa V., Stieh D., Mamhood N., Hu Q., Fletcher P., Shattock R. J., Cyanovirin-N potently inhibits human immunodeficiency virus type 1 infection in cellular and cervical explant models. Journal of General Virology 2009 90 1 234 243 2-s2.0-59849088564 10.1099/vir.0.004358-0
66. O'Keefe B. R., Vojdani F., Buffa V., Shattock R. J., Montefiori D. C., Bakke J., Mirsalis J., d'Andrea A. L., Hume S. D., Bratcher B., Saucedo C. J., McMahon J. B., Pogue G. P., Palmer K. E., Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proceedings of the National Academy of Sciences of the United States of America 2009 106 15 6099 6104 2-s2.0-65549099593 10.1073/pnas.0901506106
67. Marrazzo J. M., Wiesenfeld H. C., Murray P. J., Busse B., Meyn L., Krohn M., Hillier S. L., Risk factors for cervicitis among women with bacterial vaginosis. Journal of Infectious Diseases 2006 193 5 617 624 2-s2.0-33144486287 10.1086/500149 (Pubitemid 43271495)
68. Braat H., van den Brande J., Van Tol E., Hommes D., Peppelenbosch M., Van Deventer S., Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. American Journal of Clinical Nutrition 2004 80 6 1618 1625 2-s2.0-16544392923 (Pubitemid 41103862)
69. Lin P. W., Myers L. E. S., Ray L., Song S. C., Nasr T. R., Berardinelli A. J., Kundu K., Murthy N., Hansen J. M., Neish A. S., Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation. Free Radical Biology and Medicine 2009 47 8 1205 1211 2-s2.0-70249132476 10.1016/j.freeradbiomed.2009.07.033
70. Tien M. T., Girardin S. E., Regnault B., Le Bourhis L., Dillies M. -A., Coppée J. -Y., B'Ourdet-Sicard R., Sansonetti P. J., psanson@pasteur.fr Pédron T., Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. Journal of Immunology 2006 176 2 1228 1237 (Pubitemid 43099727)
71. Schellenberg J. J., schellej@cc.umanitoba.ca Card C. M., Ball T. B., Mungai J. N., Irungu E., Kimani J., Jaoko W., Wachihi C., Fowke K. R., Plummer F. A., Bacterial vaginosis, HIV serostatus and T-cell subset distribution in a cohort of East African commercial sex workers: retrospective analysis. AIDS 2012 26 3 387 393 10.1097/QAD.0b013e32834ed7f0
72. Schellenberg J. J., schellej@cc.umanitoba.ca Links M. G., Hill J. E., Dumonceaux T. J., Kimani J., Jaoko W., Wachihi C., Mungai J. N., Peters G. A., Tyler S., Graham M., Severini A., Fowke K. R., Ball T. B., Plummer F. A., Molecular definition of vaginal microbiota in east african commercial sex workers. Applied and Environmental Microbiology 2011 77 12 4066 4074 10.1128/AEM.02943-10
73. Hummelen R., Vos A. P., Van'T Land B., Van Norren K., Reid G., Altered host-microbe interaction in HIV: a target for intervention with pro- and prebiotics. International Reviews of Immunology 2010 29 5 485 513 2-s2.0-77956671143 10.3109/08830185.2010.505310
74. McGowan I., imcgowan@pitt.edu Microbicides for HIV prevention: reality or hope? Current Opinion in Infectious Diseases 2010 23 1 26 31 10.1097/QCO.0b013e328334fe70