Rethinking next-generation vaccines for coronaviruses, influenzaviruses, and other respiratory viruses
Summary
Viruses that replicate in the human respiratory mucosa without infecting systemically, including influenza A, SARS-CoV-2, endemic coronaviruses, RSV, and many other “common cold” viruses, cause significant mortality and morbidity and are important public health concerns. Because these viruses generally do not elicit complete and durable protective immunity by themselves, they have not to date been effectively controlled by licensed or experimental vaccines. In this review, we examine challenges that have impeded development of effective mucosal respiratory vaccines, emphasizing that all of these viruses replicate extremely rapidly in the surface epithelium and are quickly transmitted to other hosts, within a narrow window of time before adaptive immune responses are fully marshaled. We discuss possible approaches to developing next-generation vaccines against these viruses, in consideration of several variables such as vaccine antigen configuration, dose and adjuventation, route and timing of vaccination, vaccine boosting, adjunctive therapies, and options for public health vaccination polices.
Introduction
(1) after first replicating mucosally, these systemic respiratory viruses all cause significant viremia that seeds an enormous number of infectious virions throughout the body, putting them in contact with multiple immune compartments and immune competent cell types,
(2) they have relatively long incubation periods that reflect initial mucosal replication and the subsequent systemic spread of infectious virions, which allows time for the induction of the full force of adaptive immunity, and
- (3) they elicit long-term or lifetime protective immunity (Table 1).
Table 1Epidemiologic and immunologic parameters of selected human respiratory viruses and vaccines used to control them
a Viral incubation periods, especially shorter incubation periods, typically have very broad ranges; these estimates are taken from cross-sections of the literature.
b Smallpox was eradicated from natural circulation in 1978.
c Varicella-zoster virus (VZV) recrudescence (referred to as zoster, zona, or “shingles”) results from release of latent viruses from ganglia; second exogenous respiratory infections in normal persons are rare.
d Although SARS-CoV-2 antigens have been detected in multiple tissues, the virus does not appear to be associated with significant “free” viremia, as evidenced by difficulty in culturing infectious virions from blood or tissues, and by weak elicitation of broad and durable protective systemic immunity.
Taking all of these factors into account, it is not surprising that none of the predominantly mucosal respiratory viruses have ever been effectively controlled by vaccines. This observation raises a question of fundamental importance: if natural mucosal respiratory virus infections do not elicit complete and long-term protective immunity against reinfection, how can we expect vaccines, especially systemically administered non-replicating vaccines, to do so? This is a major challenge for future vaccine development, and overcoming it is critical as we work to develop “next-generation” vaccines.
Table 2Key challenges in developing next-generation vaccines against mucosal respiratory viruses including SARS-CoV-2, influenza A viruses, and emerging pandemic and other viruses of importance
Natural infections with mucosal respiratory viruses may not be fully controlled by human immune responses because the human immune system has evolved to tolerate them during very short intervals of mucosal viral replication
Since mucosal and systemic immunity only partially protects against infection with mucosal respiratory viruses, we must take advantage of alternative host immune mechanisms
Immune correlates of protection against mucosal respiratory viruses are incompletely understood, vary between viral strains and subtypes, with viral drift, and they exhibit inter-individual variation
- •preventing infection entirely, as vaccines for systemic respiratory viruses may do (Table 1);
- •
limiting viral replication or preventing transmission as with influenza anti-neuraminidase immunity;
- •
preventing disease; or
- •
only preventing severe disease (e.g., requiring hospitalization), as appears to be the case with some influenza virus and SARS-CoV-2 vaccines.
Vaccine-related questions of route of administration, antigen configuration, adjuventation, and association with adjunctive therapy are of great importance for current research
- (1)Can non-replicating vaccines, which may be considerably less effective at eliciting IgA, be as efficacious as replicating vaccines, such as live-attenuated virus vaccines and live vaccine vectors expressing key viral proteins?
- (2)
Can single- or pauci-antigen vaccines provide protection equivalent to more antigenically complex vaccines?
- (3)
Can higher antigen doses or repeat vaccinations elicit better immunity?
- (4)What are the differential effects of soluble versus particulate antigens?
- (5)What are ideal relationships between vaccine antigen load and systemic or mucosal adjuventation?
- (6)What are the optimal strategies for routes and timing of vaccination: mucosal/systemic “prime-boost”? Newer strategies such as “prime-pull” and “prime-deploy” (vaccination strategies to elicit systemic T cell responses followed by recruitment of activated T cells via attractant or recruitment of resident memory T cells, respectively, to lung),,, and others?
Vaccinated hosts and host risk groups are many and heterogeneous
Public health considerations relating to next-generation respiratory vaccines must contribute to shaping vaccine design, including vaccine schedule, role of boosting, frequency of vaccination and duration/completeness of protection, side effects, and public acceptance
Once improved vaccines are developed, vaccine recipes and schedules will need to be optimized to best elicit durable protective mucosal immunity, especially with multivalent or boosted vaccines, for which antigen immunodominance and balance between humoral and cell-mediated immune responses may be complex.
Concluding remarks
Durably protective vaccines against non-systemic mucosal respiratory viruses with high mortality rates have thus far eluded vaccine development efforts.
Past unsuccessful attempts to elicit solid protection against mucosal respiratory viruses and to control the deadly outbreaks and pandemics they cause have been a scientific and public health failure that must be urgently addressed. We are excited and invigorated that many investigators and collaborative groups are rethinking, from the ground up, all of our past assumptions and approaches to preventing important respiratory viral diseases and working to find bold new paths forward.
Acknowledgments
This work was supported by the Intramural Research Program of the NIH and NIAID.
Declaration of interests
The authors declare no competing interests.
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