Advancing vaccine development for gonorrhoea and the Global STI Vaccine Roadmap
Sami L. Gottlieb
A F , Ann E. Jerse B , Sinead Delany-Moretlwe C , Carolyn Deal D and Birgitte K. Giersing E
+ Author Affiliations
- Author Affiliations
A Department of Reproductive Health and Research, World Health Organization, Avenue Appia 20, 1211 Geneva, Switzerland.
B Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD 20814, USA.
C Wits RHI, University of the Witwatersrand, 22 Esselen Street, 2001 Johannesburg, South Africa.
D National Institute of Allergy and Infectious Diseases, National Institutes of Health, 5601 Fishers Lane, Bethesda, MD 20892, USA.
E Department of Immunizations, Vaccines, and Biologicals, World Health Organization, Avenue Appia 20, 1211 Geneva, Switzerland.
F Corresponding author. Email: gottliebs@who.int
Sexual Health 16(5) 426-432 https://doi.org/10.1071/SH19060
Submitted: 25 March 2019 Accepted: 13 May 2019 Published: 3 September 2019
Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND
Abstract
Efforts to develop vaccines against Neisseria gonorrhoeae have become increasingly important, given the rising threat of gonococcal antimicrobial resistance (AMR). Recent data suggest vaccines for gonorrhoea are biologically feasible; in particular, epidemiological evidence shows that vaccines against a closely related pathogen, serogroup B Neisseria meningitidis outer membrane vesicle (OMV) vaccines, may reduce gonorrhoea incidence. Vaccine candidates using several approaches are currently in preclinical development, including meningococcal and gonococcal OMV vaccines, a lipooligosaccharide epitope and purified protein subunit vaccines. The Global STI Vaccine Roadmap provides action steps to build on this technical momentum and advance gonococcal vaccine development. Better quantifying the magnitude of gonorrhoea-associated disease burden, for outcomes like infertility, and modelling the predicted role of gonococcal vaccines in addressing AMR will be essential for building a full public health value proposition, which can justify investment and help with decision making about future vaccine policy and programs. Efforts are underway to gain consensus on gonorrhoea vaccine target populations, implementation strategies and other preferred product characteristics that would make these vaccines suitable for use in low- and middle-income, as well as high-income, contexts. Addressing these epidemiological, programmatic and policy considerations in parallel to advancing research and development, including direct assessment of the ability of meningococcal B OMV vaccines to prevent gonorrhoea, can help bring about the development of viable gonococcal vaccines.
Additional keywords: antimicrobial resistance, gonococcal infection, Neisseria gonorrhoeae, sexually transmitted infections, STI vaccines.
References
[1] World Health Organization. Report on global sexually transmitted infection surveillance, 2018. 2018. Available online at: https://www.who.int/reproductivehealth/publications/stis-surveillance-2018/en/ [verified 1 July 2019].[2] Ndowa F, Lusti-Narasimhan M. The threat of untreatable gonorrhoea: implications and consequences for reproductive and sexual morbidity. Reprod Health Matters 2012; 20 76–82.
| The threat of untreatable gonorrhoea: implications and consequences for reproductive and sexual morbidity.Crossref | GoogleScholarGoogle Scholar | 23245412PubMed |
[3] 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 e0205863
| Adult gonorrhea, chlamydia and syphilis prevalence, incidence, treatment and syndromic case reporting in South Africa: estimates using the Spectrum-STI model, 1990–2017.Crossref | GoogleScholarGoogle Scholar | 30321236PubMed |
[4] Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC, et al Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. Lancet 1997; 349 1868–73.
| Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1.Crossref | GoogleScholarGoogle Scholar | 9217758PubMed |
[5] Hayes R, Watson-Jones D, Celum C, van de Wijgert J, Wasserheit J. Treatment of sexually transmitted infections for HIV prevention: end of the road or new beginning? AIDS 2010; 24 S15–26.
| Treatment of sexually transmitted infections for HIV prevention: end of the road or new beginning?Crossref | GoogleScholarGoogle Scholar | 21042049PubMed |
[6] World Health Organization. The gonococcal antimicrobial surveillance programme (GASP). 2019. Available online at: https://www.who.int/reproductivehealth/topics/rtis/gasp_network/en/ [verified 1 July 2019].
[7] Wi T, Lahra MM, Ndowa F, Bala M, Dillon JR, Ramon-Pardo P, et al Antimicrobial resistance in Neisseria gonorrhoeae: global surveillance and a call for international collaborative action. PLoS Med 2017; 14 e1002344
| Antimicrobial resistance in Neisseria gonorrhoeae: global surveillance and a call for international collaborative action.Crossref | GoogleScholarGoogle Scholar | 28746372PubMed |
[8] Eyre DW, Sanderson ND, Lord E, Regisford-Reimmer N, Chau K, Barker L, et al Gonorrhoea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018. Euro Surveill 2018; 23 1800323
| Gonorrhoea treatment failure caused by a Neisseria gonorrhoeae strain with combined ceftriaxone and high-level azithromycin resistance, England, February 2018.Crossref | GoogleScholarGoogle Scholar | 29991383PubMed |
[9] World Health Organization (WHO). WHO publishes list of bacteria for which new antibiotics are urgently needed. [News release] 2017. Available online at: http://www.who.int/mediacentre/news/releases/2017/bacteria-antibiotics-needed/en/ [verified 1 July 2019].
[10] Kirkcaldy RD, Bolan GA, Wasserheit JN. Cephalosporin-resistant gonorrhea in North America. JAMA 2013; 309 185–7.
| Cephalosporin-resistant gonorrhea in North America.Crossref | GoogleScholarGoogle Scholar | 23299612PubMed |
[11] Jerse AE, Bash MC, Russell MW. Vaccines against gonorrhea: current status and future challenges. Vaccine 2014; 32 1579–87.
| Vaccines against gonorrhea: current status and future challenges.Crossref | GoogleScholarGoogle Scholar | 24016806PubMed |
[12] Petousis-Harris H, Paynter J, Morgan J, Saxton P, McArdle B, Goodyear-Smith F, et al Effectiveness of a group B outer membrane vesicle meningococcal vaccine against gonorrhoea in New Zealand: a retrospective case-control study. Lancet 2017; 390 1603–10.
| Effectiveness of a group B outer membrane vesicle meningococcal vaccine against gonorrhoea in New Zealand: a retrospective case-control study.Crossref | GoogleScholarGoogle Scholar | 28705462PubMed |
[13] Paynter J, Goodyear-Smith F, Morgan J, Saxton P, Black S, Petousis-Harris H. Effectiveness of a group B outer membrane vesicle meningococcal vaccine in preventing hospitalization from gonorrhea in New Zealand: a retrospective cohort study. Vaccines (Basel) 2019; 7 5
| Effectiveness of a group B outer membrane vesicle meningococcal vaccine in preventing hospitalization from gonorrhea in New Zealand: a retrospective cohort study.Crossref | GoogleScholarGoogle Scholar |
[14] Longtin J, Dion R, Simard M, Betala Belinga J-F, Longtin Y, Lefebvre B, et al Possible impact of wide-scale vaccination against serogroup B Neisseria meningitidis on gonorrhea incidence rates in one region of Quebec, Canada. Open Forum Infect Dis 2017; 4 S734–5.
| Possible impact of wide-scale vaccination against serogroup B Neisseria meningitidis on gonorrhea incidence rates in one region of Quebec, Canada.Crossref | GoogleScholarGoogle Scholar |
[15] Whelan J, Klovstad H, Haugen IL, Holle MR, Storsaeter J. Ecologic study of meningococcal B vaccine and Neisseria gonorrhoeae infection, Norway. Emerg Infect Dis 2016; 22 1137–9.
| Ecologic study of meningococcal B vaccine and Neisseria gonorrhoeae infection, Norway.Crossref | GoogleScholarGoogle Scholar | 27191543PubMed |
[16] Wellcome Trust and BCG. Vaccines to tackle drug resistant infections. An evaluation of R&D opportunities. Executive summary. 2018. Available online at: https://vaccinesforamr.org/read-the-report/ [verified 1 July 2019].
[17] Broutet N, Fruth U, Deal C, Gottlieb S, Rees H, participants of the 2013 STI Vaccine Technical Consultation Vaccines against sexually transmitted infections: the way forward. Vaccine 2014; 32 1630–7.
| Vaccines against sexually transmitted infections: the way forward.Crossref | GoogleScholarGoogle Scholar | 24480024PubMed |
[18] Gottlieb SL, Deal CD, Giersing B, Rees H, Bolan G, Johnston C, et al The global roadmap for advancing development of vaccines against sexually transmitted infections: update and next steps. Vaccine 2016; 34 2939–47.
| The global roadmap for advancing development of vaccines against sexually transmitted infections: update and next steps.Crossref | GoogleScholarGoogle Scholar | 27105564PubMed |
[19] Jain R, Sonkar SC, Chaudhry U, Bala M, Saluja D. In-silico hierarchical approach for the identification of potential universal vaccine candidates (PUVCs) from Neisseria gonorrhoeae. J Theor Biol 2016; 410 36–43.
| In-silico hierarchical approach for the identification of potential universal vaccine candidates (PUVCs) from Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 27596531PubMed |
[20] Zielke RA, Wierzbicki IH, Baarda BI, Gafken PR, Soge OO, Holmes KK, et al Proteomics-driven antigen discovery for development of vaccines against gonorrhea. Mol Cell Proteomics 2016; 15 2338–55.
| Proteomics-driven antigen discovery for development of vaccines against gonorrhea.Crossref | GoogleScholarGoogle Scholar | 27141096PubMed |
[21] Baarda BI, Zielke RA, Nicholas RA, Sikora AE. PubMLST for antigen allele mining to inform development of gonorrhea protein-based vaccines. Front Microbiol 2018; 9 2971
| PubMLST for antigen allele mining to inform development of gonorrhea protein-based vaccines.Crossref | GoogleScholarGoogle Scholar | 30581422PubMed |
[22] Semchenko EA, Tan A, Borrow R, Seib KL. The serogroup B meningococcal vaccine Bexsero elicits antibodies to Neisseria gonorrhoeae. Clin Infect Dis 2018;
| The serogroup B meningococcal vaccine Bexsero elicits antibodies to Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 30551148PubMed |
[23] Rice PA, Shafer WM, Ram S, Jerse AE. Neisseria gonorrhoeae: drug resistance, mouse models, and vaccine development. Annu Rev Microbiol 2017; 71 665–86.
| Neisseria gonorrhoeae: drug resistance, mouse models, and vaccine development.Crossref | GoogleScholarGoogle Scholar | 28886683PubMed |
[24] Connolly K, Leduc I, Rahman N, Sempowski G, Jerse A. The group B meningococcal vaccine Bexsero induces antibodies that recognize several candidate gonorrhea vaccine targets and shows protective efficacy against experimental Neisseria gonorrhoeae genital tract infection in mice. Proceedings of the 21st International Pathogenic Neisseria Conference; 23–28 September 2018; Pacific Grove, CA, USA. 2018; Abstract O10. Available online at: http://neisseria.org/ipnc/2018/IPNC2018_abstracts.pdf [verified 1 July 2019].
[25] Matthias K, Connolly K, Begum A, Jerse A, Bash M. Immunization with porin-deficient meningococcal outer membrane vesicles enhances gonococcal clearance in a mouse model of infection. Proceedings of the 21st International Pathogenic Neisseria Conference; 23–28 September 2018; Pacific Grove, CA, USA. 2018; Abstract O13. Available online at: http://neisseria.org/ipnc/2018/IPNC2018_abstracts.pdf [verified 1 July 2019].
[26] Liu Y, Hammer LA, Liu W, Hobbs MM, Zielke RA, Sikora AE, et al Experimental vaccine induces Th1-driven immune responses and resistance to Neisseria gonorrhoeae infection in a murine model. Mucosal Immunol 2017; 10 1594–608.
| Experimental vaccine induces Th1-driven immune responses and resistance to Neisseria gonorrhoeae infection in a murine model.Crossref | GoogleScholarGoogle Scholar | 28272393PubMed |
[27] Cates W, Farley TM, Rowe PJ. Worldwide patterns of infertility: is Africa different? Lancet 1985; 326 596–8.
| Worldwide patterns of infertility: is Africa different?Crossref | GoogleScholarGoogle Scholar |
[28] Vallely LM, Toliman P, Ryan C, Rai G, Wapling J, Gabuzzi J, et al Performance of syndromic management for the detection and treatment of genital Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis among women attending antenatal, well woman and sexual health clinics in Papua New Guinea: a cross-sectional study. BMJ Open 2017; 7 e018630
| Performance of syndromic management for the detection and treatment of genital Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis among women attending antenatal, well woman and sexual health clinics in Papua New Guinea: a cross-sectional study.Crossref | GoogleScholarGoogle Scholar | 29288183PubMed |
[29] Torrone EA, Morrison CS, Chen PL, Kwok C, Francis SC, Hayes RJ, et al Prevalence of sexually transmitted infections and bacterial vaginosis among women in Sub-Saharan Africa: an individual participant data meta-analysis of 18 HIV prevention studies. PLoS Med 2018; 15 e1002511
| Prevalence of sexually transmitted infections and bacterial vaginosis among women in Sub-Saharan Africa: an individual participant data meta-analysis of 18 HIV prevention studies.Crossref | GoogleScholarGoogle Scholar | 29944660PubMed |
[30] Toskin I, Blondeel K, Peeling RW, Deal C, Kiarie J. Advancing point of care diagnostics for the control and prevention of STIs: the way forward. Sex Transm Infect 2017; 93 S81–8.
| Advancing point of care diagnostics for the control and prevention of STIs: the way forward.Crossref | GoogleScholarGoogle Scholar | 29223966PubMed |
[31] Craig AP, Gray RT, Edwards JL, Apicella MA, Jennings MP, Wilson DP, et al The potential impact of vaccination on the prevalence of gonorrhea. Vaccine 2015; 33 4520–5.
| The potential impact of vaccination on the prevalence of gonorrhea.Crossref | GoogleScholarGoogle Scholar | 26192351PubMed |
[32] Régnier SA, Huels J. Potential impact of vaccination against Neisseria meningitidis on Neisseria gonorrhoeae in the United States: results from a decision-analysis model. Hum Vaccin Immunother 2014; 10 3737–45.
| Potential impact of vaccination against Neisseria meningitidis on Neisseria gonorrhoeae in the United States: results from a decision-analysis model.Crossref | GoogleScholarGoogle Scholar | 25483706PubMed |
[33] Fingerhuth SM, Bonhoeffer S, Low N, Althaus CL. Antibiotic-resistant Neisseria gonorrhoeae spread faster with more treatment, not more sexual partners. PLoS Pathog 2016; 12 e1005611
| Antibiotic-resistant Neisseria gonorrhoeae spread faster with more treatment, not more sexual partners.Crossref | GoogleScholarGoogle Scholar | 27196299PubMed |
[34] Geisler WM, Lensing SY, Press CG, Hook EW. Spontaneous resolution of genital Chlamydia trachomatis infection in women and protection from reinfection. J Infect Dis 2013; 207 1850–6.
| Spontaneous resolution of genital Chlamydia trachomatis infection in women and protection from reinfection.Crossref | GoogleScholarGoogle Scholar | 23470847PubMed |
[35] Hobbs MM, Sparling PF, Cohen MS, Shafer WM, Deal CD, Jerse AE. Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkc. Front Microbiol 2011; 2 123
| Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkc.Crossref | GoogleScholarGoogle Scholar | 21734909PubMed |
[36] Lewis DA. Will targeting oropharyngeal gonorrhoea delay the further emergence of drug-resistant Neisseria gonorrhoeae strains? Sex Transm Infect 2015; 91 234–7.
| Will targeting oropharyngeal gonorrhoea delay the further emergence of drug-resistant Neisseria gonorrhoeae strains?Crossref | GoogleScholarGoogle Scholar | 25911525PubMed |
[37] World Health Organization (WHO). WHO preferred product characteristics (PPCs). 2019. Available online at: http://www.who.int/immunization/research/ppc-tpp/preferred_product_characteristics/en/ [verified 1 July 2019].
[38] Gottlieb SL, Giersing BK, Hickling J, Jones R, Deal C, Kaslow DC, WHO HSV Vaccine Expert Consultation Group. Meeting report: Initial World Health Organization consultation on herpes simplex virus (HSV) vaccine preferred product characteristics, March 2017. Vaccine 2017;
| Meeting report: Initial World Health Organization consultation on herpes simplex virus (HSV) vaccine preferred product characteristics, March 2017.Crossref | GoogleScholarGoogle Scholar | 29224963PubMed |
[39] Vallely LM, Toliman P, Ryan C, Rai G, Wapling J, Tomado C, et al Prevalence and risk factors of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis and other sexually transmissible infections among women attending antenatal clinics in three provinces in Papua New Guinea: a cross-sectional survey. Sex Health 2016; 13 420–7.
| Prevalence and risk factors of Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis and other sexually transmissible infections among women attending antenatal clinics in three provinces in Papua New Guinea: a cross-sectional survey.Crossref | GoogleScholarGoogle Scholar | 28636866PubMed |
[40] Torrone EA, Johnson RE, Tian LH, Papp JR, Datta SD, Weinstock HS. Prevalence of Neisseria gonorrhoeae among persons 14 to 39 years of age, United States, 1999 to 2008. Sex Transm Dis 2013; 40 202–5.
| Prevalence of Neisseria gonorrhoeae among persons 14 to 39 years of age, United States, 1999 to 2008.Crossref | GoogleScholarGoogle Scholar | 23407466PubMed |
[41] Hoots BE, Torrone EA, Bernstein KT, Paz-Bailey G, NHBS Study Group. Self-reported chlamydia and gonorrhea testing and diagnosis among men who have sex with men – 20 US cities, 2011 and 2014. Sex Transm Dis 2018; 45 469–75.
| 29465659PubMed |
[42] Hoover KW, Butler M, Workowski KA, Follansbee S, Gratzer B, Hare CB, et al Low rates of hepatitis screening and vaccination of HIV-infected MSM in HIV clinics. Sex Transm Dis 2012; 39 349–53.
| Low rates of hepatitis screening and vaccination of HIV-infected MSM in HIV clinics.Crossref | GoogleScholarGoogle Scholar | 22504597PubMed |
[43] Jansen KU, Knirsch C, Anderson AS. The role of vaccines in preventing bacterial antimicrobial resistance. Nat Med 2018; 24 10–19.
| The role of vaccines in preventing bacterial antimicrobial resistance.Crossref | GoogleScholarGoogle Scholar | 29315295PubMed |
[44] Royal Society. The value of vaccines in the avoidance of antimicrobial resistance. Centre on Global Health Security meeting summary. 2017. Available online at: https://www.chathamhouse.org/sites/default/files/events/2017-03-30-amr-vaccines-meeting-summary.pdf [verified 1 July 2019].
[45] Dodet B. Current barriers, challenges and opportunities for the development of effective STI vaccines: point of view of vaccine producers, biotech companies and funding agencies. Vaccine 2014; 32 1624–9.
| Current barriers, challenges and opportunities for the development of effective STI vaccines: point of view of vaccine producers, biotech companies and funding agencies.Crossref | GoogleScholarGoogle Scholar | 23994377PubMed |
[46] Shewell LK, Ku SC, Schulz BL, Jen FE, Mubaiwa TD, Ketterer MR, et al Recombinant truncated AniA of pathogenic Neisseria elicits a non-native immune response and functional blocking antibodies. Biochem Biophys Res Commun 2013; 431 215–20.
| Recombinant truncated AniA of pathogenic Neisseria elicits a non-native immune response and functional blocking antibodies.Crossref | GoogleScholarGoogle Scholar | 23313483PubMed |
[47] Wang S, Xue J, Lu P, Ni C, Cheng H, Han R, et al Gonococcal MtrE and its surface-expressed Loop 2 are immunogenic and elicit bactericidal antibodies. J Infect 2018; 77 191–204.
| Gonococcal MtrE and its surface-expressed Loop 2 are immunogenic and elicit bactericidal antibodies.Crossref | GoogleScholarGoogle Scholar | 29902495PubMed |
[48] Jen FE, Semchenko EA, Day CJ, Seib KL, Jennings MP. The Neisseria gonorrhoeae methionine sulfoxide reductase (msra/b) is a surface exposed, immunogenic, vaccine candidate. Front Immunol 2019; 10 137
| The Neisseria gonorrhoeae methionine sulfoxide reductase (msra/b) is a surface exposed, immunogenic, vaccine candidate.Crossref | GoogleScholarGoogle Scholar | 30787927PubMed |
[49] Plante M, Jerse A, Hamel J, Couture F, Rioux CR, Brodeur BR, et al Intranasal immunization with gonococcal outer membrane preparations reduces the duration of vaginal colonization of mice by Neisseria gonorrhoeae. J Infect Dis 2000; 182 848–55.
| Intranasal immunization with gonococcal outer membrane preparations reduces the duration of vaginal colonization of mice by Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 10950780PubMed |
[50] Freixeiro P, Connolly K, Sánchez-Busó L, Rossi O, Unemo M, Harris S, et al. A genetically-modified native outer membrane vesicle vaccine administered by a subcutaneous/intranasal route failed to accelerate clearance of gonococcus in a heterologous mouse challenge study. Proceedings of the 21st International Pathogenic Neisseria Conference; 23–28 September 2018; Pacific Grove, CA, USA. 2018; Abstract OP174. Available online at: http://neisseria.org/ipnc/2018/IPNC2018_abstracts.pdf [verified 1 July 2019].
[51] Gulati S, Zheng B, Reed GW, Su X, Cox AD, St Michael F, et al Immunization against a saccharide epitope accelerates clearance of experimental gonococcal infection. PLoS Pathog 2013; 9 e1003559
| Immunization against a saccharide epitope accelerates clearance of experimental gonococcal infection.Crossref | GoogleScholarGoogle Scholar | 24009500PubMed |
[52] Gulati S, McQuillen DP, Sharon J, Rice PA. Experimental immunization with a monoclonal antiidiotope antibody that mimics the Neisseria gonorrhoeae lipooligosaccharide epitope 2C7. J Infect Dis 1996; 174 1238–48.
| Experimental immunization with a monoclonal antiidiotope antibody that mimics the Neisseria gonorrhoeae lipooligosaccharide epitope 2C7.Crossref | GoogleScholarGoogle Scholar | 8940214PubMed |
[53] Shewell LK, Jen FE-C, Jennings MP. Refinement of immunizing antigens to produce functional blocking antibodies against the AniA nitrite reductase of Neisseria gonorrhoeae. PLoS One 2017; 12 e0182555
| Refinement of immunizing antigens to produce functional blocking antibodies against the AniA nitrite reductase of Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 28771632PubMed |
[54] Jen FE, Semchenko EA, Day CJ, Seib KL, Jennings MP. The Neisseria gonorrhoeae methionine sulfoxide reductase (MsrA/B) is a surface exposed, immunogenic, vaccine candidate. Front Immunol 2019; 10 137
| The Neisseria gonorrhoeae methionine sulfoxide reductase (MsrA/B) is a surface exposed, immunogenic, vaccine candidate.Crossref | GoogleScholarGoogle Scholar | 30787927PubMed |
[55] Price GA, Masri HP, Hollander AM, Russell MW, Cornelissen CN. Gonococcal transferrin binding protein chimeras induce bactericidal and growth inhibitory antibodies in mice. Vaccine 2007; 25 7247–60.
| Gonococcal transferrin binding protein chimeras induce bactericidal and growth inhibitory antibodies in mice.Crossref | GoogleScholarGoogle Scholar | 17720283PubMed |
[56] Zhu W, Chen CJ, Thomas CE, Anderson JE, Jerse AE, Sparling PF. Vaccines for gonorrhea: can we rise to the challenge? Front Microbiol 2011; 2 124
| Vaccines for gonorrhea: can we rise to the challenge?Crossref | GoogleScholarGoogle Scholar | 21687431PubMed |
[57] Wang L, Xing D, Le Van A, Jerse AE, Wang S. Structure-based design of ferritin nanoparticle immunogens displaying antigenic loops of Neisseria gonorrhoeae. FEBS Open Bio 2017; 7 1196–207.
| Structure-based design of ferritin nanoparticle immunogens displaying antigenic loops of Neisseria gonorrhoeae.Crossref | GoogleScholarGoogle Scholar | 28781959PubMed |
[58] Gala RP, Zaman RU, D’Souza MJ, Zughaier SM. Novel whole-cell inactivated Neisseria gonorrhoeae microparticles as vaccine formulation in microneedle-based transdermal immunization. Vaccines (Basel) 2018; 6 60
| Novel whole-cell inactivated Neisseria gonorrhoeae microparticles as vaccine formulation in microneedle-based transdermal immunization.Crossref | GoogleScholarGoogle Scholar |
