The Diversity of Challenges in the Control of Measles Outbreaks

The Nature and Role of Vaccination Gaps

Public beliefs and attitudes about vaccinations, in general, and measles vaccination, in particular, have changed over time. While the high effectiveness of 2 doses of measles vaccine is widely accepted and the autism myth promulgated by Andrew Wakefield in 1998 ³ has been refuted and retracted, resistance to vaccination remains consistent and strong. Reasons for parents refusing vaccination of their children include the belief that vaccinations are not needed, fear that too many vaccinations are stressful to their child's immune system, religious beliefs, and concern about the discomfort their child may experience when given several vaccines simultaneously. ⁴ Much of the debate around vaccination and measurement of vaccination rates has focused on pediatric populations, because they are both the target of vaccination efforts as well as the object of parental concern about their health and welfare. In Los Angeles County, prior to the implementation of SB 277 in July 2016 (which eliminated religious and personal belief exemptions from vaccination requirements to attend school), school vaccination rates varied widely, largely due to high variance in parental use of the personal belief exemption.

Of note, in the California amusement park–associated outbreak, cases occurred both in children and young adults (LA County data). In Los Angeles County, 21.4% of cases occurred in children between the ages of 1 and 17. Similarly, 21.4% of cases occurred in individuals between the ages of 18 and 24. Because there are no population-wide recommendations to vaccinate adults, older adolescents and young adults who were previously exempted from school-based vaccination requirements will continue to play an important role in the propagation of future reintroduction-associated outbreaks in the United States. While unvaccinated individuals are frequently encouraged to seek vaccination during outbreaks, it is unlikely that such efforts have any effect on overall vaccination rates, and can be assumed to have minimal impact.

In the more recent outbreak in Los Angeles County, cases occurred primarily in older-age adolescents, most of whom were beyond California's mandatory vaccination requirements, which apply only to new school entrants or those entering the seventh grade. The first wave involved 7 individuals who were siblings (5) or close contacts (2) of the index case and 2 individuals for whom no connection with the index case could be identified. The second wave included 6 relatives of 2 first-wave cases, as well as 4 other contacts. The third and final wave included 4 siblings of 1 second-wave case. In this outbreak, amplification of disease transmission in families where many children were nonvaccinated was the primary driver of the extension of the outbreak.

During the amusement park–associated outbreak, the voice of pro-vaccine parents was strong and influential. This group also expressed strong support during the period of testimony leading up to the passage of SB 277. Awareness that gaps in vaccination could lead to the infection of vulnerable populations (eg, infants, those who have a medical reason for not receiving the vaccine, and those who have not responded to the vaccine) seemed to play an important role. This voice promoted efforts to increase vaccination rates both in school-aged children and in the general population.

In contrast, during the more recent outbreak that did not extend to any significant degree beyond the single social group, public debate about the value and importance of vaccination was only apparent near the end of the outbreak. Efforts to influence vaccination uptake were largely carried out by the local health department, with the assistance of influence leaders (eg, physicians, religious leaders) in the social group. In particular, one community leader and director of a medical organization serving this tight-knit social group played a significant role in appealing to members about the importance of vaccination, as well as how vaccination aligned with the community's values. Through letters and publications in the social group's media outlets, this leader called on parents to vaccinate their children and urged school administrators, physicians, and religious leaders to champion vaccination by establishing policies more stringent than state law and to prohibit unvaccinated children from attending school or being in other public places.

In addition to refusals of vaccination, information sharing was difficult. Members of the affected social group who had developed measles were reluctant to disclose information about their contacts during interviews with health department staff for fear of being stigmatized. One parent, for example, made a reference to “Typhoid Mary.” Some parents refused to open the door of their residence to speak with public health personnel; comments were made indicating there was no sense of urgency associated with the outbreak in the affected community. Similarly, 1 of 3 affected schools refused to provide a list of nonvaccinated students in a timely manner, thwarting efforts to offer preventive treatment and quarantine unvaccinated contacts. To some extent, trusted spokespersons from within the community played a role in convincing some members of the community to disclose information to the health department, but this was limited. ⁵

Common and Unique Challenges

A variety of challenges were common to both outbreaks. In each, the number of contacts exceeded 2,000. This taxed both the health department's ability to conduct contact interviews (to determine vaccination status) as well as its ability to analyze a large amount of information to identify and respond to any emerging difficulties. In both outbreaks, some exposures occurred in healthcare facilities, requiring the health department to provide guidance and technical assistance to other health professionals who were unfamiliar with public health practices. In addition, laboratory testing, while available, required substantial resources and necessarily took time. Finally, because Los Angeles County's borders blend seamlessly with other counties in the region, the inevitable spread of disease across these borders led to the need for close interjurisdictional coordination as well as assistance from the California Department of Public Health.

In the amusement park–associated outbreak, the nature of the initial exposure created an additional set of unique challenges. Because the first wave of cases was widely dispersed throughout the county, response efforts were similarly dispersed and focused on preventing further spread in multiple geographic locations. In addition, because a large proportion of cases were adults whose daily activities included extensive travel in densely populated sections of the county, the number of individuals exposed was both potentially large and difficult to determine.

In the outbreak that occurred in the closed social group, a different set of unique challenges was encountered. While not initially anticipated, it quickly became apparent that individuals were not only opposed to vaccination, but were also reluctant to cooperate with health department investigations. A number of individuals and 1 affected school refused to provide information on contacts or those who were non-immune, respectively, in a timely manner, thwarting efforts to provide preventive treatment and limit the spread of the outbreak.

Finally, while Los Angeles County's Department of Public Health is very experienced in the use of legal authority to address ongoing health threats (eg, legal orders for tuberculosis care or facility actions to limit disease spread), it had not had recent experience with large measles outbreaks and the unique challenges this disease presents. The use of the health officer's authority to enforce quarantine was considered in the first outbreak but was never used, as all exposed individuals voluntarily complied with requests to limit personal activities that could expose others.

So, the first outbreak provided no experience for the challenges that were encountered in the second outbreak. These included the absence of preexisting orders that could be quickly adapted to address the new challenges, lack of a process to quickly sort through hundreds of contact investigations to identify instances where legal authority could be applied, and a lack of preexisting decision support tools to facilitate rapid decision making as to when to use legal authority in the context of an outbreak that evolved quickly over a 3-week period. During the outbreak, the potential use of legal orders was discussed, but leaders were reluctant to use this approach because of concerns over ethical issues, lack of evidence that such orders could be effective, and uncertainty about how such orders could or should be enforced.

Strategies for Outbreak Control

The incident command system (ICS) was used to manage both outbreaks. Each of the authors served as the incident commander for one of these outbreaks (JDG: 2014-15 outbreak; FDP: 2016-17 outbreak). Los Angeles County's Department of Public Health has substantial experience in using the incident command system and has relied on this system to manage at least 10 incidents since the national response to H1N1 in 2009. While the incident command system requires considerable staffing and infrastructure support, its use has assured a consistent approach in managing all elements of these responses.

Response to both outbreaks relied on the well-established methods of case identification, contact investigation, and prophylaxis (when appropriate) and restriction of activities of susceptible individuals. Scores of susceptible individuals received prophylaxis with either vaccine or immune globulin. In the 2014-15 outbreak, 9 (1.3%) of 683 susceptible individuals received immunoglobulin, whereas for the 2016-17 outbreak, the corresponding figures were 26 (14.7%) of 177 individuals. The higher rate of administration during the latter outbreak was largely because of the efforts of a single pediatrician who responded promptly to requests made by parents. The assistance of healthcare facilities was particularly important in this effort, as nearly half of the contacts were healthcare facility–related. Total health department costs for the 2014-15 outbreak were estimated at more than $540,000; for the 2016-17 outbreak, the cost exceeded $336,000.

Despite the identification of thousands of contacts and hundreds of susceptible individuals, the quarantining of people who eventually developed measles was rare. There may have been some reduction in transmission during the more recent outbreak because of voluntary isolation in a tightly knit social group, but, collectively, these traditional disease control methods probably had limited impact on the spread of disease. Rather, in both outbreaks, the eventual cessation of disease spread was likely determined by the presence of herd immunity. Cases in the last wave of each outbreak certainly exposed a number of individuals, but all must have been immune, and they stood as a barrier against further spread of the outbreak. It is difficult, and probably nearly impossible, to significantly increase levels of herd immunity during an active measles outbreak. Public announcements about the outbreak and encouragements to receive vaccine probably had minimal impact on the first outbreak and no impact on the second.

In the more recent outbreak, substantial efforts were made to influence vaccine-related beliefs, attitudes, and behaviors in the affected social group. When initial efforts at the individual level appeared to be unsuccessful, a new strategy was adopted. Leaders of the affected social group were identified and engaged for education and support. The Los Angeles County Department of Public Health found these community leaders to be both receptive to and very supportive of disease control efforts. Several of these leaders made public statements, including posting information on the internet, in support of the department's work and strongly encouraging everyone to cooperate and get vaccinated. ⁶

We believe that, compared to traditional disease control methods, this latter type of work performed by community leaders will be the most important factor in limiting the impact of future reintroduction-related outbreaks. Development of relationships with leaders in communities where anti-vaccination beliefs and behaviors exist, both during and between outbreaks, is vital to enhancing the overall level of herd immunity in our communities. Direct efforts to meet with these leaders, both to provide accurate information about the benefits and effectiveness of vaccination as well as to highlight the importance of their voice in support of vaccinations, are critical to raising the level of health protection for the entire community. The potential impact of this approach may be high in light of the fact that reports of measles outbreaks in closed social groups continue to be frequent.^7-10

Conclusion

Los Angeles County has experienced 2 measles outbreaks since December 2014. These 2 outbreaks were distinctly different, both in the groups that were affected and the challenges that were encountered. The nature of the gap in vaccination that allowed the virus to be propagated in affected communities was different between the 2 outbreaks and, as a result, required different strategies to limit further spread. While traditional communicable disease control activities were employed in both response efforts, the primary determinant of outbreak cessation was likely the prevailing level of background immunity.

While laws such as California's SB 277 will eventually have a large and positive impact on overall population vaccination rates, the large number of older adolescents and young adults who are currently susceptible and beyond the reach of mandatory school-based vaccination programs will play a major role in measles outbreaks in the United States for many decades to come. Strategies to address and close this gap are needed if nationwide achievement of elimination is to be sustained. In addition, in communities where anti-vaccination beliefs and behaviors prevail, proactive engagement with leaders is necessary to improve response efforts and protect health. While outbreaks afford and usually demand such engagement, this opportunity exists during inter-epidemic periods and should be taken.