The Importance of MMR Immunization in the United States Olivia Perrone, MD, H. Cody Meissner, MD

Despite the established safety and efficacy of the measles-mumps-rubella abstract vaccine after almost 50 years of widespread use, the United States is encountering higher levels of measles and mumps disease than has occurred for years. Return of disease threatens the health of those who remain unimmunized by choice as well as those who are immunized appropriately but experience loss of vaccine-induced immunity. The solution to continued threats of illness caused by these untreatable but readily preventable diseases is compliance with recommendations for administration of the measles- mumps-rubella vaccine. Here we examine trends in the epidemiology of measles, mumps, and rubella in recent years and consider the consequences of loss of protective immunity within our country.

Department of Pediatrics, School of Medicine, Tufts University and Tufts Medical Center, Boston, Massachusetts

Growing concern among health care ∼97% effective in prevention of clinical Drs Perrone and Meissner conceptualized and designed the study, drafted the initial manuscript, professionals and the public regarding disease and is considered to provide fi 2 reviewed the revised manuscript, approved the nal the severity and the contagiousness of lifelong protection against rubella. In manuscript as submitted, and agree to be measles and mumps, 2 previously view of the availability of MMR, a safe accountable for all aspects of the work. controlled diseases in the United States, and effective vaccine, why does disease DOI: https://doi.org/10.1542/peds.2020-0251 has focused attention on the role of the still occur, and what can be done to Accepted for publication May 5, 2020 measles-mumps-rubella vaccine control the spread of measles, to (MMR). The number of reported control the outbreaks of mumps, and to Address correspondence to H. Cody Meissner, MD, Department of Pediatrics, School of Medicine, Tufts measles, mumps, and rubella cases sustain the elimination of rubella? University and Tufts Medical Center, 800 Washington decreased by .95% after introduction St, Boston, MA 02111. E-mail: cmeissner@ of each monovalent vaccine, yet disease tuftsmedicalcenter.org continues to occur nearly 50 years after MEASLES PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, the 3 vaccines were combined into Before measles vaccines were licensed 1098-4275). a single trivalent vaccine in 1971. in 1963, childhood infection with Copyright © 2020 by the American Academy of Measles occurs mainly among measles was nearly universal, resulting Pediatrics unimmunized people exposed to in an estimated 3 to 4 million cases FINANCIAL DISCLOSURE: The authors have indicated fi a contagious traveler who arrives from annually (the birth cohort), .500 they have no nancial relationships relevant to this article to disclose. a country outside the United States deaths, and thousands of cases of 1,2 FUNDING: where measles virus is circulating. measles-associated encephalitis in the No external funding. Mumps outbreaks occur after exposure United States.1 After licensure of the POTENTIAL CONFLICT OF INTEREST: Dr Meissner fi to an index case in settings where first measles vaccines, the incidence of serves as ex-of cio to the Committee on Infectious Diseases, is a member of the National Vaccine people have close, prolonged contact, disease declined rapidly. By 2000, the such as universities or close-knit Advisory Committee, is a member of the Vaccine and United States was certified to be free of Related Biological Products Advisory Committee, and communities, and may or may not have measles, meaning that after is chair of the Vaccine Injury Compensation Program; 2–4 received 2 doses of MMR. The importation of a case, no continuous and Dr Perrone has indicated she has no potential fl attenuated rubella virus contained in transmission occurred for at least 12 con icts of interest to disclose. MMR (Wistar RA 27/3) is more months. Between 1997 and 2013 the effective at inducing protective incidence of measles remained To cite: Perrone O and Meissner HC. The immunity than the measles or mumps remarkably low at ,1 case per 1 Importance of MMR Immunization in the United States. Pediatrics. 2020;146(2):e20200251 vaccine strains, and a single dose is million population.1 Starting in 2014,

Downloaded from www.aappublications.org/news by guest on October 4, 2021 PEDIATRICS Volume 146, number 2, August 2020:e20200251 SPECIAL ARTICLE the number of cases increased, and in because of high 2-dose immunization among children who experience 2019, .1250 cases of measles were rates of MMR (that results in high measles than among children who are reported, representing the highest rates of immunity in the community) not infected. This has been attributed number in 17 years.5 Approximately and the rapid implementation of to suppression of innate and adaptive 90% of reported cases occurred control measures from state and local immunity that is associated with among people who were health departments. However, these natural measles virus infection.12 unvaccinated (70%) or whose control measures are costly and draw Some immunologic abnormalities vaccination status was unknown resources away from other critical resolve soon after infection, but (20%).5 public health responsibilities.8 epidemiological studies demonstrate a strong association between measles In the United States, a single dose of In the absence of antiviral therapy, virus infection and increased a measles-containing vaccine treatment of measles consists of morbidity and mortality for months administered at 12 months of age has management of dehydration and to years after infection. In recent a vaccine effectiveness of ∼93% (and nutritional deficiencies (including reports, authors describe immune 97% when administered at vitamin A) and antimicrobial therapy abnormalities that appear to explain 15 months of age). Primary measles if secondary bacterial infections this increased risk of infection after vaccine failure (lack of occur. Approximately 30% of – recovery from measles.13 15 During seroconversion) occurs in ∼2% to 5% reported measles cases result in one an outbreak of measles in the of vaccine recipients who receive 1 of the following complications: Netherlands, unvaccinated children dose of the vaccine. Primary vaccine diarrhea, otitis media, pneumonia, were evaluated before measles failure may be caused by passive and less commonly, acute infection and again 2 months after antibodies in the vaccine recipient at encephalitis, degenerative neurologic recovery. Results revealed an the time of immunization (such as disease (subacute sclerosing impaired adaptive immune response, residual maternal antibodies), panencephalitis [SSPE]), or death.1 as evidenced by an 11% to 73% loss a damaged vaccine, or incorrect SSPE is an invariably fatal, persistent of antibody repertoire, after measles records (ie, administration of the viral infection of neuronal and glial infection. This appears to be incorrect vaccine). Secondary measles cells caused by a defective virus that secondary to measles virus vaccine failure (waning antibody occurs after a wild-type measles replication in and destruction of both concentrations to unprotective levels infection, particularly among children naïve and memory B cells, cells after an initial response) seldom who are infected in the first few years responsible for production of occurs. More than 98% of people who of life. Reports from the prevaccine circulating and secreted antibodies. receive $2 doses of a measles- era suggested rates of SSPE of 5 to 10 This loss of humoral immunity leaves containing vaccine, according to the cases per 1 million measles cases.1,9 children at an increased risk for recommended immunization This figure is considered now to be an infection from pathogens to which schedule, develop serological underestimation because an average they previously had been immune evidence of immunity.1 The second of 6 to 10 years occurs between the because of infection or vaccination. MMR dose is not a booster dose; measles infection and the onset of Recovery of lost immunity was rather, it is intended to induce symptoms of SSPE, making an restored after reexposure to immunity in the small number of association difficult to discern. In pathogens. Remarkably, despite this people who do not develop protective studies after the 1989–1991 measles immunosuppression, lifelong immunity after the first dose. outbreak in the United States and immunity to measles develops among Europe, authors report that the rate The number of measles cases survivors of acute measles infection. of SSPE is more common than occurring in the United States in Measles vaccination is not associated estimated previously, at least 1 case a given year is determined by 2 with the immunologic deficits of SSPE per 5000 measles cases, and factors: first, the number of travelers associated with wild-type measles is perhaps as common as 1 case per who become infected abroad and infection. 1000 measles cases among children travel to or return to this country infected in the first year of life.10,11 In while contagious; and second, the The consequences to a community countries where appropriate measles number of susceptible people who that does not maintain vaccine- immunization programs have been are exposed to the traveler.6,7 Clusters induced protective immunity (herd established, SSPE is nearly of disease are more likely to occur in immunity) to measles can be undetectable. communities with pockets of dramatic. In September 2019, several unvaccinated people. The majority of In reports from countries in Africa cases of suspected measles were importations have not resulted in and elsewhere, authors describe reported in the Samoan islands, and larger outbreaks in the United States higher morbidity and mortality rates by October 2019, a national measles

Downloaded from www.aappublications.org/news by guest on October 4, 2021 2 PERRONE and MEISSNER outbreak was declared. By January 7, MMR confer long-lived immunity others at increased risk of 2020, a total of 5655 cases were and meet the CDC definition of exposure do not have written reported in the Independent State of immune. Measurement of levels of documentation of immunization, Samoa, with an associated 83 deaths serum antibodies to measles is not history of infection, or antibody mostly in children ,5 years of age.16 indicated in a person who has evidence of immunity, 2 doses of More than 2.5% of the population of received 2 documented doses of MMR should be administered. 199 000 people in Samoa became MMR according to the People at increased risk who do infected. A decline in MMR recommended schedule. not have evidence of vaccination immunization rates among Samoan  Special circumstances include the or of a measles infection can children from 90% in 2013 to 34% in following: either be tested for immunity or 2018 created the opportunity for an can be administered 2 doses of ○ The first MMR dose may be outbreak once the measles virus was MMR 28 days apart without administered as early as introduced into the community. serological testing. There is no 6 months of age in a measles Because of the severity of the increased risk of harm from outbreak setting, before outbreak, a state of emergency was administering MMR to a person international travel, or as declared, schools were closed, who is already immune to any or postexposure prophylaxis. A a curfew was established, public all 3 of the viruses. dose administered before gatherings were prohibited, airline ○ 12 months of age should not be Health care personnel born in passengers were denied entrance, included as part of the routine 1957 or later should have unimmunized pregnant women were 2-dose series. A minimum of at serological evidence of restricted from attending their place least 28 days should lapse immunity or documentation of of employment, and measles between the first and second receipt of 2 doses of MMR. Birth vaccination became mandatory for dose and between the second before 1957 is generally priority groups. The Samoan and third dose (for children considered acceptable evidence Government noted the outbreak immunized before 12 months). of measles immunity. “[tears] at the very social fabric of Some evidence suggests that ○ Persons who received a measles society as every aspect of life is measles vaccination before vaccine in 1963–1967 affected.”16 12 months of age may be (presently 53–57 years of age) How can pediatricians and other associated with a limited and are unsure of the type of health care experts best counsel immune response after vaccine should receive 1 (if at families about measles vaccination to subsequent vaccine doses low risk) or 2 doses (if at high avoid the consequences of vaccine compared with measles risk) of MMR. The inactivated hesitancy, such as what occurred in vaccination at or after 12 (killed) measles vaccine used Samoa? Parents must understand months.18 This observation, as from 1963 to 1967 was not they have the power and the well as the low rates of measles effective. responsibility to protect their occurring in children between children from measles by ensuring the 12-month dose and the adherence to the following second dose at 4 to 6 years, MUMPS forms the basis for the current recommendations from the Centers Before initiation of the mumps for Disease Control and Prevention recommended schedule in the 19 vaccination program in this country (CDC) and the American Academy of United States. ∼ 1,17 in 1967, 186 000 cases of mumps Pediatrics : ○ Children and adolescents from were reported annually, but the actual  Routine administration of 2 doses kindergarten to 12th grade number was likely much higher of MMR (or measles, mumps, should have documentation of 2 because of underreporting. In rubella, and varicella) is doses of MMR. Adults 18 years addition, 15% to 27% of mumps recommended as the standard of of age and older should have cases were asymptomatic, but an care for measles prevention. The documentation of at least 1 dose unvaccinated, infected, asymptomatic first dose should be administered of MMR. person was contagious and able to at 12 to 15 months, and the ○ Students and staff in a college or transmit the virus to susceptible second dose should be other type of post–high school contacts. Parotitis is the most administered at 4 to 6 years of education should have common complication of mumps, age. The second dose can be documentation of 2 doses of followed by orchitis, oophoritis, administered as soon as 28 days MMR. If college students or mastitis, viral meningitis, after the first dose. Two doses of encephalitis, pancreatitis, and

Downloaded from www.aappublications.org/news by guest on October 4, 2021 PEDIATRICS Volume 146, number 2, August 2020 3 deafness. In the prevaccine era, control of mumps in the general RUBELLA mumps was the leading cause of viral population, and a formal Rubella is generally a mild viral encephalitis and sudden-onset recommendation for a third dose of 20 illness occurring among susceptible hearing loss in the United States. a mumps-containing vaccine was not children and young adults. Breakthrough mumps infection in issued. However, because of possible Complications of rubella include a fully vaccinated person is less likely waning vaccine immunity after 2 arthritis in up to 70% of infected to result in severe symptoms or doses of MMR, mumps protection adult women, encephalitis, complications compared with may be lost in a high-intensity thrombocytopenia, and orchitis.25 The infection in an incompletely exposure setting, such as during an public health importance of rubella is vaccinated or unvaccinated person. outbreak. Guidance was revised to due to the severe complications Whether a vaccinated person who state that a person previously associated with congenital rubella experiences asymptomatic vaccinated with 2 doses of MMR who syndrome (CRS), which occurs in up fi breakthrough infection can transmit is identi ed by public health to 85% of infants born to a woman virus to susceptible contacts is not authorities to be at increased risk fi 21 infected in the rst trimester of clear. Mumps infection during because of a continuing mumps pregnancy. The last major rubella pregnancy is no more severe than outbreak (such as a college campus or epidemic in the United States that in women who are not pregnant, among military personnel) should occurred during 1964–1965 and and no consistent complication in the receive a third dose of MMR. This resulted in an estimated 12.5 million fetus is recognized among pregnant recommendation was based on cases and 20 000 infants born with women who are infected during experience during previous mumps CRS. Relative to measles, rubella is gestation. Median mumps vaccine outbreaks when a third dose of MMR less contagious, but like measles, effectiveness is estimated to be 78% was administered (with institutional 20 rubella has only a single antigenic after 1 dose and 88% after 2 doses. review board approval) to the type.25 affected populations and subsequent In 2006 a multistate mumps outbreak attack rates were lower than those in resulted in .6500 cases mainly After introduction of the live individuals who had received 2 doses. involving students on several college attenuated rubella vaccine in 1969, A third dose appears to temporarily campuses in the Midwest.20 In reported cases of rubella and CRS boost immunity and assist in control 2009–2010, .3000 people were declined, but clusters continued to of an outbreak. However, a third dose infected in an outbreak among occur among unvaccinated older is unlikely to confer prolonged 3 a close-knit community in New York adolescents and young adults. When immunity. No available evidence City. The following year, an outbreak rubella immunization was directed at indicates additional benefit from .3 involved 500 people in the United adolescent girls or women of doses of a mumps-containing vaccine. States territory of Guam. Since 2015, childbearing age, the epidemiology an increase in the number of mumps remained largely unchanged; CRS still MMR contains the genotype A Jeryl occurred because of infection among outbreaks has continued to occur in Lynn mumps virus vaccine strain. the United States, primarily where unimmunized individuals, enabling Among the 12 recognized mumps the virus to continue to circulate, and people have close, prolonged contact virus genotypes, genotype G currently after introduction of mumps into the recommendations were changed to 20 is the most common genotype a routine immunization. During community. Outbreaks often involve 3 detected in the United States. Studies – populations with high rates of having 1989 1991, a global resurgence of reveal that antibodies induced by the rubella occurred, with spread to received 2 doses of MMR. The Jeryl Lynn vaccine strain neutralizes continued introduction of mumps unvaccinated adolescents and young genotype G strains, but the antigenic adults. After initiation of a routine 2- into this country is demonstrated by differences between genotype A and the 2019 report that mumps dose MMR schedule in the United genotype G strains may contribute to States in 1989, cases of rubella and outbreaks occurred among staff and the lower effectiveness of the Jeryl detained migrants in detention CRS fell to an all-time low. In 2004, 22 Lynn vaccine strain, particularly if endemic rubella was declared facilities in 7 states. 23 waning immunity occurs. eliminated from the United States.26 In 2018 the CDC issued guidance on Suggestions have been proposed for the use of a third dose of MMR among a change in the Jeryl Lynn strain to Estimates from the World Health persons at increased risk for a live attenuated genotype G strain or Organization suggest that .100 000 acquiring mumps because of an an inactivated genotype G strain that infants worldwide are born annually outbreak.3 The existing might provide a superior immune with CRS.27 Rubella virus continues to recommendation for 2 doses of MMR boost compared with a second dose circulate widely in Africa, the Middle 24 was determined to offer adequate of the Jeryl Lynn strain. East, and South and Southeast Asia.

Downloaded from www.aappublications.org/news by guest on October 4, 2021 4 PERRONE and MEISSNER Because .90% of children in the from this survey revealed that 20 administration of MMR according to United States have received $1 dose states had MMR coverage of ,90%. the immunization schedule cannot be of MMR, rubella elimination has been Measles virus transmission will not overstated. Reemergence of these sustained in this country despite the occur in communities where at least once-controlled diseases is not continued circulation of rubella in 95% of the population are a legacy that should be left to future other parts of the world. In recent appropriately immunized.2 Mumps generations. years, the few infants born in the virus infection is less likely to be United States with CRS generally associated with lifelong consequences were born to mothers who were compared with measles or rubella ABBREVIATIONS infected while pregnant before infections, but severe disease still CDC: Centers for Disease Control coming to this country. The entry of may occur in under-vaccinated and Prevention residents from rubella-endemic populations. The tragic complications CRS: congenital rubella syndrome countries emphasizes the risk of of CRS are avoided by ensuring that MMR: measles-mumps-rubella reemergence of CRS if vaccination women of childbearing age have vaccine rates decline. Between 2013 and received at least 1 dose of MMR. The SSPE: subacute sclerosing 2015, a median of 6 imported cases of spread of false concerns by panencephalitis rubella were reported annually, and antivaccine activists regarding a total of 3 cases of CRS were vaccine safety, particularly on social identified in the United States.28 media, has led to unfounded anxiety Sporadic cases of CRS occur in the regarding vaccine adverse events. In United States, and physicians should other countries, health care systems REFERENCES be alert to this possibility in the have collapsed because of political fl 1. Centers for Disease Control and appropriate epidemiological setting. unrest and armed con ict, resulting Prevention. Manual for the Surveillance To maintain elimination, high in inadequate immunization rates. of Vaccine-Preventable Diseases. immunization rates among children Wherever immunization rates are Chapter 7: Measles. 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Downloaded from www.aappublications.org/news by guest on October 4, 2021 The Importance of MMR Immunization in the United States Olivia Perrone and H. Cody Meissner Pediatrics 2020;146; DOI: 10.1542/peds.2020-0251 originally published online July 27, 2020;

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