Containment Cuts Measles Spread in Undervaccinated Population

Targeted containment efforts implemented by local authorities, combined with high baseline immunity in the general population, limited the spread of measles in an undervaccinated Amish community during a 2014 outbreak, researchers report in an article published in the October 7 issue of the New England Journal of Medicine.

"Vaccination of susceptible persons is the backbone of measles outbreak control, and the data suggest that the control measures that were instituted may have been effective in curtailing some measles transmission," write Paul A. Gastañaduy, MD, MPH, from the Centers for Disease Control and Prevention, Atlanta, Georgia, and colleagues. "A decline in infections coincided with the scaling up of vaccine administration, and vaccination efforts effectively removed close to a third of the susceptible pool (8726 of approximately 28,100 previously unvaccinated Amish persons received the [measles-mumps-rubella (MMR)] vaccine)."

In the United States, widespread use of the MMR vaccine, and implementation of aggressive measures for outbreak control, have led to significant reductions in the number of measles cases compared with in the prevaccine era.

Although the United States achieved measles elimination in 2000, imported cases can lead to outbreaks. In particular, such outbreaks occur in areas where unvaccinated people cluster, including in religious communities.

Although Amish religious doctrine does not prohibit vaccination, cultural health-related beliefs and practices serve as a barrier to preventive healthcare, resulting in low vaccination rates and an increased risk for vaccine-preventable diseases in Amish communities.

In March 2014, a measles outbreak in Ohio was linked to two unvaccinated Amish men who had returned to their US communities after a missionary trip to the Philippines. The two men were unaware that they had been infected with measles virus during their trip. According to the World Health Organization, in 2014, the Philippines experienced 21,403 confirmed cases of measles and 110 measles-associated deaths.

Dr Gastañaduy and colleagues describe the epidemiologic features of this measles outbreak, which affected one of the largest Amish settlements in the United States, and discuss how public health responses limited the spread of the disease.

The two source patients were 22 and 23 years of age and had returned from the Philippines to their homes in Knox County, Ohio, on March 21, 2014. Both developed fever and cough, coryza, or conjunctivitis on March 22, followed by a generalized red maculopapular rash on March 24. Diagnostic testing identified thrombocytopenia in both men, who then received a diagnosis of dengue.

The third and fourth case patients also traveled from the Philippines with the two source patients and developed rash on April 6 and April 8, respectively. Patient 3 also had thrombocytopenia and received a diagnosis of dengue.

After 12 more Amish people developed a febrile illness with rash, measles was recognized and was reported to the Knox County health department on April 21. Diagnostic testing confirmed measles in seven of the initial case patients, including in three of the four patients who had returned from the Philippines.

From March 24, 2014, through July 23, 2014, nine counties in Ohio reported a total of 383 outbreak-related cases of measles in patients of median age 15 years (range, <1 year - 53 years). Of the 383 case patients, 380 (99%) were Amish, 178 (46%) were female, and 340 (89%) were unvaccinated.

The age distribution of the case patients changed during the course of the outbreak. Before May 14, 2014, the approximate midpoint of the outbreak, 26% of the measles cases occurred among children and adolescents (aged 5 - 17 years), and 48% occurred among young adults (aged 18 - 39 years); however, these rates changed on or after May 14 to 52% and 25%, respectively (P < .001).

The reported source of exposure also changed, initially involving church in 38% of cases and home in 48%; later, these rates changed to 5% and 90%, respectively (P = .10).

Sixty-nine (18%) of the 383 case patients underwent diagnostic testing, and 57 (15%) received a diagnosis of measles. The virus strain was characterized as genotype D9, which was circulating in the Philippines during the reporting period.

The authors highlight that this was the largest measles outbreak in the United States in more than 2 decades. At 12 cases per 1000 Amish persons, its crude attack rate was several orders of magnitude larger than the annual incidence of measles (<1 case per million persons) in the country. The 4-month duration of the outbreak was also longer than any other measles outbreak since the disease was eliminated in the United States.

Compared with more than 88% of the general (non-Amish) Ohio community, an estimated 14% of affected Amish households had MMR coverage with at least a single dose of the vaccine.

Containment efforts followed Centers for Disease Control and Prevention guidelines. As part of the public health response, 10,644 persons received the MMR vaccine, including 106 (28%) case patients, 16 (15%) of whom received it before assumed measles exposure. Case patients were also isolated until 4 days after the onset of rash, when they were no longer infectious. Nonimmune individuals who were exposed to measles underwent voluntary quarantine at home and were monitored for symptoms until the end of the 21-day incubation period of the virus. The organization responsible for the missionary work in the Philippines also adopted pretravel immunization measures for subsequent volunteers.

"The magnitude and duration of the outbreak illustrate how communities that object to vaccination are at increased risk for the spread of measles and for potentially becoming a source of further transmission," the authors write.

Interestingly, however, the affected Amish community was less opposed to immunization during the 2014 outbreak compared with other Amish communities that had refused vaccination during previous outbreaks.

Infected and susceptible community members were also willing to avoid church gatherings and other such events. This may also help to explain the shift in age groups and transmission settings involved over the course of the outbreak.

The authors stress how this outbreak "illustrates the way in which a clustering of persons who do not routinely vaccinate against measles can result in an accumulation of susceptible persons and can subsequently create a niche of sustained measles transmission."

Although they highlight the importance of early recognition of measles and how prompt initiation of control measures may be key to limiting its spread, they emphasize that the single best means of containment of the disease "is maintenance of high initial levels of measles immunity in the population."

In an accompanying editorial, David D. Durrheim, MBChB, DrPH, from the Western Pacific Measles Regional Verification Commission, Wallsend, New South Wales, Australia, discusses how this study emphasizes the value of measles outbreaks in identifying and characterizing immunity gaps that require action.

"The outbreak in the Amish community highlights the challenge posed by unimmunized or partially immunized young adult travelers who visit areas in which measles is still endemic and subsequently return home with the virus," he writes.

However, he stresses the difficulty in reaching such communities, who do not seek pretravel advice and immunization. More creative ways of linking immunization with visa issuance should therefore be investigated. "Every immunity gap should be filled," he says.

Because the measles virus has the ability to expose immunity gaps, Dr Durrheim notes the importance of capitalizing on this and allowing measles outbreaks to serve as a guide in progressing toward the ultimate goal of measles eradication.

"Every death from measles is a tragedy that should have been prevented," he concludes.

This study was supported by the Centers for Disease Control and Prevention. The authors and editorialist have disclosed no relevant financial relationships.

New Engl J Med. Published online October 6, 2016.

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