Clinics in Dermatology
Volume 28, Issue 5 , Pages 539-545 , September 2010

Management of syphilis in the HIV-infected patient: Facts and controversies

  • David Farhi, MD

      Affiliations

    • Department of Dermatology and Venereology, Pavillon Tarnier, Hôpital Cochin, APHP, Université Paris V, 89 rue d'Assas, 75006 Paris, France
    • Corresponding Author InformationCorresponding author. Cabinet de dermatologie médicale et chirurgicale, 7 rue Coypel, 75013 Paris, France. Tel.: +33 1 42 17 07 37; fax: +33 1 58 41 28 95.
  • ,
  • Nicolas Dupin, MD

      Affiliations

    • Laboratoire de Recherche en Dermatologie. UPRES1833, Centre National de Reference de la Syphilis, Hôpital Cochin—Pavillon Gustave Roussy Université Paris V—Faculté de médecine, 89 rue d'Assas, 75006 Paris, France

References 

  1. Doherty L, Fenton KA, Jones J, et al. Syphilis: old problem, new strategy. BMJ. 2002;325:153–156
  2. Farhi D, Dupin N. Infections sexuellement transmissibles: syphilis, uréthrites et condylomes. In:  Bessis D editors. Paris: Masson; 2008;
  3. Lautenschlager S. Cutaneous manifestations of syphilis: recognition and management. Am J Clin Dermatol. 2006;7:291–304
  4. Zetola NM, Klausner JD. Syphilis and HIV infection: an update. Clin Infect Dis. 2007;44:1222–1228
  5. French P. Syphilis. BMJ. 2007;334:143–147
  6. Dupin N, Jdid R, N'Guyen YT, et al. Syphilis and gonorrhoea in Paris: the return. AIDS. 2001;15:814–815
  7. Chen SY, Gibson S, Katz MH, et al. Continuing increases in sexual risk behavior and sexually transmitted diseases among men who have sex with men: San Francisco, Calif, 1999-2001, USA. Am J Public Health. 2002;92:1387–1388
  8. Hourihan M, Wheeler H, Houghton R, et al. Lessons from the syphilis outbreak in homosexual men in east London. Sex Transm Infect. 2004;80:509–511
  9. Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis. 1992;19:61–77
  10. Golden MR, Marra CM, Holmes KK. Update on syphilis: resurgence of an old problem. JAMA. 2003;290:1510–1514
  11. Workowski KA, Berman SM. Sexually transmitted diseases treatment guidelines, 2006. MMWR Recomm Rep. 2006;55:1–94
  12. Dumortier C, Alcaraz I, Tone A, et al. Non-cutaneous manifestations of secondary syphilis. Ann Dermatol Venereol. 2008;135:451–458
  13. Health Protection Agency . Mapping the issues: HIV and other sexually transmitted infections in the United Kingdom. Available at: www.hpa.org.ul//web/HPAwebFile/HPAweb_C/1194947365435Accessed Feb 8, 2008
  14. Scheer S, Chu PL, Klausner JD, et al. Effect of highly active antiretroviral therapy on diagnoses of sexually transmitted diseases in people with AIDS. Lancet. 2001;357:432–435
  15. Belongia EA, Danila RN, Angamuthu V, et al. A population-based study of sexually transmitted disease incidence and risk factors in human immunodeficiency virus-infected people. Sex Transm Dis. 1997;24:251–256
  16. Chesson HW, Heffelfinger JD, Voigt RF, et al. Estimates of primary and secondary syphilis rates in persons with HIV in the United States, 2002. Sex Transm Dis. 2005;32:265–269
  17. Blocker ME, Levine WC, St Louis ME. HIV prevalence in patients with syphilis, United States. Sex Transm Dis. 2000;27:53–59
  18. Quinn TC, Cannon RO, Glasser D, et al. The association of syphilis with risk of human immunodeficiency virus infection in patients attending sexually transmitted disease clinics. Arch Intern Med. 1990;150:1297–1302
  19. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect. 1999;75:3–17
  20. Rottingen JA, Cameron DW, Garnett GP. A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: how much really is known?. Sex Transm Dis. 2001;28:579–597
  21. Cameron DW, Simonsen JN, D'Costa LJ, et al. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet. 1989;2:403–407
  22. Darrow WW, Echenberg DF, Jaffe HW, et al. Risk factors for human immunodeficiency virus (HIV) infections in homosexual men. Am J Public Health. 1987;77:479–483
  23. Gadkari DA, Quinn TC, Gangakhedkar RR, et al. HIV-1 DNA shedding in genital ulcers and its associated risk factors in Pune, India. J Acquir Immune Defic Syndr Hum Retrovirol. 1998;18:277–281
  24. Lafond RE, Lukehart SA. Biological basis for syphilis. Clin Microbiol Rev. 2006;19:29–49
  25. Theus SA, Harrich DA, Gaynor R, et al. Treponema pallidum, lipoproteins, and synthetic lipoprotein analogues induce human immunodeficiency virus type 1 gene expression in monocytes via NF-kappaB activation. J Infect Dis. 1998;177:941–950
  26. Sellati TJ, Wilkinson DA, Sheffield JS, et al. Virulent Treponema pallidum, lipoprotein, and synthetic lipopeptides induce CCR5 on human monocytes and enhance their susceptibility to infection by human immunodeficiency virus type 1. J Infect Dis. 2000;181:283–293
  27. Buchacz K, Patel P, Taylor M, et al. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS. 2004;18:2075–2079
  28. Kofoed K, Gerstoft J, Mathiesen LR, et al. Syphilis and human immunodeficiency virus (HIV)-1 coinfection: influence on CD4 T-cell count, HIV-1 viral load, and treatment response. Sex Transm Dis. 2006;33:143–148
  29. Flores JL. Syphilis. A tale of twisted treponemes. West J Med. 1995;163:552–559
  30. Ghanem KG, Moore RD, Rompalo AM, et al. Antiretroviral therapy is associated with reduced serologic failure rates for syphilis among HIV-infected patients. Clin Infect Dis. 2008;47:258–265
  31. Birnbaum NR, Goldschmidt RH, Buffett WO. Resolving the common clinical dilemmas of syphilis. Am Fam Phys 1999;59:2233-40, 45-6.
  32. Johns DR, Tierney M, Felsenstein D. Alteration in the natural history of neurosyphilis by concurrent infection with the human immunodeficiency virus. N Engl J Med. 1987;316:1569–1572
  33. Berry CD, Hooton TM, Collier AC, et al. Neurologic relapse after benzathine penicillin therapy for secondary syphilis in a patient with HIV infection. N Engl J Med. 1987;316:1587–1589
  34. Katz DA, Berger JR, Duncan RC. Neurosyphilis. A comparative study of the effects of infection with human immunodeficiency virus. Arch Neurol. 1993;50:243–249
  35. Gourevitch MN, Selwyn PA, Davenny K, et al. Effects of HIV infection on the serologic manifestations and response to treatment of syphilis in intravenous drug users. Ann Intern Med. 1993;118:350–355
  36. Hutchinson CM, Hook EW, Shepherd M, et al. Altered clinical presentation of early syphilis in patients with human immunodeficiency virus infection. Ann Intern Med. 1994;121:94–100
  37. Rompalo AM, Joesoef MR, O'Donnell JA, et al. Clinical manifestations of early syphilis by HIV status and gender: results of the syphilis and HIV study. Sex Transm Dis. 2001;28:158–165
  38. Rolfs RT, Joesoef MR, Hendershot EF, et al. A randomized trial of enhanced therapy for early syphilis in patients with and without human immunodeficiency virus infection. The Syphilis and HIV Study Group. N Engl J Med. 1997;337:307–314
  39. Chan DJ. Syphilis and HIV co-infection: when is lumbar puncture indicated?. Curr HIV Res. 2005;3:95–98
  40. Hook EW, Marra CM. Acquired syphilis in adults. N Engl J Med. 1992;326:1060–1069
  41. Berger JR. Neurosyphilis in human immunodeficiency virus type 1-seropositive individuals. A prospective study. Arch Neurol. 1991;48:700–702
  42. Katz DA, Berger JR. Neurosyphilis in acquired immunodeficiency syndrome. Arch Neurol. 1989;46:895–898
  43. Holtom PD, Larsen RA, Leal ME, et al. Prevalence of neurosyphilis in human immunodeficiency virus-infected patients with latent syphilis. Am J Med. 1992;93:9–12
  44. Lukehart SA, Hook EW, Baker-Zander SA, et al. Invasion of the central nervous system by Treponema pallidum: implications for diagnosis and treatment. Ann Intern Med. 1988;109:855–862
  45. Marra CM, Maxwell CL, Smith SL, et al. Cerebrospinal fluid abnormalities in patients with syphilis: association with clinical and laboratory features. J Infect Dis. 2004;189:369–376
  46. Marra CM, Maxwell CL, Tantalo L, et al. Normalization of cerebrospinal fluid abnormalities after neurosyphilis therapy: does HIV status matter?. Clin Infect Dis. 2004;38:1001–1006
  47. Ghanem KG, Moore RD, Rompalo AM, et al. Neurosyphilis in a clinical cohort of HIV-1-infected patients. AIDS. 2008;22:1145–1151
  48. Goh BT, van Voorst Vader PC. European guideline for the management of syphilis. Int J STD AIDS. 2001;12(suppl 3):14–26
  49. British Association for Sexual Health and HIV  Clinical Effectiveness Group. UK national guidelines on the management of syphilis 2008. 2008;Available at: http://www.bashh.org/documents/1771Accessed Feb 8, 2008
  50. Goh BT. Syphilis in adults. Sex Transm Infect. 2005;81:448–452
  51. Marshall DW, Brey RL, Butzin CA, et al. CSF changes in a longitudinal study of 124 neurologically normal HIV-1-infected U.S. Air Force personnel. J Acquir Immune Defic Syndr. 1991;4:777–781
  52. Collier AC, Marra C, Coombs RW, et al. Central nervous system manifestations in human immunodeficiency virus infection without AIDS. J Acquir Immune Defic Syndr. 1992;5:229–241
  53. Halperin LS. Neuroretinitis due to seronegative syphilis associated with human immunodeficiency virus. J Clin Neuroophthalmol. 1992;12:171–172
  54. Hicks CB, Benson PM, Lupton GP, et al. Seronegative secondary syphilis in a patient infected with the human immunodeficiency virus (HIV) with Kaposi sarcoma. A diagnostic dilemma. Ann Intern Med. 1987;107:492–495
  55. Terry PM, Page ML, Goldmeier D. Are serological tests of value in diagnosing and monitoring response to treatment of syphilis in patients infected with human immunodeficiency virus?. Genitourin Med. 1988;64:219–222
  56. Rompalo AM, Cannon RO, Quinn TC, et al. Association of biologic false-positive reactions for syphilis with human immunodeficiency virus infection. J Infect Dis. 1992;165:1124–1126
  57. Augenbraun MH, DeHovitz JA, Feldman J, et al. Biological false-positive syphilis test results for women infected with human immunodeficiency virus. Clin Infect Dis. 1994;19:1040–1044
  58. Jurado RL, Campbell J, Martin PD. Prozone phenomenon in secondary syphilis. Has its time arrived. Arch Intern Med. 1993;153:2496–2498
  59. Rusnak JM, Butzin C, McGlasson D, et al. False-positive rapid plasma reagin tests in human immunodeficiency virus infection and relationship to anti-cardiolipin antibody and serum immunoglobulin levels. J Infect Dis. 1994;169:1356–1359
  60. Goeman J, Kivuvu M, Nzila N, et al. Similar serological response to conventional therapy for syphilis among HIV-positive and HIV-negative women. Genitourin Med. 1995;71:275–279
  61. Browning DJ. Posterior segment manifestations of active ocular syphilis, their response to a neurosyphilis regimen of penicillin therapy, and the influence of human immunodeficiency virus status on response. Ophthalmology. 2000;107:2015–2023
  62. Long CM, Klausner JD, Leon S, et al. Syphilis treatment and HIV infection in a population-based study of persons at high risk for sexually transmitted disease/HIV infection in Lima, Peru. Sex Transm Dis. 2006;33:151–155
  63. Ghanem KG, Erbelding EJ, Wiener ZS, et al. Serological response to syphilis treatment in HIV-positive and HIV-negative patients attending sexually transmitted diseases clinics. Sex Transm Infect. 2007;83:97–101
  64. Telzak EE, Greenberg MS, Harrison J, et al. Syphilis treatment response in HIV-infected individuals. AIDS. 1991;5:591–595
  65. Yinnon AM, Coury-Doniger P, Polito R, et al. Serologic response to treatment of syphilis in patients with HIV infection. Arch Intern Med. 1996;156:321–325
  66. Malone JL, Wallace MR, Hendrick BB, et al. Syphilis and neurosyphilis in a human immunodeficiency virus type-1 seropositive population: evidence for frequent serologic relapse after therapy. Am J Med. 1995;99:55–63
  67. Walter T, Lebouche B, Miailhes P, et al. Symptomatic relapse of neurologic syphilis after benzathine penicillin G therapy for primary or secondary syphilis in HIV-infected patients. Clin Infect Dis. 2006;43:787–790
  68. Parkes R, Renton A, Meheus A, et al. Review of current evidence and comparison of guidelines for effective syphilis treatment in Europe. Int J STD AIDS. 2004;15:73–88
  69. Cohen CE, Winston A, Asboe D, et al. Increasing detection of asymptomatic syphilis in HIV patients. Sex Transm Infect. 2005;81:217–219

PII: S0738-081X(10)00036-2

doi: 10.1016/j.clindermatol.2010.03.012

Clinics in Dermatology
Volume 28, Issue 5 , Pages 539-545 , September 2010