Secondary buruli ulcer skin lesions emerging several months after completion of chemotherapy: Paradoxical reaction or evidence for immune protection?

PLoS Neglected Tropical Diseases

Volumn 5, Issue 8, 2011, Pages

  Ruf, Marie Thérèse ^a,b   Chauty, Annick ^c,d   Adeye, Ambroise ^c,d   Ardant, Marie Françoise ^c,d   Koussemou, Hugues ^c,d   Johnson, Roch Christian ^d   Pluschke, Gerd ^a,b  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c Centre de Diagnostic et de Traitement de l'ulcère de Buruli Fondation Raoul Follereau   (Benin)

^d Fondation Raoul Follereau ^*  (Benin)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; MYCOLACTONE; RIFAMPICIN; STREPTOMYCIN; UNCLASSIFIED DRUG; LEUKOCYTE ANTIGEN; TUBERCULOSTATIC AGENT;

ACID FAST BACTERIUM; ANTIBIOTIC THERAPY; ARTICLE; B LYMPHOCYTE; BURULI ULCER; CASE REPORT; CELL INFILTRATION; CHILD; DEBRIDEMENT; DISEASE ASSOCIATION; DRUG EFFICACY; EXCISION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LEUKOCYTE; MALE; MYCOBACTERIUM ULCERANS; PARADOXICAL DRUG REACTION; PRESCHOOL CHILD; SKIN DEFECT; SKIN NODULE; SKIN TRANSPLANTATION; TISSUE NECROSIS; TREATMENT DURATION; ULCER HEALING; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; NECROSIS; NEGLECTED DISEASE; PATHOLOGY; SKIN; TREATMENT OUTCOME;

ANTIBIOTICS, ANTITUBERCULAR; ANTIGENS, CD; BURULI ULCER; CHILD; HUMANS; IMMUNOHISTOCHEMISTRY; LEUKOCYTES; MALE; MYCOBACTERIUM ULCERANS; NECROSIS; NEGLECTED DISEASES; RIFAMPIN; SKIN; STREPTOMYCIN; TREATMENT OUTCOME;

EID: 80052402896     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001252     Document Type: Article

References (59)

1. Evans MR, Thangaraj HS, Wansbrough-Jones MH, (2000) Buruli ulcer. Curr Opin Infect Dis 13: 109-112.
2. Johnson PDR, Stinear T, Small PLC, Pluschke G, Merritt RW, et al. (2005) Buruli ulcer (M. ulcerans infection): new insights, new hope for disease control. PLoS Med 2: e108 doi:10.1371/journal.pmed.0020108.
3. Walsh DS, Portaels F, Meyers WM, (2008) Buruli ulcer (Mycobacterium ulcerans infection). Trans R Soc Trop Med Hyg 102: 969-978 doi:10.1016/j.trstmh.2008.06.006.
4. Asiedu K, Scherpbier, R, Raviglione, M, (2000) Buruli ulcer: Mycobacterium ulcerans infection. Geneva World Health Organization.
5. Rondini S, Horsfield C, Mensah-Quainoo E, Junghanss T, Lucas S, et al. (2006) Contiguous spread of Mycobacterium ulcerans in Buruli ulcer lesions analysed by histopathology and real-time PCR quantification of mycobacterial DNA. The Journal of Pathology 208: 119-128.
6. Hayman J, McQueen A, (1985) The pathology of Mycobacterium ulcerans infection. Pathology 17: 594-600.
7. Adusumilli S, Mve-Obiang A, Sparer T, Meyers W, Hayman J, et al. (2005) Mycobacterium ulcerans toxic macrolide, mycolactone modulates the host immune response and cellular location of M. ulcerans in vitro and in vivo. Cell. Microbiol 7: 1295-1304 doi:10.1111/j.1462-5822.2005.00557.x.
8. George KM, Chatterjee D, Gunawardana G, Welty D, Hayman J, et al. (1999) Mycolactone: a polyketide toxin from Mycobacterium ulcerans required for virulence. Science 283: 854-857.
9. Snyder DS, Small PLC, (2003) Uptake and cellular actions of mycolactone, a virulence determinant for Mycobacterium ulcerans. Microb. Pathog 34: 91-101.
10. Bozzo C, Tiberio R, Graziola F, Pertusi G, Valente G, et al. (2010) A Mycobacterium ulcerans toxin, mycolactone, induces apoptosis in primary human keratinocytes and in HaCaT cells. Microbes Infect doi:10.1016/j.micinf.2010.08.005.
11. Coutanceau E, Marsollier L, Brosch R, Perret E, Goossens P, et al. (2005) Modulation of the host immune response by a transient intracellular stage of Mycobacterium ulcerans: the contribution of endogenous mycolactone toxin. Cell. Microbiol 7: 1187-1196 doi:10.1111/j.1462-5822.2005.00546.x.
12. Torrado E, Fraga AG, Castro AG, Stragier P, Meyers WM, et al. (2007) Evidence for an intramacrophage growth phase of Mycobacterium ulcerans. Infect. Immun 75: 977-987 doi:10.1128/IAI.00889-06.
13. Amofah G, Bonsu F, Tetteh C, Okrah J, Asamoa K, et al. (2002) Buruli ulcer in Ghana: results of a national case search. Emerging Infect Dis 8: 167-170.
14. Debacker M, Aguiar J, Steunou C, Zinsou C, Meyers WM, et al. (2004) Mycobacterium ulcerans disease: role of age and gender in incidence and morbidity. Trop Med Int Health 9: 1297-1304 doi:10.1111/j.1365-3156.2004.01339.x.
15. Eddyani M, Portaels F, (2007) Survival of Mycobacterium ulcerans at 37 degrees C. Clin Microbiol Infect 13: 1033-1035 doi:10.1111/j.1469-0691.2007.01791.x.
16. Fyfe JAM, Lavender CJ, Johnson PDR, Globan M, Sievers A, et al. (2007) Development and application of two multiplex real-time PCR assays for the detection of Mycobacterium ulcerans in clinical and environmental samples. Appl Environ Microbiol 73: 4733-4740 doi:10.1128/AEM.02971-06.
17. Stienstra Y, van der Werf TS, Guarner J, Raghunathan PL, Spotts Whitney EA, et al. (2003) Analysis of an IS2404-based nested PCR for diagnosis of Buruli ulcer disease in regions of Ghana where the disease is endemic. J Clin Microbiol 41: 794-797.
18. Phillips RO, Sarfo FS, Osei-Sarpong F, Boateng A, Tetteh I, et al. (2009) Sensitivity of PCR targeting Mycobacterium ulcerans by use of fine-needle aspirates for diagnosis of Buruli ulcer. J Clin Microbiol 47: 924-926 doi:10.1128/JCM.01842-08.
19. Eddyani M, Debacker M, Martin A, Aguiar J, Johnson CR, et al. (2008) Primary culture of Mycobacterium ulcerans from human tissue specimens after storage in semisolid transport medium. J Clin Microbiol 46: 69-72 doi:10.1128/JCM.00301-07.
20. Schütte D, Um-Boock A, Mensah-Quainoo E, Itin P, Schmid P, et al. (2007) Development of highly organized lymphoid structures in Buruli ulcer lesions after treatment with rifampicin and streptomycin. PLoS Negl Trop Dis 1: e2 doi:10.1371/journal.pntd.0000002.
21. Hayman J, (1993) Out of Africa: observations on the histopathology of Mycobacterium ulcerans infection. J Clin Pathol 46: 5-9.
22. Guarner J, Bartlett J, Whitney EAS, Raghunathan PL, Stienstra Y, et al. (2003) Histopathologic features of Mycobacterium ulcerans infection. Emerging Infect Dis 9: 651-656.
23. Radford AJ, (2009) The surgical management of lesions of ulcerans infections due to Mycobacterium ulcerans, revisited. Transactions of the Royal Society of Tropical Medicine and Hygiene 103: 981-984 doi:10.1016/j.trstmh.2009.04.009.
24. Sizaire V, Nackers F, Comte E, Portaels F, (2006) Mycobacterium ulcerans infection: control, diagnosis, and treatment. Lancet Infect Dis 6: 288-296 doi:10.1016/S1473-3099(06)70464-9.
25. Etuaful S, Carbonnelle B, Grosset J, Lucas S, Horsfield C, et al. (2005) Efficacy of the combination rifampin-streptomycin in preventing growth of Mycobacterium ulcerans in early lesions of Buruli ulcer in humans. Antimicrob. Agents Chemother 49: 3182-3186 doi:10.1128/AAC.49.8.3182-3186.2005.
26. World Health organisation. (2004) Provisional guidance on the role of specific antibiotics in the managment of Mycobacterium ulcerans disease. Geneva.
27. Chauty A, Ardant M, Adeye A, Euverte H, Guedenon A, et al. (2007) Promising Clinical Efficacy of Streptomycin-Rifampin Combination for Treatment of Buruli Ulcer (Mycobacterium ulcerans Disease). Antimicrob. Agents Chemother 51: 4029-4035.
28. Nienhuis WA, Stienstra Y, Thompson WA, Awuah PC, Abass KM, et al. (2010) Antimicrobial treatment for early, limited Mycobacterium ulcerans infection: a randomised controlled trial. Lancet 375: 664-672 doi:10.1016/S0140-6736(09)61962-0.
29. Kibadi K, Boelaert M, Fraga AG, Kayinua M, Longatto-Filho A, et al. (2010) Response to treatment in a prospective cohort of patients with large ulcerated lesions suspected to be Buruli Ulcer (Mycobacterium ulcerans disease). PLoS Negl Trop Dis 4: e736 doi:10.1371/journal.pntd.0000736.
30. Sarfo FS, Phillips R, Asiedu K, Ampadu E, Bobi N, et al. (2010) Clinical efficacy of combination of rifampin and streptomycin for treatment of Mycobacterium ulcerans disease. Antimicrob. Agents Chemother 54: 3678-3685 doi:10.1128/AAC.00299-10.
31. Kibadi AK, (2006) [Relapses after surgical treatment of Buruli ulcer in Africa]. Bull Soc Pathol Exot 99: 230-235.
32. Amofah G, Asamoah S, Afram-Gyening C, (1998) Effectiveness of excision of pre-ulcerative Buruli lesions in field situations in a rural district in Ghana. Trop Doct 28: 81-83.
33. Kanga JM, Kacou DE, Sangaré A, Dabila Y, Asse NH, et al. (2003) [Recurrence after surgical treatment of Buruli ulcer in Cote d'Ivoire]. Bull Soc Pathol Exot 96: 406-409.
34. Debacker M, Aguiar J, Steunou C, Zinsou C, Meyers WM, et al. (2004) Mycobacterium ulcerans disease (Buruli ulcer) in rural hospital, Southern Benin, 1997-2001. Emerging Infect Dis 10: 1391-1398.
35. Sopoh GE, Dossou AD, Brun LV, Barogui YT, Houézo JG, et al. (2010) Severe multifocal form of buruli ulcer after streptomycin and rifampin treatment: comments on possible dissemination mechanisms. Am J Trop Med Hyg 83: 307-313 doi:10.4269/ajtmh.2010.09-0617.
36. Portaels F, Aguiar J, Debacker M, Guédénon A, Steunou C, et al. (2004) Mycobacterium bovis BCG vaccination as prophylaxis against Mycobacterium ulcerans osteomyelitis in Buruli ulcer disease. Infect Immun 72: 62-65.
37. Hofer M, Hirschel B, Kirschner P, Beghetti M, Kaelin A, et al. (1993) Brief report: disseminated osteomyelitis from Mycobacterium ulcerans after a snakebite. N Engl J Med 328: 1007-1009 doi:10.1056/NEJM199304083281405.
38. Pszolla N, Sarkar MR, Strecker W, Kern P, Kinzl L, et al. (2003) Buruli ulcer: a systemic disease. Clin Infect Dis 37: e78-82 doi:10.1086/377170.
39. Hayman J, (1985) Clinical features of Mycobacterium ulcerans infection.Australas J Dermatol 26: 67-73.
40. Schütte D, UmBoock A, Pluschke G, (2009) Phagocytosis of Mycobacterium ulcerans in the course of rifampicin and streptomycin chemotherapy in Buruli ulcer lesions. British Journal of Dermatology 160: 273-283.
41. O'Brien DP, Robson ME, Callan PP, McDonald AH, (2009) "Paradoxical" immune-mediated reactions to Mycobacterium ulcerans during antibiotic treatment: a result of treatment success, not failure. Med J Aust 191: 564-566.
42. WHO, (2001) Buruli Ulcer. Diagnosis of Mycobacterium ulcerans disease (eds F Portaels, P Johnson, WM Meyers). WHO/CDS/CPE/GBUI/2001.
43. Kumar V, (2004) High resolution shadowing of Mycobacterium leprae. Biotechnic and Histochemistry 79: 197-201.
44. Coutanceau E, Decalf J, Martino A, Babon A, Winter N, et al. (2007) Selective suppression of dendritic cell functions by Mycobacterium ulcerans toxin mycolactone. J Exp Med 204: 1395-1403 doi:10.1084/jem.20070234.
45. Diaz D, Dobeli H, Yeboah-Manu D, Mensah-Quainoo E, Friedlein A, et al. (2006) Use of the Immunodominant 18-Kilodalton Small Heat Shock Protein as a Serological Marker for Exposure to Mycobacterium ulcerans. Clin Vaccine Immunol 13: 1314-1321.
46. Okenu DMN, Ofielu LO, Easley KA, Guarner J, Spotts Whitney EA, et al. (2004) Immunoglobulin M antibody responses to Mycobacterium ulcerans allow discrimination between cases of active Buruli ulcer disease and matched family controls in areas where the disease is endemic. Clin Diagn Lab Immunol 11: 387-391.
47. Dobos KM, Spotts EA, Marston BJ, Horsburgh CR, King CH, (2000) Serologic response to culture filtrate antigens of Mycobacterium ulcerans during Buruli ulcer disease. Emerging Infect Dis 6: 158-164.
48. Schütte D, Pluschke G, (2009) Immunosuppression and treatment-associated inflammatory response in patients with Mycobacterium ulcerans infection (Buruli ulcer). Expert Opin Biol Ther 9: 187-200 doi:10.1517/14712590802631854.
49. Müller M, Wandel S, Colebunders R, Attia S, Furrer H, et al. (2010) Immune reconstitution inflammatory syndrome in patients starting antiretroviral therapy for HIV infection: a systematic review and meta-analysis. Lancet Infect Dis 10: 251-261 doi:10.1016/S1473-3099(10)70026-8.
50. Breton G, (2010) [Immune reconstitution inflammatory syndrome or IRIS]. Med Sci (Paris) 26: 281-289.
51. Beatty GW, (2010) Immune reconstitution inflammatory syndrome. Emerg Med Clin North Am 28: 393-407, Table of Contents doi:10.1016/j.emc.2010.01.004.
52. Kiertiburanakul S, (2010) Immune reconstitution inflammatory syndrome in HIV-infected patients with tuberculosis. J Med Assoc Thai 93: 257-264.
53. Moreno C, Taverne J, Mehlert A, Bate CA, Brealey RJ, et al. (1989) Lipoarabinomannan from Mycobacterium tuberculosis induces the production of tumour necrosis factor from human and murine macrophages. Clin Exp Immunol 76: 240-245.
54. Wallis RS, Amir-Tahmasseb M, Ellner JJ, (1990) Induction of interleukin 1 and tumor necrosis factor by mycobacterial proteins: the monocyte western blot.Proc Natl Acad Sci U S A 87: 3348-3352.
55. Troncoso Mariño A, Campelo Sánchez E, Martínez López de Castro N, Inaraja Bobo MT, (2010) Haemophagocytic syndrome and paradoxical reaction to tuberculostatics after treatment with infliximab. Pharm World Sci 32: 117-119 doi:10.1007/s11096-010-9369-x.
56. Garcia Vidal C, Garau J, (2005) Systemic steroid treatment of paradoxical upgrading reaction in patients with lymph node tuberculosis. Clin Infect Dis 41: 915-916; author reply 916-917 doi:10.1086/432807.
57. Garcia Vidal C, Rodríguez Fernández S, Martínez Lacasa J, Salavert M, Vidal R, et al. (2005) Paradoxical response to antituberculous therapy in infliximab-treated patients with disseminated tuberculosis. Clin Infect Dis 40: 756-759 doi:10.1086/427941.
58. Safdar A, Brown AE, Kraus DH, Malkin M, (2000) Paradoxical reaction syndrome complicating aural infection due to Mycobacterium tuberculosis during therapy. Clin Infect Dis 30: 625-627 doi:10.1086/313731.
59. Huygen K, Adjei O, Affolabi D, Bretzel G, Demangel C, et al. (2009) Buruli ulcer disease: prospects for a vaccine. Med Microbiol Immunol 198: 69-77 doi:10.1007/s00430-009-0109-6.