Sabine Wicker and Gregory Poland, Vaccine, May 2012
Global measles cases have declined dramatically over the last decade, to a new “low” of an estimated 20 million cases annually, with 164,000 deaths. Unfortunately, however, this obscures an important trend worth noting. In the U.S., much of Europe, and elsewhere, the number of measles cases has been increasing as parts of the population and even healthcare personnel (HCP) fail to be immunized , as well as among those who received vaccine, but experienced primary or secondary vaccine failure. In 2011, the U.S. had more recognized measles cases (an estimated 244) than in any of the past 10 years. This is in spite of the fact that in the U.S., measles was declared eliminated in 2000 . Among 33 European countries, more than 30,000 known cases have recently occurred .
Importantly, the goal of eliminating measles by 2010 has not been achieved and it is very unlikely that this will be achieved by 2015, which is the new WHO target for elimination of measles . Multiple previous measles elimination goals have been set, and none have been met.
Among the difficulties in measles elimination and eradication is the fact that measles is the most transmissible human disease known, requiring very high population-level immunity. For this reason, even a single case of measles in a healthcare setting can result in a nosocomial outbreak and deserves immediate action . Given their professional duties, and the increasing numbers of cases to which they may be exposed, it is not surprising that HCP are at substantially higher risk than the general population for becoming infected with measles, and transmission occurs within medical facilities due to HCP [6–11]. In one study, HCP were 19 times more likely to be infected than other adults . During the measles resurgence of 1989–1991, medical settings constituted a highly significant site of measles transmission [6,12,13]. Despite this, only three states in the U.S. mandate that hospital personnel be immune to measles [6,14]. Importantly, non-immune HCP pose a risk to themselves and to others (e.g., patients, colleagues, and family); therefore, the moral, ethical, and perhaps legal onus for protection lies not only with occupational vaccination programs in the institutions within which HCP work, but also with HCP themselves.
Current recommendations in the U.S. for HCP are that all “HCP who work in medical facilities should be immune to measles, mumps, and rubella .” HCP who were born in 1957 or later are considered immune only if they have laboratory confirmation of immunity or documentation of having received two appropriate doses of vaccine. The recommendations go on to state that while birth prior to 1957 is acceptable evidence of immunity, “healthcare facilities should consider recommending two doses of MMR vaccine routinely to unvaccinated HCP who do not have laboratory evidence of immunity .” Two doses of measles vaccine provide long-lasting immunity in nearly all recipients; a two-dose vaccine effectiveness of 99% has been described by the Centers for Disease Control and Prevention , but we would contend that these estimates are inflated by results from highly controlled clinical trials, and not routine field use in clinical practice. Nonetheless, for HCPs who have two documented doses of measles vaccine, serologic testing is not recommended by the Advisory Committee on Immunization Practices (ACIP) .
Similarly, the German Standing Committee on Vaccination (STIKO) does not recommend serologic testing for HCP. In Germany a two-dose measles vaccination program (first dose at age 11–14 months and a second dose between 15 and 23 months) is recommended.
In addition, HCP who were born after 1970 and who do not know their vaccination status, or who have never been vaccinated against measles or who have been vaccinated only once during childhood, should receive one additional measles vaccination. Remarkably, in Europe only Finland has established a policy for mandatory measles vaccination for HCP. At the current time half of European countrieshave no recommendations or requirements for HCP measles vaccination .However, as discussed, measles vaccines are not 100% protective
against subsequent disease, and in part this relates to evidence of both primary and secondary vaccine failure . Published formal clinical trials demonstrating extremely high rates of seroprotection are not directly generalizable to the general population. In clinical trials, clinical subjects are healthy and highly selected, and vaccines are stored and administered according to strict protocols that are not in place during routine field or clinical use. In a variety of studies, for example, measles vaccine has had a failure rate measured at 2–10% and immunity can and does wane over time allowing for future infection upon exposure [9–11,13,18–20]. For this reason,measles outbreaks have been reported in highly vaccinated communities, and this seeming paradox has been previously discussed [21,22]. In a measles outbreak in Canada, more than 50% of the 98 individuals involved had received two previous doses of measles vaccine [22,23] and measles infections have been described even after three doses of vaccine .
This is clear evidence of the need for a second generation, more highly immunogenic measles vaccine, ideally only requiring a single dose .
Chen et al. recommended that “because performing rapid serology testing during an outbreak is costly and disruptive, healthcare facilities should have serologic evidence of immunity available for all HCP to facilitate rapid vaccination response during a measles outbreak .” However, the sensitivity of the various serologic tests might distort the actual rate of humoral immunity, as different laboratories use different assays for measuring humoral immunity (i.e., neutralization assays, EIA assays, and indirect immunoflourescence assays, etc.), and HCP personal history of immunity may not be reliable . Too, it is important to note that serologic assays of humoral immunity appear to be independent of cellular immune responses to measles .
Measles is a serious global public and occupational health problem. Nosocomial outbreaks are costly and highly disruptive [8,9,20], and are associated with increased HCP absenteeism and medical leave, and more importantly with transmission to highly vulnerable patients. We believe that it is imperative that all HCP have documented and easily retrievable evidence of measles immunity to ensure case management and rapid outbreak response [6,9]. To protect the public and the patients we serve, receipt of appropriate measles immunization(s) should be mandatory, absent a valid medical contraindication, for all HCP. In addition, further thought must be given for requiring measles serology among individual HCP where the risk of non-immunity may be higher (i.e., HCP unable to receive vaccine, immunocompromised HCP, those HCP who received vaccine at an earlier than recommended age in infancy, or HCP who received vaccines of unknown efficacy, type, or handling in other countries). The data clearly demonstrating the higher risk of HCP being exposed to measles, the increasing number of recent cases, the associated morbidity and mortality of the disease, the economic costs of containing an outbreak, the extreme disruption of nosocomial measles, and the risk of transmission to patients and other healthcare staff, as well as the demonstrated safety and efficacy of the vaccine; provide a solid basis for such a mandate. HCP, their patients, fellow staff, and the public deserve to know that as a profession we take prevention of highly transmissible diseases seriously, and hold ourselves accountable to the highest possible standard to protect them.
Dr. Poland serves on a data management and safety committee for non-measles investigational vaccines being developed by Merck Research Laboratories. He also serves as the American College of Physician’s liaison member to the Advisory Committee on Immunization Practices.
Dr. Wicker is a member of the German Standing Committee on Vaccination (STIKO).
The views in this article are the personal views of the authors and do not necessarily represent the views of the professional organizations or institutions within which we are members.
© 2012 Elsevier Ltd. All rights reserved.
Editorial / Vaccine 30 (2012) 4407– 4408
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 Sepkowitz KA. Occupationally acquired infections in health care workers. Part I. Annals of Internal Medicine 1996;125(November (10)):826–34.
 Steingart KR, Thomas AR, Dykewicz CA, Redd SC. Transmission of measles virus in healthcare settings during a communitywide outbreak. Infection Control and Hospital Epidemiology 1999;20(February (2)):115–9.
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 Weber DJ, Consoli S, Sickbert-Bennett E, Miller MB, Rutala WA. Susceptibility to measles, mumps, and rubella in newly hired (2006–2008) healthcare workers born before 1957. Infection Control and Hospital Epidemiology 2010;31(June (6)):655–7.
 Ammari LK, Bell LM, Hodinka RL. Secondary measles vaccine failure in healthcare workers exposed to infected patients. Infection Control and Hospital Epidemiology 1993;14:81–6.
 Farizo KM, Stehr-Green PA, Simpson DM, Markowitz LE. Pediatric emergency room visits: a risk factor for acquiring measles. Pediatrics 1991;87(January (1)):74–9.
 Rivera ME, Mason WH, Ross LA, Wright Jr HT. Nosocomial measles infection in a pediatric hospital during a community-wide epidemic. Journal of Pediatrics 1991;119:183–6.
 Centers for Disease Control and Prevention. Immunization administration requirements for hospital employees for MMR; 2012. http://www.cdc.gov/print.do?url=http%3A%2F%2Fwww2a.cdc.gov%2Fnip%2FStateVaccApp%2FstatevaccsApp%2FAdministrationbyVaccine.asp%3FVaccinetmp%3DMMR
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 Willy ME, Koziol DE, Fleisher T, et al. Measles immunity in a population of healthcare workers. Infection Control and Hospital Epidemiology
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 Poland GA, Jacobson RM. Failure to reach the goal of measles elimination.
Apparent paradox of measles infections in immunized persons. Archives of Internal Medicine 1994;154:1815–20.
 De SG, Boulianne N, Defay F, et al. Higher risk of measles when the first dose of a two-dose schedule is given at 12–14 versus 15 months of age. Clinical Infectious Diseases 2012;(April).
 Poland GA, Jacobson RM. The re-emergence of measles in developed countries: time to develop the next-generation measles vaccines? Vaccine 2012;30(January (2)):103–4.
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 Wicker S, Allwinn R, Gottschalk R, Rabenau HF. Reliability of medical students’ vaccination histories for immunisable diseases. BMC Public Health 2008;8: 121.
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Gregory A. Poland∗
Mayo Vaccine Research Group, Mayo Clinic and Foundation, Rochester, MN 55905, United States
∗ Corresponding author. Tel.: +1 507 284 4968; fax:
10 May 2012
Pediatrics, Vol. 128 No. 3 September 1, 2011, pp. 435 -437
The First Measles Vaccine
Jeffrey P. Baker, MD, PhD
+ Author Affiliations
Department of Pediatrics, Duke University School of Medicine, Durham, North Carolina
Like in the more familiar story of polio vaccine, the development of the first successful live attenuated vaccine against measles began in the laboratory of John Enders. One of the greatest virologists of the 20th century, Enders pioneered the technique of viral tissue culture, which makes it possible to grow viruses in vitro in cells nourished in laboratory media.1 In 1949, he and his pediatric infectious disease fellows Thomas Weller and Frederick Robbins showed that poliovirus could be cultivated in tissue of nonneuronal origins, a discovery that set the stage for the first successful vaccines against the disease and led to a Nobel Prize in 1954.2 Enders himself was a remarkable character. He never tried to patent his work or share results with the media before peer review. He was consistently generous in sharing his knowledge with potential competitors, and despite his personal wealth he was equally known for his frugality; fellows learned to wash their own glassware, and every year the “chief” returned unspent grant money to the National Institutes of Health. Above all, Enders took seriously the role of mentor, rounding each day beside the benches of his select group of fellows with his bow tie, vest, and jacket asking, “Well, what's new?” A positive response was often rewarded by an hour-long conversation.3
In 1954, while the national field trials of Jonas Salk's polio vaccine captivated media attention, Enders and pediatrician Thomas Peebles successfully cultivated measles virus in human kidney cell culture for the first time.4 Ever-ingenious in finding sources for his tissue cultures, Enders obtained kidneys from a neurosurgeon colleague who treated hydrocephalus by performing a unilateral nephrectomy and connecting a shunt to carry cerebrospinal fluid to the ureter. Peebles traveled the Boston, Massachusetts, area with a throat swab in search of measles outbreaks in private boarding schools. His first, and most famous, success involved an 11-year-old boy named David Edmonston, whose name became attached to the strain that would become the source for the first measles vaccine.3
Enders decided to play a much more “hands-on” role with measles vaccine than he had with polio. He was unhappy with how the polio vaccine saga had unfolded after he had left its development to others. Less than a month after the Salk vaccine's approval and licensure in April 1955, it became apparent that some of the vaccine lots were contaminated with wild polio. The ensuing disaster, in which some 260 children developed paralytic polio from the vaccine, was widely blamed at the time on Cutter pharmaceuticals.5,6 Enders, however, believed Salk's own inactivation process had been at fault. He wanted to stay personally involved to be sure that the measles vaccine's development would proceed more smoothly.3
An immediate problem was to find a new human tissue culture system; Enders' neurosurgery colleague was no longer removing kidneys to place shunts. Two new members now joined the Enders team: the Yugoslav virologist Milan V. Milovanovic (who would later be put in charge of polio vaccine production in Yugoslavia) and a pediatric infectious disease fellow, Samuel L. Katz. Enders set his eyes on the placentas being discarded across the street by the Boston Lying-in Hospital: “There are those nice amnions that lie in the placenta,” he observed to his colleagues; “Let's do something with them.”3 Milovanovic and Katz set forth and returned with fresh placentas, from which they could peel off the amniotic membranes and trypsinize their cells to make beautiful cell cultures.
Because humans were the sole natural host of measles, Enders reasoned that the virus could be attenuated by being adapted to a nonhuman species. Earlier investigators had grown influenza, mumps, and yellow fever viruses in embryonated chick eggs; indeed, in the 1930s Max Theiler and Hugh Smith used this system to develop the attenuated yellow fever vaccine still used today.7 After some early false starts, Milovanovic and Katz succeeded in establishing measles vaccine in this system.8 The next step was to repeat this success in tissue cultures obtained by trypsinizing chick embryos. Although at first it was not clear whether anything was growing at all, characteristic cytopathic changes appeared in the fifth passage.3
After 3 years of work (involving 24 passages through human kidney tissue culture, 28 through human amniotic cell culture, 6 in fertilized hens' eggs, and 13 in chick embryo cell cultures), the investigators finally felt ready to test the modified Edmonston strain in monkeys. The injected monkeys developed a strong antibody response but no fever, viremia, or rash, which is consistent with successful attenuation.9
After more safety trials in monkeys, it was time to test the vaccine in humans. As the only physician on the team, Katz played an increasingly central role at that point. Following the time-honored tradition of autoexperimentation, the lead investigators first tested the strain on each other. Their antibody titers rose, and no adverse effects followed. Next, Enders and Katz approached the Walter E. Fernald State School near Waltham, Massachusetts. This was an institution typical of many others of the time that provided long-term custodial and medical care for severely handicapped children with conditions such as microcephaly, trisomy 21, and cerebral palsy. “They lived in dormitories,” Katz recollected, “and they had really severe outbreaks of measles every few years—not just with morbidity, but with mortality.”3
Conducting a clinical trial among institutionalized children raised significant ethical questions. Indeed, just 10 years earlier, the Fernald School had permitted nontherapeutic nutritional studies without informing families that their children were being given radioisotopes.10 Given that research ethics in the 1950s remained largely unregulated, some historians have argued that the Nuremberg code's powerful articulation of informed consent in 1946 had little impact on American research until the 1960s.11 In this light, it is notable that Katz explained the trial in person to every parent, and the ensuing article clearly stated that no child was given the vaccine without written parental consent.3,12
Every morning and afternoon Katz and technician Ann Holloway went to the school, examined the children, took throat swabs, and drew blood specimens. Returning to the laboratory, they attempted to detect measles virus from their samples but never did. A number of the children developed fevers and an evanescent rash but “seemed perfectly fine—in fact, it was a little bit like roseola,” Katz recounted. The children had nonetheless developed antibodies, and when the next measles outbreak struck the Fernald School, all of them were totally protected.3
Enders and Katz then recruited a number of colleagues from around the country to test the vaccine in children in other settings, both institutionalized and home-dwelling. The resulting articles appeared together in the New England Journal of Medicine on July 28, 1960. Written by figures who were on their way to becoming pediatric leaders in their own right, such as Saul Krugman, C. Henry Kempe, and Robert Haggerty, they joined those of Enders, Milovanovic, and Katz to provide an impressive justification of the first live measles vaccine.13
The subsequent story can only be traced briefly here. The Edmonston strain became the basis for the first measles vaccine licensed in the United States in 1963 and for the still-more attenuated products developed in the next several years by Anton Schwarz at Pitman Moore-Dow and Maurice Hilleman at Merck.14 By the end of the decade, the annual number of measles cases in the United States had decreased from several million to several thousand.15
Although the domestic eradication of measles proved to be more difficult than optimists in the late 1960s predicted, the remarkable safety record of measles vaccine (incorporated into Merck's MMR combination against measles, mumps, and rubella in 1971) is worth noting. In contrast to whole-cell pertussis and live polio vaccines, which were at the center of highly visible vaccine-safety controversies in the 1970s and 80s, measles vaccine enjoyed wide public acceptance. It figured prominently in the rise of school mandates as a strategy for promoting vaccination.16 Families who declined it did so not so much for reasons of safety than questioning the clinical severity of measles (as was the case, ironically, with David Edmonston's decision not to vaccinate his own son). 17
This long period of relatively little safety controversy ended abruptly with the rise of the MMR/autism controversy in 1997. Perhaps because Britain did not begin to routinely vaccinate infants with the MMR vaccine until the late 1980s, the vaccine began to be used on a widespread basis in that country at the same time that the number of autism cases were rising. The MMR vaccine/autism hypothesis has been discredited on many fronts. 18,19 For parents, one of the most intuitively persuasive objections may simply be the fact that the United States had used the MMR vaccine widely since the early 1970s and yet experienced no corresponding rise in autism cases.
From a global perspective, measles vaccine has been one of the greatest public health breakthroughs of the 20th century. It is fitting to think of its origins 50 years ago in the no-frills laboratory of a Connecticut Yankee scientist, John F. Enders.
Accepted June 21, 2011.
Address correspondence to Jeffrey P. Baker, MD, PhD, Trent Center for Bioethics, Humanities, and History of Medicine, Box 3040 DUMC, Durham, NC 27710. E-mail: firstname.lastname@example.org
FINANCIAL DISCLOSURE: The author has indicated he has no financial relationships relevant to this article to disclose.
1. Weller TH, Robbins FC John Franklin Enders. In: Biographical Memoirs, National Academy of Science. Vol 60. Washington, DC: National Academy Press; 1991:47–61
2. Enders JF, Weller TH, Robbins FC Cultivation of the Lansing strain of poliomyelitis virus in cultures of various human embryonic tissues. Science. 1949;109(2822):85–87
3. Baker JP Oral History Interview, Samuel L. Katz, March 7, 2002 [transcript at Pediatric History Center]. American Academy of Pediatrics: Elk Grove Village, IL; 2002
4. Enders JF, Peebles TC Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc Soc Exp Biol Med. 1954;86(2):277–286
5. Nathanson N, Langmuir AD The Cutter incident: poliomyelitis following formaldehyde-inactivated poliovirus vaccination in the United States during the spring of 1955. Am J Hyg. 1963;78:16–81
6. Offit PA The Cutter Incident: How America's First Polio Vaccine Led to the Growing Vaccine Crisis. New Haven, CT: Yale University Press; 2005
7. Theiler M Smith HH. Use of yellow fever virus modified by in vitro cultivation for human immunization. J Exp Med. 1937;65(6):787–800
8. Milovanovic MB, Enders JF, Mitus A Cultivation of measles virus in human amnion cells and in developing chick embryo. Proc Soc Exp Biol Med. 1957;95(1):120–127
9. Enders JF, Katz SL, Milovanovic MV, Holloway A Studies on an attenuated measles-virus vaccine. I. Development and preparation of the vaccine: technics for assay of effects of vaccination. N Engl J Med. 1960;263:153–159
10. Advisory Committee on Human Radiation Experiments. The Human Radiation Experiments: Final Report of the President's Advisory Committee. Oxford, United Kingdom: Oxford University Press; 1996:210–212
11. Rothman D Strangers at the Bedside: A History of How Law and Bioethics Transformed Medical Decision Making. New York, NY: Aldine de Gruyter; 2003
12. Katz SL, Enders JF, Holloway A Studies on an attenuated measles-virus vaccine: clinical, virological, and immunological effects of vaccine in institutionalized children. N Engl J Med. 1960;263:159–161
13. Katz SL, Kempe HC, Black FL, et al Studies on an attenuated measles vaccine: VIII. General summary and evaluation of results of vaccination. N Engl J Med. 1960;263:180–184
14. Galambos L, Sewell JE Networks of Innovation: Vaccine Development at Merck, Sharp, and Dohme, and Mulford, 1895–1995. Cambridge, United Kingdom: Cambridge University Press; 1995
15. Koprowski H, Oldstone MBA, Katz SL The history of measles vaccine of attempts to control measles. In: Koprowski H, Oldstone MBA eds. Microbe Hunters: Then and Now. Bloomington, IL: Medi-Ed Press; 1996:69–76
16. Colgrove J State of Immunity: The Politics of Vaccination in Twentieth-Century America. Berkeley, CA: University of California Press; 2006
17. Allen A Vaccine: The Controversial Story of Medicine's Greatest Lifesaver. New York, NY: WW Norton; 2007:247
18. Wakefield AJ, Murch SH, Anthony A, et al Ileal-lymphoid-nodular hyperplasia, non-specific colitis, and pervasive developmental disorder in children. Lancet. 1998;351(9103):637–641
19. Fitzpatrick M MMR and Autism. London, United Kingdom: Routledge; 2004
These weekly bulletins give regular updates on the progress of measles and rubella in the Americas.
These bimonthly newsletters give regular updates on routine immunization.
From the homepage of the GAVI Alliance:
WASHINGTON, D.C. 13 June 2012 — Seeking to address the devastating resurgence of measles, the GAVI Alliance will provide up to an additional US$ 162 million to control and prevent outbreaks in developing countries. This funding will help countries bridge critical gaps in their efforts to build sustainable systems to control this deadly disease.
GAVI will exceptionally make up to US$ 107 million available for measles control and prevention in six high-risk countries: Afghanistan, Chad, DR Congo, Ethiopia, Nigeria and Pakistan. A further US$ 55 million will be offered through the Measles & Rubella Initiative for rapid response vaccination campaigns in GAVI-eligible countries where outbreaks occur.
Delivering on the promise
Today's decision by the GAVI Board tops a year of progress outlined in a report card reviewing developments since GAVI's first pledging conference on 13 June 2011, at which donors pledged funding to immunise an additional 250 million children by 2015 to save four million lives.
By targeting measles we can have a major impact on health equity and ensure that people are protected against this disease no matter where they live.
Dagfinn Høybråten, Chair of the GAVI Alliance Board
The increased measles support, between now and 2017, will strengthen routine immunisation systems and follows a decision last November to provide more than US$ 600 million to tackle rubella through a combined measles-rubella (MR) vaccine. It is expected that 48 countries will introduce the MR vaccine by 2018 with GAVI’s support.
“By targeting measles we can have a major impact on health equity and ensure that people are protected against this disease no matter where they live,” said Dagfinn Høybråten, Chair of the GAVI Alliance Board. “This strategic investment is critical for the countries where children are at highest risk of infection.”
Canary in the coal mine
Measles is highly infectious and can cause serious illness, life-long disability, and death. In 1980, before widespread use of a global vaccine, an estimated 2.6 million people died worldwide. Increased routine vaccination has led to a 74% drop in measles mortality, from an estimated 535,000 deaths in 2000 to 139,000 in 2010. Rubella is the leading cause of vaccine-preventable birth defects leading to life-long disabilities.
In recent years, however, progress at further reducing the measles death toll has stalled due to outbreaks in Africa and a high disease burden in India.
“Measles is the ‘canary in the coal mine’ because outbreaks can signal that routine immunisation coverage is faltering,” said Dr Seth Berkley, CEO of the GAVI Alliance. “In order to eliminate measles, vaccine coverage must be at least 90 % so that adequate herd immunity is created. Fighting back when outbreaks occur and ensuring high routine coverage are critical to controlling measles and all other vaccine-preventable diseases.”
Over the past year, a growing number of new private donors have joined GAVI’s mission. The Church of Jesus Christ of Latter-day Saints announced a US$ 1.5 million gift yesterday, which was doubled through the GAVI Matching Fund by the Bill & Melinda Gates Foundation. The gift makes the Church-sponsored LDS Charities the seventh partner in the programme.