The oral presentation of secondary syphilis among men: the evolving interplay between syphilis, HIV and prophylactic strategies
DOI:
https://doi.org/10.17159/sadj.v78i01.15742Keywords:
disassociation, SerologicalAbstract
Syphilis has been intricately linked with HIV because of shared transmission pathways and because these infections promote each other’s transmission. In addition, HIV infection may change the clinical presentation and management of syphilis lesions. Initially, the HIV epidemic had improved safe sex practices among men who have sex with men (MSM), but subsequent effective treatment and prophylaxis strategies, have resulted in behavioural disinhibition and a resurgence of syphilis. Here, we report on three cases of oral secondary syphilis and explore the relationship between oral syphilis and sexual practices, HIV and prophylactic measures that MSM employ. Three men, who presented to the University of Pretoria Oral Health Centre (UPOHC), complaining of oral lesions, were
diagnosed by histopathology with secondary syphilis. The clinical appearance of the lesions, HIV status, treatment and
prophylaxis employed by the men were documented. The clinical presentation, sexual practices, HIV status and prophylactic measures among these men differed and demonstrate the complexity of oral secondary syphilisdiagnosis and management.
Syphilis presents variably in the oral cavity, and this may be linked to the sexual practices and HIV status of the patient.
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References
Hook EW, 3rd. Syphilis. Lancet. 2017; 389(10078):1550-7. doi:10.1016/s0140-6736(16)32411-4 DOI: https://doi.org/10.1016/S0140-6736(16)32411-4
Greenblatt RM, Lukehart SA, Plummer FA, Quinn TC, Critchlow CW, Ashley RL, et al., Genital ulceration as a risk factor for human immunodeficiency virus infection. Aids. 1988; 2(1):47-50. doi:10.1097/00002030-198802000-00008 DOI: https://doi.org/10.1097/00002030-198802000-00008
Farhi D, Dupin N. Management of syphilis in the hiv-infected patient: Facts and controversies. Clin Dermatol. 2010; 28(5):539-45. doi:10.1016/j.clindermatol.2010.03.012 DOI: https://doi.org/10.1016/j.clindermatol.2010.03.012
Hertel M, Matter D, Schmidt-Westhausen AM, Bornstein MM. Oral syphilis: A series of 5 cases. J Oral Maxillofac Surg. 2014; 72(2):338-45. doi:10.1016/j.joms.2013.07.015 DOI: https://doi.org/10.1016/j.joms.2013.07.015
Doherty L, Fenton KA, Jones J, Paine TC, Higgins SP, Williams D, et al.,Syphilis: Old problem, new strategy. Bmj. 2002; 325(7356):153-6. doi:10.1136/bmj.325.7356.153 DOI: https://doi.org/10.1136/bmj.325.7356.153
Mayer KH, Ramjee G. The current status of the use of oral medication to prevent hiv transmission. Curr Opin HIV AIDS. 2015; 10(4):226-32. doi:10.1097/coh.0000000000000170 DOI: https://doi.org/10.1097/COH.0000000000000170
Compilato D, Amato S, Campisi G. Resurgence of syphilis: A diagnosis based on unusual oral mucosa lesions. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009; 108(3):e45-9. doi:10.1016/j.tripleo.2009.05.013 DOI: https://doi.org/10.1016/j.tripleo.2009.05.013
Schuch LF, da Silva KD, de Arruda JAA, Etges A, Gomes APN, Mesquita RA, et al., Forty cases of acquired oral syphilis and a review of the literature. Int J Oral Maxillofac Surg. 2019; 48(5):635-43. doi:10.1016/j.ijom.2018.10.023 DOI: https://doi.org/10.1016/j.ijom.2018.10.023
Leão JC, Gueiros LA, Porter SR. Oral manifestations of syphilis. Clinics (Sao Paulo). 2006; 61(2):161-6. doi:10.1590/s1807-59322006000200012 DOI: https://doi.org/10.1590/S1807-59322006000200012
Czerninski R, Pikovski A, Meir K, Casap N, Moses AE, Maly A. Oral syphilis lesions--a diagnostic approach and histologic characteristics of secondary stage. Quintessence Int. 2011; 42(10):883-9.
Eyer-Silva WA, Freire MAL, Horta-Araujo CA, Almeida Rosa da Silva G, Francisco da Cunha Pinto J, Raphael de Almeida Ferry F. Secondary syphilis presenting as glossodynia, plaques en prairie fauchée, and a split papule at the oral commissure: Case report and review. Case Rep Med. 2017; 2017:1980798. doi:10.1155/2017/1980798 DOI: https://doi.org/10.1155/2017/1980798
Lampros A, Seta V, Gerhardt P, Isnard C, Husson C, Dupin N. Oral forms of secondary syphilis: An illustration of the pitfalls set by the great imitator. J Am Acad Dermatol. 2021; 84(2):348-53. doi:10.1016/j.jaad.2020.04.089 DOI: https://doi.org/10.1016/j.jaad.2020.04.089
Barrett AW, Villarroel Dorrego M, Hodgson TA, Porter SR, Hopper C, Argiriadou AS, et al., The histopathology of syphilis of the oral mucosa. J Oral Pathol Med. 2004; 33(5):286-91. doi:10.1111/j.0904-2512.2004.00099.x DOI: https://doi.org/10.1111/j.0904-2512.2004.00099.x
Buffet M, Grange PA, Gerhardt P, Carlotti A, Calvez V, Bianchi A, et al., Diagnosing treponema pallidum in secondary syphilis by pcr and immunohistochemistry. J Invest Dermatol. 2007; 127(10):2345-50. doi:10.1038/sj.jid.5700888 DOI: https://doi.org/10.1038/sj.jid.5700888
Ramírez-Amador V, Anaya-Saavedra G, Crabtree-Ramírez B, EsquivelPedraza L, Saeb-Lima M, Sierra-Madero J. Clinical spectrum of oral secondary syphilis in hiv-infected patients. J Sex Transm Dis. 2013; 2013:892427. doi:10.1155/2013/892427 DOI: https://doi.org/10.1155/2013/892427
Tampa M, Sarbu I, Matei C, Benea V, Georgescu SR. Brief history of syphilis. Journal of medicine and life. 2014; 7:4-10.
Hoque M, Hoque ME, van Hal G, Buckus S. Prevalence, incidence and seroconversion of hiv and syphilis infections among pregnant women of south africa. Southern African journal of infectious diseases. 2021; 36(1):296-. doi:10.4102/sajid.v36i1.296 DOI: https://doi.org/10.4102/sajid.v36i1.296
Kularatne RS, Niit R, Rowley J, Kufa-Chakezha T, Peters RPH, Taylor MM, et al., Adult gonorrhea, chlamydia and syphilis prevalence, incidence, treatment and syndromic case reporting in south africa: Estimates using the spectrum-sti model, 1990-2017. PLoS One. 2018; 13(10):e0205863. doi:10.1371/journal.pone.0205863 DOI: https://doi.org/10.1371/journal.pone.0205863
SA S. 2020 mid-year population estimates. 2020. South African Census, Statistics South Africa.
Prevention CfDCa. Sexually transmitted disease surveillance 2017. Atlanta: US Department of Health and Human Services, 2018.
Abara WE, Hess KL, Neblett Fanfair R, Bernstein KT, Paz-Bailey G. Syphilis trends among men who have sex with men in the united states and western europe: A systematic review of trend studies published between 2004 and 2015. PLoS One. 2016; 11(7):e0159309. doi:10.1371/journal.pone.0159309 DOI: https://doi.org/10.1371/journal.pone.0159309
Spiteri G, Unemo M, Mårdh O, Amato-Gauci AJ. The resurgence of syphilis in high-income countries in the 2000s: A focus on europe. Epidemiol Infect. 2019; 147:e143. doi:10.1017/s0950268819000281 DOI: https://doi.org/10.1017/S0950268819000281
Vuylsteke B, Reyniers T, De Baetselier I, Nöstlinger C, Crucitti T, Buyze J, et al.,Daily and event-driven pre-exposure prophylaxis for men who have sex with men in belgium: Results of a prospective cohort measuring adherence, sexual behaviour and sti incidence. Journal of the International AIDS Society. 2019; 22(10):e25407-e. doi:10.1002/jia2.25407 DOI: https://doi.org/10.1002/jia2.25407
Traeger MW, Cornelisse VJ, Asselin J, Price B, Roth NJ, Willcox J, et al., Association of hiv preexposure prophylaxis with incidence of sexually transmitted infections among individuals at high risk of hiv infection. Jama. 2019; 321(14):1380-90. doi:10.1001/jama.2019.2947 DOI: https://doi.org/10.1001/jama.2019.2947
Unemo M, Bradshaw CS, Hocking JS, de Vries HJC, Francis SC, Mabey D, et al., Sexually transmitted infections: Challenges ahead. Lancet Infect Dis. 2017; 17(8):e235-e79. doi:10.1016/s1473-3099(17)30310-9 DOI: https://doi.org/10.1016/S1473-3099(17)30310-9
Bolan RK, Beymer MR, Weiss RE, Flynn RP, Leibowitz AA, Klausner JD. Doxycycline prophylaxis to reduce incident syphilis among hiv-infected men who have sex with men who continue to engage in high-risk sex: A randomized, controlled pilot study. Sex Transm Dis. 2015; 42(2):98-103. doi:10.1097/olq.0000000000000216 DOI: https://doi.org/10.1097/OLQ.0000000000000216
Molina JM, Charreau I, Chidiac C, Pialoux G, Cua E, Delaugerre C, et al., Postexposure prophylaxis with doxycycline to prevent sexually transmitted infections in men who have sex with men: An open-label randomised substudy of the anrs ipergay trial. Lancet Infect Dis. 2018; 18(3):308-17. doi:10.1016/s1473-3099(17)30725-9 DOI: https://doi.org/10.1016/S1473-3099(17)30725-9
Soares AB GH, Jorge MA, Barraviera SRCS. Oral manifestations of syphilis: A review. J. Venom. Anim. Toxins incl. Trop. Dis. 2004; 10(1):2-9. DOI: https://doi.org/10.1590/S1678-91992004000100002
Wu MY, Gong HZ, Hu KR, Zheng H-y, Wan X, Li J. Effect of syphilis infection on hiv acquisition: A systematic review and meta-analysis. Sexually Transmitted Infections. 2021; 97(7):525-33. doi:10.1136/sextrans-2020-054706 DOI: https://doi.org/10.1136/sextrans-2020-054706
Lafond RE, Lukehart SA. Biological basis for syphilis. Clin Microbiol Rev. 2006; 19(1):29-49. doi:10.1128/cmr.19.1.29-49.2006 DOI: https://doi.org/10.1128/CMR.19.1.29-49.2006
Radolf JD, Deka RK, Anand A, Šmajs D, Norgard MV, Yang XF. Treponema pallidum, the syphilis spirochete: Making a living as a stealth pathogen. Nat Rev Microbiol. 2016; 14(12):744-59. doi:10.1038/nrmicro.2016.141 DOI: https://doi.org/10.1038/nrmicro.2016.141
Salazar JC, Cruz AR, Pope CD, Valderrama L, Trujillo R, Saravia NG, et al.,Treponema pallidum elicits innate and adaptive cellular immune responses in skin and blood during secondary syphilis: A flow-cytometric analysis. J Infect Dis. 2007; 195(6):879-87. doi:10.1086/511822 DOI: https://doi.org/10.1086/511822
Kofoed K, Gerstoft J, Mathiesen LR, Benfield T. Syphilis and human immunodeficiency virus (hiv)-1 coinfection: Influence on cd4 t-cell count, hiv-1 viral load, and treatment response. Sexually Transmitted Diseases. 2006; 33(3):143-8. doi:10.1097/01.olq.0000187262.56820.c0 DOI: https://doi.org/10.1097/01.olq.0000187262.56820.c0
Workowski KA, Bolan GA. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep. 2015; 64(Rr-03):1-137.
Costa-Silva M, Azevedo C, Azevedo F, Lisboa C. Early syphilis treatment in hivinfected patients: Single dose vs. Three doses of benzathine penicillin g. J Eur Acad Dermatol Venereol. 2016; 30(10):1805-9. doi:10.1111/jdv.13766 DOI: https://doi.org/10.1111/jdv.13766
Edwards S, Carne C. Oral sex and transmission of non-viral stis. Sex Transm Infect. 1998; 74(2):95-100. doi:10.1136/sti.74.2.95 DOI: https://doi.org/10.1136/sti.74.2.95
de Andrade RS, de Freitas EM, Rocha BA, Gusmão ES, Filho MR, Júnior HM. Oral findings in secondary syphilis. Med Oral Patol Oral Cir Bucal. 2018; 23(2):e138-e43. doi:10.4317/medoral.22196 DOI: https://doi.org/10.4317/medoral.22196
Schacker T, Collier AC, Hughes J, Shea T, Corey L. Clinical and epidemiologic features of primary hiv infection. Ann Intern Med. 1996; 125(4):257-64. doi:10.7326/0003-4819-125-4-199608150-00001 DOI: https://doi.org/10.7326/0003-4819-125-4-199608150-00001
Rothenberg RB, Scarlett M, del Rio C, Reznik D, O’Daniels C. Oral transmission of hiv. Aids. 1998; 12(16):2095-105. doi:10.1097/00002030-199816000-00004 DOI: https://doi.org/10.1097/00002030-199816000-00004
Gilbart VL, Evans BG, Dougan S. Hiv transmission among men who have sex with men through oral sex. Sex Transm Infect. 2004; 80(4):324. doi:10.1136/sti.2004.009217 DOI: https://doi.org/10.1136/sti.2004.009217
Cohen MS, Shugars DC, Fiscus SA. Limits on oral transmission of hiv-1. Lancet. 2000; 356(9226):272. doi:10.1016/s0140-6736(00)02500-9 DOI: https://doi.org/10.1016/S0140-6736(00)02500-9
Wood LF, Chahroudi A, Chen HL, Jaspan HB, Sodora DL. The oral mucosa immune environment and oral transmission of hiv/siv. Immunol Rev. 2013; 254(1):34-53. doi:10.1111/imr.12078 DOI: https://doi.org/10.1111/imr.12078
Leuci S, Martina S, Adamo D, Ruoppo E, Santarelli A, Sorrentino R, et al., Oral syphilis: A retrospective analysis of 12 cases and a review of the literature. Oral Dis. 2013; 19(8):738-46. doi:10.1111/odi.12058 DOI: https://doi.org/10.1111/odi.12058
Zhou X, Wu MZ, Jiang TT, Chen XS. Oral manifestations of early syphilis in adults: A systematic review of case reports and series. Sex Transm Dis. 2021; 48(12):e209-e14. doi:10.1097/olq.0000000000001538 DOI: https://doi.org/10.1097/OLQ.0000000000001538
Carbone PN, Capra GG, Nelson BL. Oral secondary syphilis. Head Neck Pathol. 2016; 10(2):206-8. doi:10.1007/s12105-015-0623-3 DOI: https://doi.org/10.1007/s12105-015-0623-3
www.sada.co.za / SADJ Vol. 78 No.1 New draft2.indd 30 2023/02/22 15:03CASE REPORT < 31
Dai T, Song NJ. An unusual case of oral condyloma lata. Int J Infect Dis. 2021; 105:349-50. doi:10.1016/j.ijid.2021.02.051 DOI: https://doi.org/10.1016/j.ijid.2021.02.051
Pourang A, Fung MA, Tartar D, Brassard A. Condyloma lata in secondary syphilis. JAAD case reports. 2021; 10:18-21.doi:10.1016/j.j dcr.2021.01.025 DOI: https://doi.org/10.1016/j.jdcr.2021.01.025
Aquilina C, Viraben R, Denis P. Secondary syphilis simulating oral hairy leukoplakia. J Am Acad Dermatol. 2003; 49(4):749-51.doi:10.1067/s0190-9622(03)00484-5 DOI: https://doi.org/10.1067/S0190-9622(03)00484-5
de Paulo LF, Servato JP, Oliveira MT, Durighetto AF, Jr., Zanetta-Barbosa D. Oral manifestations of secondary syphilis. Int J Infect Dis. 2015; 35:40-2. doi:10.1016/j.ijid.2015.04.007 DOI: https://doi.org/10.1016/j.ijid.2015.04.007
Araujo JP, Jaguar GC, Alves FA. Syphilis related to atypical oral lesions affecting an elderly man. A case report. Gerodontology. 2015; 32(1):73-5. doi:10.1111/ger.12047 DOI: https://doi.org/10.1111/ger.12047
Kelner N, Rabelo GD, da Cruz Perez DE, Assunção JN, Jr., Witzel AL, Migliari DA, et al., Analysis of nonspecific oral mucosal and dermal lesions suggestive of syphilis: A report of 6 cases. Oral Surg Oral Med Oral Pathol Oral Radiol. 2014; 117(1):1-7. doi:10.1016/j.oooo.2012.04.028 DOI: https://doi.org/10.1016/j.oooo.2012.04.028
Leone C, Sugaya N, Migliari D. An intriguing case of ectopic benign migratory glossitis resembling secondary syphilis: A case report. Case Rep Dermatol. 2020; 12(3):262-5. doi:10.1159/000510776 DOI: https://doi.org/10.1159/000510776
Dybeck Udd S, Lund B. Oral syphilis: A reemerging infection prompting clinicians’ alertness. Case Rep Dent. 2016; 2016:6295920. doi:10.1155/2016/6295920 DOI: https://doi.org/10.1155/2016/6295920
Rompalo AM, Joesoef MR, O’Donnell JA, Augenbraun M, Brady W, Radolf JD, et al., Clinical manifestations of early syphilis by hiv status and gender: Results of the syphilis and hiv study. Sex Transm Dis. 2001; 28(3):158-65. doi:10.1097/00007435-200103000-00007 DOI: https://doi.org/10.1097/00007435-200103000-00007
Theel ES, Katz SS, Pillay A. Molecular and direct detection tests for treponema pallidum subspecies pallidum: A review of the literature, 1964-2017. Clin Infect Dis. 2020; 71(Suppl 1):S4-s12. doi:10.1093/cid/ciaa176 DOI: https://doi.org/10.1093/cid/ciaa176
Hook EW, 3rd, Roddy RE, Lukehart SA, Hom J, Holmes KK, Tam MR. Detection of treponema pallidum in lesion exudate with a pathogen-specific monoclonal antibody. Journal of clinical microbiology. 1985; 22(2):241-4. doi:10.1128/jcm.22.2.241-244.1985 DOI: https://doi.org/10.1128/jcm.22.2.241-244.1985
Pierce EF, Katz KA. Darkfield microscopy for point-of-care syphilis diagnosis. MLO Med Lab Obs. 2011; 43(1):30-1.
Yousefi L, Leylabadlo HE, Pourlak T, Eslami H, Taghizadeh S, Ganbarov K, et al.,Oral spirochetes: Pathogenic mechanisms in periodontal disease. Microb Pathog. 2020; 144:104193. doi:10.1016/j.micpath.2020.10419359. Loeffelholz MJ, Binnicker MJ. It is time to use treponema-specific antibody screening tests for diagnosis of syphilis. J Clin Microbiol. 2012; 50(1):2-6. doi:10.1128/jcm.06347-11 DOI: https://doi.org/10.1016/j.micpath.2020.104193
Marra CM, Ghanem KG. Centers for disease control and prevention syphilis summit: Difficult clinical and patient management issues. Sex Transm Dis. 2018; 45(9S Suppl 1):S10-s2. doi:10.1097/olq.0000000000000851 DOI: https://doi.org/10.1097/OLQ.0000000000000851
Who guidelines approved by the guidelines review committee. Who guidelines for the treatment of treponema pallidum (syphilis). Geneva: World Health Organization © World Health Organization 2016.; 2016.
Thakrar P, Aclimandos W, Goldmeier D, Setterfield JF. Oral ulcers as a presentation of secondary syphilis. Clin Exp Dermatol. 2018; 43(8):868-75. doi:10.1111/ced.13640 DOI: https://doi.org/10.1111/ced.13640
Stafylis C, Keith K, Mehta S, Tellalian D, Burian P, Millner C, et al., Clinical efficacy of cefixime for the treatment of early syphilis. Clin Infect Dis. 2021; 73(5):907-10. doi:10.1093/cid/ciab187 DOI: https://doi.org/10.1093/cid/ciab187
Beale MA, Marks M, Sahi SK, Tantalo LC, Nori AV, French P, et al., Genomic epidemiology of syphilis reveals independent emergence of macrolide resistance across multiple circulating lineages. Nat Commun. 2019; 10(1):3255. doi:10.1038/s41467-019-11216-7 DOI: https://doi.org/10.1038/s41467-019-11216-7
Ghanem KG, Erbelding EJ, Wiener ZS, Rompalo AM. Serological response to syphilis treatment in hiv-positive and hiv-negative patients attending sexually transmitted diseases clinics. Sexually transmitted infections. 2007; 83(2):97-101. doi:10.1136/sti.2006.021402 DOI: https://doi.org/10.1136/sti.2006.021402
Rolfs RT, Joesoef MR, Hendershot EF, Rompalo AM, Augenbraun MH, Chiu M, 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(5):307-14. doi:10.1056/nejm199707313370504 DOI: https://doi.org/10.1056/NEJM199707313370504
White AC, Jr. Treatment of early syphilis in hiv: What do we really know? Clinical Infectious Diseases. 2016; 64(6):765-6.doi:10.1093/cid/ciw866 DOI: https://doi.org/10.1093/cid/ciw866
Blank LJ, Rompalo AM, Erbelding EJ, Zenilman JM, Ghanem KG. Treatment of syphilis in hiv-infected subjects: A systematic review of the literature. Sex Transm Infect. 2011; 87(1):9-16. doi:10.1136/sti.2010.043893 DOI: https://doi.org/10.1136/sti.2010.043893
Andrade R, Rodriguez-Barradas MC, Yasukawa K, Villarreal E, Ross M, Serpa JA. Single dose versus 3 doses of intramuscular benzathine penicillin for early syphilis in hiv: A randomized clinical trial. Clin Infect Dis. 2017; 64(6):759-64. doi:10.1093/cid/ciw862 DOI: https://doi.org/10.1093/cid/ciw862
Ganesan A, Mesner O, Okulicz JF, O’Bryan T, Deiss RG, Lalani T, et al., A single dose of benzathine penicillin g is as effective as multiple doses of benzathine penicillin g for the treatment of hiv-infected persons with early syphilis. Clin Infect Dis. 2015; 60(4):653-60. doi:10.1093/cid/ciu888 DOI: https://doi.org/10.1093/cid/ciu888
Çakmak SK, Tamer E, Karadag AS, Waugh M. Syphilis: A great imitator. Clin Dermatol. 2019; 37(3):182-91.doi:10.1016/j.clindermatol .2019.01.007 DOI: https://doi.org/10.1016/j.clindermatol.2019.01.007
Achterbergh RCA, Hoornenborg E, Boyd A, Coyer L, Meuzelaar SJA, Hogewoning AA, et al., Changes in mental health and drug use among men who have sex with men using daily and event-driven pre-exposure prophylaxis: Results from a prospective demonstration project in amsterdam, the netherlands. EClinicalMedicine. 2020; 26:100505. doi:10.1016/j.eclinm.2020.100505 DOI: https://doi.org/10.1016/j.eclinm.2020.100505
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