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The Development of Vaccines: How the Past Led to the Future PERSPECTIVES In the last decade of the nineteenth TIMELINE century, vaccine development started to have a rationale. The science was produced The development of vaccines: by workers in Great Britain, Germany, the United States and Pasteur’s laboratory in how the past led to the future France. The key developments were methods to inactivate whole bacteria, which could then be used as vaccines, the discovery of Stanley A. Plotkin and Susan L. Plotkin bacterial toxins, the production of antitoxins Abstract | The history of vaccine development has seen many accomplishments, and the realization that immune serum con- tained substances (antibodies) that neutral- but there are still many diseases that are difficult to target, and new technologies ized toxins or bacterial replication. Daniel are being brought to bear on them. Past successes have been largely due to Salmon and Theobald Smith were the first to elicitation of protective antibodies based on predictions made from the study of inactivate bacteria, and wrote: “Immunity is animal models, natural infections and seroepidemiology. Those predictions have the result of exposure of … the animal body often been correct, as indicated by the decline of many infections for which to the chemical products of the growth of specific microbes which constitute the virus vaccines have been made over the past 200 years. of contagious fever.” (REF. 17.) Furthermore, during the last years of the nineteenth It is said that only those who have seen the complexions of milkmaids and inferred that century and the beginning of the twentieth, beginning of things can understand the cowpox protected them from the ravages of inactivated whole-cell vaccines against present. As the development of vaccines con- smallpox. Jesty inoculated his own family6, typhoid18, cholera19 and plague20 were tinues in the twenty-first century, and as it but Jenner carried out what passed for clini- produced and tested. is now over 215 years since vaccinology was cal trials in the eighteenth century and then The key workers responsible for develop- launched by Edward Jenner’s observations of broadcast the results to the world7,8. There ing the concept of serum antibody include the powers of cowpox to prevent smallpox, ensued a rapid spread of inoculation, using Emil von Behring, Shibasaburo Kitasato, it is useful to contemplate the past. This is all material obtained from poxvirus lesions on Émile Roux, Alexandre Yersin, Almwroth the more true because there is a great deal the arms of humans9,10. To this day, we do Wright and Paul Ehrlich. In 1888, Roux and of forward gazing, with an explosion of new not know the origin of the virus that Jenner Yersin demonstrated that diphtheria bacilli potential strategies for vaccine development called vaccinia, which may have been a now- produce an exotoxin21, and 2 years later von based on genetic engineering, and the hope extinct strain of horsepox11,12, but its use was Behring and Kitasato showed that an anti- that systems biology and structural biology adopted in all parts of the world, culminating toxin was induced in the sera of animals that will tell us which genes must be upregulated in the eradication of smallpox. had received sublethal doses of the toxin22. or downregulated and what antigenic con- However, 80 years were to pass before Von Behring summarized both the practical structions are needed to achieve a protective the next step in the history of vaccines, and theoretical facets of the work by saying: immune response1–4. However, as the future which was taken in the laboratory of Louis “Briefly expressed, serum therapy works unfolds, the past is sometimes deprecated, a Pasteur. The story that his discovery of through antibodies.” (REF. 23.) Ehrlich, in fact that is conveyed in recent expressions by attenuation — using the causative organ- particular, thoroughly developed the con- two distinguished individuals: “What hap- ism of chicken cholera, now known as cept of antibody as being complementary to pened in the past is that most vaccines have Pasteurella multocida — was an accident has antigen24. been made empirically without a real immu- gained currency13,14. That story is disputed In 1923, Alexander Glenny and Barbara nologic rationale” (REF. 5) and “We really don’t but, whether by accident or premeditation, Hopkins showed that diphtheria toxin can know how to make vaccines in a predictable Pasteur learned that he could attenuate a be converted into a toxoid by the action of way. It’s still a little bit of black magic” (REF. 5). bacterium by exposure to adverse condi- formalin25. Its toxicity was thus reduced, but Although those statements are true of the tions. His work on anthrax and rabies it was well tolerated only in combination early history of vaccines, they have not been followed from that discovery15,16, but with antitoxin. A stable, non-toxic, formalin- true for most of the twentieth century, as we his theoretical basis for attenuation was inactivated diphtheria antigen was finally show below. completely wrong. Pasteur thought that produced by Gaston Ramon26. resistance was due to the depletion of an In the early years of the twentieth The beginning element that was crucial to the growth of an century, it became clear that the passage First, let us return to the 1700s, when both organism. Nevertheless, although he did not of organisms in unnatural hosts results the farmer Benjamin Jesty and the physician understand what the vaccines were doing, in genetic selection for avirulent strains. Edward Jenner paid attention to the unsullied the practical results achieved were epochal. Thus, the Mycobacterium bovis bacille NATURE REVIEWS | MICROBIOLOGY VOLUME 9 | DECEMBER 2011 | 889 © 2011 Macmillan Publishers Limited. All rights reserved PERSPECTIVES Timeline | A history of vaccine development Tick-borne encephalitis Tuberculosis Pneumococcal (Mycobacterium Anthrax disease Hepatitis B Tetanus bovis bacille Polio (injected, (secreted (pneumococcal (plasma Smallpox Typhoid Plague (toxoid) Calmette-Guérin) Influenza inactivated) Mumps (live) proteins) polysaccharides) derived) 1798 1885 1886 1896 1897 1923 1924 1926 1927 1935 1936 1938 1955 1963 1967 1969 1970 1974 1977 1980 1981 1985 1986 1987 1989 1991 1992 1993 1994 1995 1996 1998 1999 2000 2003 2005 2006 2009 2010 Rabies Cholera Diphtheria (toxoid) Pertussis Yellow fever Typhus Polio (oral, live) Rubella Meningococcal Adenovirus infection (live) disease (live) Measles (live) (meningococcal polysaccharides) Rabies (cell culture) *Capsular polysaccharide conjugated to carrier proteins. ‡Killed, recombinant B subunit, whole-cell vaccine. §Cholera toxin B combined with enterotoxigenic Escherichia coli. ||Now withdrawn. Calmette–Guérin vaccine was obtained by Wilson Smith, one of the discoverers of applied to vaccine development40. The 230 serial passages of M. bovis over a period influenza virus, used the ferret as an experi- 1950s was the era of the great poliovirus of 14 years, on artificial medium containing mental animal to show that prior infection vaccine controversies, during which both bile. Albert Calmette and Camille Guérin by influenza virus induces immunity to an inactivated vaccine and a live vaccine demonstrated that the resulting mutant future challenge36. However, by the 1940s it were developed, the former by Jonas Salk41 protected animals and infants against was clear that there is more than one influ- and the latter by Albert Sabin42. Salk had Mycobacterium tuberculosis, although the enza virus strain and that antigenic variation learned about virus inactivation from his basis for protection was unknown27,28. occurs frequently, rendering earlier vaccines prior work on the influenza virus vac- ineffective37. Routine vaccination with inac- cine, and Sabin’s selection of attenuated Viruses tivated influenza virus or, later, with viral mutants in cell culture followed Hilary Filterable agents, which were subsequently haemagglutinin is based on the protection Koprowski’s attenuation of poliovirus called viruses, were also described in the afforded by haemagglutination-inhibiting type 2 by passage in mice43. In both cases last years of the nineteenth century. At antibodies. Nevertheless, antigenic varia- it was understood that antibodies against this time, yellow fever was an important tion continues to be a problem, and cur- the three types of poliovirus would protect problem in Africa, and many scientists rent research is directed towards finding individuals, because prior successful trials sought to attenuate the virus. The yellow conserved antigens. In addition, building had demonstrated the prophylactic power fever virus strain 17D was selected from a on the work that was initially carried out in of immunoglobulins44. virulent strain by Max Theiler by serial pas- the former Soviet Union38, an intranasally In the 1960s, three classical attenuated- sage in minced chicken embryo and then in administered live attenuated influenza virus virus vaccines were developed: against mea- embryonated chicken eggs29,30. The goal was vaccine is now in use39. This vaccine is effec- sles virus, by Samuel Katz and John Enders45; to eliminate neurovirulence, and for animals tive because it induces secretory immuno- mumps virus, by Maurice Hilleman46; and this was lost between the eighty-ninth and globulin A in the nasopharynx and serum, rubella virus, by several workers (including one hundred and seventy-sixth passages, but as well as cytotoxic T cell responses against S.A.P.)47–49. These were all developed by pas- the attenuated virus still elicited neutralizing the virus. sage in embryonated eggs or cell culture, and antibodies that protected monkeys from in the case of rubella virus, passage in cells 29–31 o challenge with a virulent virus . The vac- In the last decade of the incubated at 30 C selected for attenuation. cine made with yellow fever virus strain 17D In all three cases, it had been established became a major public health success. nineteenth century, vaccine using passive administration that the pres- At about the same time, two additional development started to have a ence of neutralizing antibodies correlated vaccines came into use: the whole-cell rationale.
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