Abstract
Neisseria meningitidis (Nm) is asymptomatically carried in the nasopharynx of 5–10% adults, although certain populations, such as men who have sex with men (MSM), exhibit a higher colonisation rate. Interest in Nm carriage has been renewed, owed to meningitis outbreaks within populations of MSM. The aim of this study was to characterise Nm isolates and risk factors for its carriage among MSM attending a sexual health unit. A retrospective cross-sectional study was undertaken between June 2018 and December 2021. We took anal, oropharyngeal, urethral, and blood samples as part of the sexually transmitted infection screening procedures routinely implemented. Nm isolates were subjected to antimicrobial susceptibility testing; the serogroup and genogroup were determined by multi-locus sequence typing. A total of 399 subjects were recruited, and the Nm oropharyngeal carriage rate was 29%, similar among both people living with HIV (PLWH) and uninfected individuals. Nm carriage was less common in vaccinated individuals, especially those who had received the tetravalent vaccine (2.6% vs. 10.6%, p = 0.008). The most frequent serogroups were B (40%) and non-groupable (45%). Most of the isolates were susceptible to ciprofloxacin (96%) and ceftriaxone (100%). However, we identified 21 strains (20%) belonging to hyperinvasive lineages (CC11, CC4821, CC32, CC41/44, CC213, and CC269), most of which belonged to serogroup B. Given that vaccination with MenACWY was associated with a low Nm carriage, we encourage routine vaccination of all MSM. Moreover, the administration of the meningitis B vaccine should also be assessed considering that several invasive lines included in serogroup B are circulating among MSM.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
van de Beek D, Brouwer MC, Koedel U, Wall EC (2021) Community-acquired bacterial meningitis. The Lancet 25(398):1171–1183. https://doi.org/10.1016/S0140-6736(21)00883-7
Taha MK, Weil-Olivier C, Bouée S, Emery C, Nachbaur G, Pribil C et al (2021) Risk factors for invasive meningococcal disease: a retrospective analysis of the French national public health insurance database. Hum Vaccin Immunother 17:1858–1866. https://doi.org/10.1080/21645515.2020.1849518
Lundbo LF, Harboe ZB, Sandholdt H, Smith-Hansen L, Valentiner-Branth P, Hoffmann S et al (2021) Comorbidity increases the risk of invasive meningococcal disease in adults. Clin Infect Dis 75:1. https://doi.org/10.1093/cid/ciab856
Aye AMM, Bai X, Borrow R, Bory S, Carlos J, Caugant DA et al (2020) Meningococcal disease surveillance in the Asia-Pacific region (2020): the global meningococcal initiative. J Infect 1(81):698–711. https://doi.org/10.1016/j.jinf.2020.07.025
Hill DJ, Griffiths NJ, Borodina E, Virji M (2010) Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin Sci (Lond) 9(118):547–564. https://doi.org/10.1042/CS20090513
Ngai S, Weiss D, Bell JA, Majrud D, Zayas G, Crawley A et al (2020) Carriage of neisseria meningitidis in men who have sex with men presenting to public sexual health clinics. New York City Sex Transm Dis 1(47):541–548. https://doi.org/10.1097/OLQ.0000000000001205
Neri A, Palmieri A, Prignano G, Giuliani M, Latini A, Fazio C, et al (2021) Molecular characterisation and antibiotic susceptibility of meningococcal isolates from healthy men who have sex with men. Sex Transm Infect 17;sextrans-2021–055173. https://doi.org/10.1136/sextrans-2021-055173
Tinggaard M, Slotved HC, Fuursted K, Rosenstierne MW, Kronborg G, Lebech AM et al (2021) Oral and anal carriage of Neisseria meningitidis among sexually active HIV-infected men who have sex with men in Denmark 2014–15. Int J Infect Dis 1(105):337–344. https://doi.org/10.1016/j.ijid.2021.02.062
Folaranmi TA, Kretz CB, Kamiya H, MacNeil JR, Whaley MJ, Blain A et al (2017) Increased risk for meningococcal disease among men who have sex with men in the United States, 2012–2015. Clin Infect Dis 1(65):756–763. https://doi.org/10.1093/cid/cix438
Fernández-Rodríguez A, Alcalá B, Álvarez-Lafuente R (2008) Real-time polymerase chain reaction detection of Neisseria meningitidis in formalin-fixed tissues from sudden deaths. Diagn Microbiol Infect Dis 60:339–346. https://doi.org/10.1016/j.diagmicrobio.2007.10.014
Fraisier C, Stor R, Tenebray B, Sanson Y, Nicolas P (2009) Use of a new single multiplex PCR-based assay for direct simultaneous characterization of six Neisseria meningitidis serogroups. J Clin Microbiol 47:2662–2666. https://doi.org/10.1128/JCM.02415-08
Bennett DE, Mulhall RM, Cafferkey MT (2004) PCR-based assay for detection of Neisseria meningitidis capsular serogroups 29E, X, and Z. J Clin Microbiol 42:1764–1765. https://doi.org/10.1128/JCM.42.4.1764-1765.2004
Alcalá B, Salcedo C, Arreaza L, Abad R, Enríquez R, de La Fuente L et al (2004) Antigenic and/or phase variation of PorA protein in non-subtypable Neisseria meningitidis strains isolated in Spain. J Med Microbiol 1(53):515–518. https://doi.org/10.1099/jmm.0.05517-0
Maiden MCJ, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms (molecular typingNeisseria meningitidishousekeeping genesWorld-Wide Webhyper-virulent clones) [Internet]. www.pnas.org. Accessed 01 Oct 2022
Jacquinet S, Mattheus W, Quoilin S, Wyndham-Thomas C, Martin C, van der Linden D et al (2022) Outbreak of invasive meningococcal disease caused by a meningococcus serogroup B in a nursery school, Wallonia, Belgium, 2018. Eurosurveillance 3:27. https://doi.org/10.2807/1560-7917.ES.2022.27.9.2100224
Kratz MM, Weiss D, Ridpath A, Zucker JR, Geevarughese A, Rakeman J et al (2015) Community-based outbreak of Neisseria meningitidis serogroup C infection in men who have sex with men, New York City, New York, USA, 2010–2013. Emerg Infect Dis 23(21):1379–1386. https://doi.org/10.3201/eid2108.141837
Ladhani SN, Lucidarme J, Parikh SR, Campbell H, Borrow R, Ramsay ME (2020) Meningococcal disease and sexual transmission: urogenital and anorectal infections and invasive disease due to Neisseria meningitidis. The Lancet 13(395):1865–1877. https://doi.org/10.1016/S0140-6736(20)30913-2
Comité Asesor de Vacunas (CAV-AEP). Meningococo. Manual de vacunas en línea de la AEP [Internet]. Madrid: AEP; ene/2023. Available in: http://vacunasaep.org/documentos/manual/cap-30. Accessed 01 Oct 2022
Balmer P, Burman C, Serra L, York LJ (2018) Impact of meningococcal vaccination on carriage and disease transmission: a review of the literature. Hum Vaccin Immunother 4(14):1118–1130. https://doi.org/10.1080/21645515.2018.1454570
Campbell H, Andrews N, Parikh SR, White J, Edelstein M, Bai X et al (2022) Impact of an adolescent meningococcal ACWY immunisation programme to control a national outbreak of group W meningococcal disease in England: a national surveillance and modelling study. Lancet Child Adolesc Health 6:96–105. https://doi.org/10.1016/S2352-4642(21)00335-7
McMillan M, Chandrakumar A, Wang HLR, Clarke M, Sullivan TR, Andrews RM et al (2021) Effectiveness of meningococcal vaccines at reducing invasive meningococcal disease and pharyngeal Neisseria meningitidis carriage: a systematic review and meta-analysis. Clin Infect Dis 1(73):E609–E619. https://doi.org/10.1093/cid/ciaa1733
Rossotti R, Merli M, Cantone M, Moioli MC, Motta D, Orcese C et al (2019) Risk factors for community-acquired bacterial meningitis: men who have sex with men (MSM) as a population at risk for meningococcal nasopharyngeal carriage. Infect Dis 51:714–717. https://doi.org/10.1080/23744235.2019.1642512
Meiring S, Cohen C, de Gouveia L, du Plessis M, Ganesh K, Kleynhans J et al (2021) Human immunodeficiency virus infection is associated with increased meningococcal carriage acquisition among first-year students in 2 South African universities. Clin Infect Dis 1(73):E28-38. https://doi.org/10.1093/cid/ciaa521
GESIDA (2019) Documento de Consenso de Gesida/Plan Nacional Sobre el Sida Respecto al Tratamiento Antirretroviral en Adultos Infectados por el Virus de la Inmunodeficiencia Humana. GESIDA, Madrid
Morselli S, Gaspari V, Cantiani A, Salvo M, Foschi C, Lazzarotto T et al (2022) Meningococcal carriage in ‘men having sex with men’ with pharyngeal gonorrhoea. Front Cell Infect Microbiol 12:11. https://doi.org/10.3389/fcimb.2021.798575
Theuretzbacher U, Barbee L, Connolly K, Drusano G, Fernandes P, Hook E et al (2020) Pharmacokinetic/pharmacodynamic considerations for new and current therapeutic drugs for uncomplicated gonorrhoea—challenges and opportunities. Clin Microbiol Infect 26:1630–1635. https://doi.org/10.1016/j.cmi.2020.08.006
McMullan BK, Mostaghim M (2015) Prescribing azithromycin. Aust Prescr 1(38):87–89. https://doi.org/10.18773/austprescr.2015.030
Vacca P, Fazio C, Neri A, Ambrosio L, Palmieri A, Stefanelli P (2018) Neisseria meningitidis antimicrobial resistance in Italy, 2006 to 2016. Antimicrob Agents Chemother 62. https://doi.org/10.1128/AAC.00207-18
Willerton L, Lucidarme J, Walker A, Lekshmi A, Clark SA, Walsh L et al (2021) Antibiotic resistance among invasive Neisseria meningitidis isolates in England, Wales and Northern Ireland (2010/11 to 2018/19). PLoS ONE 1:16. https://doi.org/10.1371/journal.pone.0260677
Arreaza L, de La Fuente L, Vázquez JA (2000) Antibiotic susceptibility patterns of Neisseria meningitidis isolates from patients and asymptomatic carriers. Antimicrob Agents Chemother 44:1705–1707. https://doi.org/10.1128/AAC.44.6.1705-1707.2000
Nacional de Epidemiología Instituto de Salud Carlos III Ministerio de Ciencia Innovación C (2018) Resultados de la Vigilancia Epidemiológica de las enfermedades transmisibles. Informe anual. Años 2017–2018 [Internet]. http://publicaciones.isciii.es. Accessed 01 Oct 2022
Harrison OB, Cole K, Peters J, Cresswell F, Dean G, Eyre DW et al (2017) Genomic analysis of urogenital and rectal Neisseria meningitidis isolates reveals encapsulated hyperinvasive meningococci and coincident multidrug-resistant gonococci. Sex Transm Infect 93:445–451. https://doi.org/10.1136/sextrans-2016-052781
Nuttens C, Findlow J, Balmer P, Swerdlow DL, Tin Tin Htar M (2022) Evolution of invasive meningococcal disease epidemiology in Europe, 2008 to 2017. Euro Surveill 27. https://doi.org/10.2807/1560-7917.ES.2022.27.3.2002075
Chen M, Harrison OB, Bratcher HB, Bo Z, Jolley KA, Rodrigues CMC et al (2021) Evolution of sequence type 4821 clonal complex hyperinvasive and quinolone-resistant meningococci. Emerg Infect Dis 27:1110–1122. https://doi.org/10.3201/eid2704.203612
Freudenburg-de Graaf W, Knol MJ, van der Ende A (2020) Predicted coverage by 4CMenB vaccine against invasive meningococcal disease cases in the Netherlands. Vaccine 38:7850–7857. https://doi.org/10.1016/j.vaccine.2020.10.008
Acknowledgements
The authors would like to thank all the patients, clinicians, and nurses at the Álvaro Cunqueiro Infectious Disease Unit without whom this work would not have been possible.
Funding
This research did not receive any specific funding grants from any agencies in the public, commercial, or not-for-profit sectors. Alexandre Pérez is employed on a Rio Hortega contract, financed by the Instituto de Salud Carlos III, file number CM20/00243.
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APG and CP conceptualised the study, APG planned the statistical analysis with input from CP and RC. APG, AAA, and AO designed the database and performed the data curation. RA and CN performed the Nm identification and molecular characterisation. CP and RC performed the cultures and antimicrobial susceptibility tests of Nm isolates. APG wrote the original manuscript draft, and EP and RA revised it for important intellectual content. All the authors have approved the final version of this article.
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All the procedures performed in studies involving human participants were conducted in accordance with the ethical standards of the institutional research committee at Galicia and complied with the 1964 declaration of Helsinki and its later amendments or comparable ethical standards. This work was approved by the Ethics Committee of Pontevedra-Vigo-Ourense with reference number 2021/311.
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Pérez-González, A., Carballo, R., Araújo-Ameijeiras, A. et al. Meningococcal carriage in men who have sex with men presenting at a sexual health unit in Spain. Eur J Clin Microbiol Infect Dis 42, 287–296 (2023). https://doi.org/10.1007/s10096-023-04550-8
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DOI: https://doi.org/10.1007/s10096-023-04550-8