1. The Role of Non-Medical Exemptions in the Current Epidemiology of Measles in the U.S.
Preeta K. Kutty MD, MPH
Division of Viral Disease
National Center for Immunizations and Respiratory Diseases
43rd National Immunization Conference
March 30, 2009
Good afternoon. My talk on Non-Medical Exemptions in the
Current Epidemiology of Measles in the United States

2. Overview History of Immunization Laws Impact of Non-Medical Exemptions
Measles Epidemiology, 2008
Challenges
Future Directions
will be covered under the following topics
History of Immunization laws
Importance of Non-Medical Exemptions
Measles Epidemiology, 2008
Challenges and
Future Directions

3. History of U. S. Immunization Laws
1809- State of Massachusetts requires population to be vaccinated against smallpox
1905- Supreme court upholds rights of states to pass compulsory vaccination law (Jacobson v. Massachusetts, 197 U.S. 1 (1905))
1922 – Supreme Court upholds law requiring vaccination for school entry (Zucht v. King)
’s- school immunization laws used to enhance measles elimination efforts
The United States has a long history of immunization laws beginning in 1809 when the State of Massachusetts required the population to be vaccinated against small pox.
In 1905 the Supreme court upheld the rights of states to pass compulsory vaccination law (Jacobson v. Massachusetts, 197 U.S. 1 (1905))
In 1922 the Supreme Court upheld the law requiring vaccination for school entry (Zucht v. King)
And during the ’s the school immunization laws were used to enhance measles elimination efforts
Jackson CL. Public Health Report 1969; 84, (9):
Orenstein WA, Hinman AR. Vaccine 1999; 17: S19-24

4. U. S. School Immunization Laws
Are legal requirements that children have received vaccinations as a condition of participation in school
Are all state laws
Vary markedly by state
Are specific for grades and vaccines
Cover public and private schools
May not cover home-schooled children
U. S. School immunization laws are legal requirements that children have received vaccinations as a condition of participation in school. They are all state laws but vary markedly by state. The laws are specific for grades and vaccines and cover public and private schools. However, the school laws may not cover home-schooled children*
Orenstein WA, Hinman AR. Vaccine 1999; 17: S19-24
National Advisory Vaccine Advisory Committee, 1998:1-5

5. Effect of School Immunization Laws
Incentive for parents to vaccinate their children to protect the public health
System/safety net for immunization
Extremely effective in achieving very high immunization coverage in school populations
Reducing or eliminating vaccine preventable disease in these populations
School immunization laws are extremely effective in achieving very high immunization coverage in school populations. They are an incentive for parents to vaccinate their children to protect the public health. They act as a system or a safety net for immunization
And are extremely effective in achieving very high immunization coverage in school populations.
They also help in reducing or eliminating vaccine preventable disease in these populations.
Orenstein WA, Hinman AR. Vaccine 1999; 17: S19-24

6. Measles Epidemiology, U.S., 1962- 2008*
1963
Vaccine Licensed
1st Dose Recommendation
1989
2nd Dose
Recommendation
2000
Elimination
Declared
School Immunization
laws
Measles Cases
Following introduction of measles vaccine in 1963, reported measles cases declined rapidly.
During the 1970’s the predominant age group affected by measles were school-aged children and schools were the major site of transmission. It was the control of real disease which spurred school law efforts.
The schools laws also played a crucial role in the measles resurgence when a second dose of MMR vaccine was recommended in 1989.
By 2000, measles was declared eliminated from the U.S.
Elimination is defined as the absence of endemic disease transmission. Although elimination has been declared, it is possible to lose elimination status if we do not maintain our strongest wall of defense, which is sustaining high levels of vaccination coverage. Since the 1990s, national one dose coverage among month olds, depicted by the light blue line, has been up to 93% and two-dose coverage among adolescents, depicted by the green line, has been up to 89%.
Resurgence
Year
*Provisional data reported to NCIRD through 12/31/08

7. U. S. School Law Exemptions
1961: First philosophical exemption law was introduced in California as an exemption to polio vaccine
Early 1970’s: Universal implementation of state laws offering medical exemptions based on religion grounds§
Schools have access to all children, but not all children can be vaccinated
Exemptions allow school participation (which) is legally required for those unable to be vaccinated
Exemptions serve as an “escape valve” for school laws
In 1961, the first philosophical exemption was introduced in California as an exemption to polio vaccine
It was in the early 1970’s that Universal implementation of state laws offering medical exemptions based on religious grounds occurred.
Exemptions to these school entry laws exist because school participation is required by law in the US but not all children can be vaccinated to meet the requirements of these laws. Exemptions allow school participation (which) is legally required for those unable to be vaccinated. The Exemptions also serve as an “escape valve” for school laws.
§Evers DB. JONA’s Healthcare Law, Ethics, and regulation. 200;2 (2)

8. Types of Exemptions Medical Child on chemotherapy (temporary)
Child with immune deficiency (permanent)
Religious
Philosophical (Personal Belief)
Vaccination in-progress (temporary)
There are four types or categories of exemptions that are permitted for school entry. The first is medical exemptions which is used for children with medical contraindications to vaccination.
Exemptions are also allowed for persons who have deeply held religious beliefs in opposition to immunization.
Philosophical exemptions allow parents to decline immunizations for their children because they personally object to one or more vaccinations.
Vaccination in progress exemptions are granted on a temporary basis for children who may be in the process of receiving vaccines but who are not yet up to date because of the timing of vaccine schedules.

9. Types of Exemptions to Schools
Laws No. of States*
Medical
Religious §
Personal or
Philosophical
Currently, all 50 states allow for medical exemptions and 48 allow for religious exemption
Far fewer, 20, allow for personal or philosophical exemptions *
§Except Mississippi and West Virginia

10. Philosophical Exemptions Are Associated with More Exemptors
During , Salmon and colleagues conducted a study which demonstrated that states that allow philosophical exemptions to school entry laws have significantly higher rates of exemptions than states that do not.
In Massachusetts and Missouri, the states that did not permit philosophical exemptions, the overall state reported proportion of exemptiors was 0.4 to 0.6 % while in the states that allowed philosophical exemptions, ( in this case, Colorado and Washington) this proportion was considerably higher, exceeding 2%.
Salmon DA et al. Am J Public Health 2005; 95 (3):

11. Impact of Exemptions
Colorado, U.S.: Exemptors were 22 times more likely to have had measles than vaccinated children
Excess risk of measles among exemptors greatest among children ages 3-10 yrs (RR: 62.0; 95% CI: )
Incidence of measles among vaccinated children aged 3-10 yrs was significantly associated with the frequency of exemptors in the county
U.S.: From 1985 through 1992 exemptors in all States were 35 times more likely to contract measles than nonexempt children
Netherlands: 224 times (95% CI: ) more likely to acquire measles than vaccinated
In addition, various studies have shown that exemptors are at a higher risk of developing the disease than unvaccinated.
A population-based retrospective cohort study conducted by Feiken and colleagues in Colorado showed that exemptors were 22 times more likely to have had measles than vaccinated children and that the excess risk of measles among exemptors was greatest among children aged 3-10 yrs (RR; 62.0; 95% CI: ). Perhaps, more importantly, this study demonstrated that exemptors also increased their community’s risk of disease transmission. The annual incidence of measles among vaccinated children aged 3-10 yrs was significantly associated with the frequency of exemptors in the county where they lived.
Salmon et al found that from 1985 through 1992 exemptors in all States were 35 times more likely to contract measles than nonexempt children
And in Netherlands exemptors were 224 times (95% CI: ) more likely to acquire measles than vaccinated. Paradoxically, more cases of measles were reported from vaccine-accepting individuals living among unvaccinated clusters than from PBEs who lived among vaccinated individuals
Individuals at risk due to these exemptions are those who cannot be immunized for medical reasons, children too young to be immunized and few who do not respond to vaccines.
Feikin DR et al, JAMA 2000; 284: Salmon DA et al. JAMA. 1999; 282: 47-53
van Den Hof et al, J Inf Dis, 2002; 186:

12. Measles Epidemiology, U. S., 2008
140 cases from 19 states and DC
127 cases in U.S. residents
116 (91%) cases unvaccinated or unknown vaccination status
98 (85%) were vaccine eligible
67 (68%) were Personal Belief Exemptors (PBEs)
I shall now talk about the measles epidemiology in 2008 pertaining to the exemptors.
During 2008, 140 measles cases were reported from 19 states and DC.
Of the 127 measles cases in US residents, 116 or 91% of the cases were either unvaccinated or had unknown vaccination status.
Of the 116, 98 (85%) were vaccine eligible of which 67 or 68% were were Personal belief exemptors or PBEs
Note: Of the 98, 53 were school-aged children all of whom were PBEs.

13. Ratio of Indigenously Acquired to Imported Cases, U.S., 2001- 2008*
This slide summarizes the number of measles cases reported every year that are due to a direct importation ( usually either by a foreign traveler or a US resident returning from travel abroad) in a year, and cases where spread is indigenous (shown here in blue). , usually via secondary spread from one of these Importations The green line shows the ratio of indigenous to imported cases that are not imports
One of the major difference between the epi of measles in 2008 compared to what we saw from is that the ratio of indigenous to imported cases was higher in The green line shows how the ratio of indigenously acquired cases has increased up to 5.8 in 2008 compared to a ratio of 0.4 to 1.8 from 2001 to 2007, reflecting the higher spread of the virus within unvaccinated communities in 2008.
* Provisional data reported to NCIRD through 12/31/08

14. U.S. Residents with Measles, January-December 2008, by Age
Another important observation during 2008 was that measles cases occurred primarily in children and adolescents including 17 cases in children under the age of 12 months for whom vaccine is not yet recommended. These children count on the herd immunity that others provide to protect them from disease.
Of note, 80% of measles cases in 2008 were in persons who were under the age of 20, of whom 56% are covered by school immunization laws.
N = 127
80% cases < 20 years

15. Percent of Cases Aged 5-19 Years Claiming Personal Belief Exemptions (PBE), 2001- 2008*
This graph emphases the point that a higher proportion of cases aged 5-19 years (shown here in the purple line) claimed personal or religious belief exemptions during 2008: 93% in 2008 compared to 0-87% from
Of note, during 2005, there was a large outbreak of measles in Indiana that was focused in a community with religious and personal objections to vaccination, the largest measles so far this decade…
* Provisional data reported to NCIRD through 12/31/08

16. *PBE: Personal Belief Exemptors
Large Measles Outbreaks in Pockets of Unvaccinated School-aged Children
Indiana (2005): 34 cases
3 hospitalizations
28 school-aged children
Only 1 was vaccinated
20 home-schooled (none were vaccinated)
Public Health cost: $167,685
San Diego (2008): 12 cases
4 children were exposed in the pediatrician's office (3 were <12 months)
7 school-aged children
None were vaccinated (all were PBE*)
Public Health cost : ~ $177,000
Washington State (2008): 19 cases
16 school-aged children
11 home-schooled
None were vaccinated (all were PBE)
Public Health cost : $140,000
I will next highlight three outbreaks of measles in pockets of unvaccinated school children
In 2005, in Indiana an outbreak of 34 cases in which there were 3 hospitalizations. Of the 34 measles cases, 28 were school-aged children of which 20 were home-schooled, none of whom were vaccinated. The Public Health Costs incurred: $167,685
Early in 2008, an outbreak of 12 cases occurred in San Diego. This included 4 children were exposed in a pediatrician's office, 3 were <12 months.
Of the 12 cases, 7 were school-aged children; none had been previously vaccinated because their parents also had objections to vaccination. The public health cost incurred ~ $177,000
Washington State experienced an outbreak that resulted in 19 cases including 16 school-aged children (11/16 were being home-schooled); none of these children were vaccinated (all were PBE). Public health Cost incurred $140,000
*PBE: Personal Belief Exemptors

17. MMR Vaccine Coverage U.S. California Washington Indiana
Overall 1-dose MMR coverage in month olds
(July 2007-June 2008)*
92%
94%
90%
2-dose MMR coverage Kindergarten survey ( )£
95%
[San Diego: 91.5%]
91%
96%
% of children with religious or philosophical exemptions
1.6%
[San Diego: 2.5%]
5.9%
0.6% §
If we look at the vaccine coverage in these three states, as you can see from the first two rows, the vaccine coverage for MMR (dose 1 and 2) is approximately 90% and above. And statewide, between 0.6% and 5.9% of children attending kindergarten report having religious or philosophical beliefs against exemptions..
It is important to note here that states use a variety of different methods in their kindergarten surveys. For example, both WA and CA include home-schooled children in their surveys. In Indiana religious exemptions are legally acceptable while philosophical objections are not.
So Based on these data, we might not feel too concerned about the number of cases of measles that we have seen this past year.
In San Diego, over all PBE 2.5% but by school district the proportion ranged from 0% to 21% * £
§Courtesy of Indiana State Department of Health

18. Exemption Rates may Vary Considerably within a State
But this may be somewhat misleading.
For example on this Washington state map for classes Kindergarten to Grade 12, there is considerable variability in exemption rates among counties. Some are as high as 10% or more as those seen in brown.

19. Reasons Parents Choose Not to Immunize their Children: Indiana, 2005
Reasons for not receiving all recommended vaccines
N=6
Vaccines are not safe
67%
Vaccines are not necessary for health
Media
Personal/religious objections
50%
Prefer natural infection
Advice from an alternative health-care provider
Fear of getting the disease from the vaccine
33%
Personal experience
17%
Advice from a doctor or nurse
These outbreaks raised an important question: why do Parents choose not to immunize their children?
A survey conducted by Kennedy during the Indiana measles outbreak in 2005 among a religious group found that
67% thought that vaccines were not safe, were not necessary for health
50% had Personal/religious objections, Preferred natural infection and had taken the advice from an alternative health-care provider
33% had Fear of getting the disease from the vaccine
More studies are needed to understand these issues and prevent outbreaks described in the previous slides.
Kennedy AM, Gust DA. Pub Health Reports. 2008;123:

20. Summary
School immunization laws played a crucial role in measles and rubella elimination in the U.S.
Measles Epidemiology, 2008:
Largest number of cases reported in over a decade
Characterized by:
High proportion of cases among unvaccinated U.S. residents
High proportion of cases in school-aged children whose parents claimed exemptions
Many of these children were homeschooled
To summarize,
School immunization laws played a crucial role in measles and rubella elimination in the U.S.
During 2008, the largest number of measles cases was reported in over a decade. The epidemiology of measles was characterized by a higher proportion of cases among unvaccinated U.S. residents, a higher proportion of cases in school-aged children whose parents have claimed exemptions, many of whom were home-schooled.

21. Ongoing Challenges
The U.S. remains at risk for measles importations and thereby more measles outbreaks.
Maintain high 2-dose vaccination coverage rates
Possibility for large measles outbreaks exists
Monitor the impact of vaccine exemption, and understand reasons for vaccine exemptions
Effect of school immunization laws, measurement of exemptor rates, and identify communities at risk
Although the U.S. has maintained elimination, with large measles outbreaks occurring in highly-traveled developed countries and unvaccinated populations clustered geographically, the U.S. remains at risk of more measles outbreaks.
To maintain elimination, it will be necessary to maintain high two-dose vaccination coverage rates.
As seen in 2008, the opportunity for large measles outbreaks exist and hence it is necessary to monitor the impact of vaccine exemption on vaccine coverage, and understand trends and reasons for vaccine exemptions. We would also need to understand the effect of school immunization laws, to measure exemptor rates, and to identify communities at risk.

22. Future Directions Monitor trends in the U.S.
- Measles and other vaccine preventable diseases
- PBE
- Vaccine preventable diseases among PBE
Determine knowledge, attitudes and beliefs of exempt and non-exemptor population
Home schooled children may be an important population to study
We must continue to
Monitor trends in the US of Measles and other Vaccine Preventable Diseases,- Personal Belief Exemptors and Vaccine Preventable Diseases in Personal Belief Exemptors
Determine Knowledge, attitudes and beliefs of exempt and non-exemptor population
Home schooled children may be an important population to study

23. represent the view of the Centers for Disease Control and Prevention
Acknowledgements
State and Local Health partners
Division of Viral Diseases
- Kathleen Gallagher William Bellini
- Susan Redd Paul Rota
- Albert Barskey Jenny Rota
- Amy Parker Mark Papania
- Charles LeBaron Jane Seward
- Huong McLean Greg Armstrong
- Greg Wallace
I would like to acknowledge the following especially the state and local health partners who play an important role in maintaining the elimination of measles. I would also like to thank Dr. Gallagher who has graciously allowed me to use her slides.
Disclaimer
The findings and conclusions are those of the authors and do not necessarily
represent the view of the Centers for Disease Control and Prevention

24. 1967
Thank you

25. Additional Slides

26. MMR Vaccine Recommendations
Children:
Routine:
1st dose between months
2nd dose between 4- 6 years of age
Traveling abroad:
6-11 months – 1 dose
≥12 months – 2 doses ≥28 days apart
Adults: Absent proof of immunity
2 Doses: health care workers, international travelers, university students
1 dose: others
The current recommendations for MMR vaccine in the U.S. calls for children to receive their first dose of MMR between months of age and the second dose at school entry at 4-6 years of age.
Children 6-11 months of age traveling abroad should receive their first dose of MMR, and children ≥12 months should receive 2 doses at least 28 days apart, ideally before traveling. Adults who are absent proof of immunity should receive two doses if they are healthcare workers, international travelers, or university students. All other adults should have one dose. Of MMR vaccine.

27. Nonmedical Exemptions for States With Religious Exemptions and With Personal Belief Exemptions
Only Religious Exemptions Permitted
Personal Belief Exemptions Permitted
Exemption Rate
Exemption Rate
An analysis of data from for state-rates of non-medical exemptions at school entry verified these findings…states that permitted personal belief exemptions had higher overall exemption rates and this proportion increased over time. In states offering personal belief exemptions, exemption rates increased from 0.99% in 1991 o 2.54% in Exemption rates did not change significantly in states that allowed only religious exemptions.
Omer , Pan, Halsey et al., JAMA, 2006

28. Key Differences Between Parents of Exempt and Non-exempt Children
% exemptors
% non-exemptors
Odds Ratio
Too many immunizations
82%
20% 17
Weaken children’s immune system
80%
32% 9
Better to be immune by being sick
51%
11%
Healthy children do not need immunizations
26% 2% 14
Immunizations do more harm than good
34% 4% 13
Freedom of choice critical 9% 11
Parents should be allowed to send unvaccinated children to school
77%
24%
There are key differences between parents who claim exemptions for their children and those who don’t.
This slide shows results of a survey of 277 children with non-medical exemptions in Colorado, Massachusetts, Missouri and Washington and matched controls
Parents of exemptors were more likely to think that:
Too many immunizations
Weaken children’s immune system
Better to be immune by being sick
Healthy children do not need immunizations
Immunizations do more harm than good
Freedom of choice critical
Parents should be allowed to send unvaccinated children to school
From:   Salmon DA et al. Arch Pediatr Adolesc Med, 2005; 159(5):470–476

29. Measles Cases Reported to CDC, 2008 (N= 140)
Grant County, WA
Outbreak N=19
Missaukee County, MI Outbreak, N=4
Milwaukee County, WI Outbreak, N=6
New York City, NY
N=27
San Diego, CA
Outbreak N=12
(CA =11, HI =1)
This map shows the geographic location of these 140 cases. You can see that the cases are dispersed throughout the US. Yellow dots depict sporadic cases. The seven outbreaks that happened during 2008 are highlighted in pink. During 2008, there were sizeable measles outbreaks in in Washington State, San Diego, AZ, IL, and NYC.
Du Page Co, I L Outbreak N=31
Pima County, AZ Outbreak N=14

30. Reported Measles Cases, U.S. 1997-2008*, by Importation Status
This slide shows the number of reported measles cases each year that have been due to direct importation over the past decade. During 2008, 24( 17% of the total number of) cases were importations , 11 in US residents who traveled abroad and 13 in foreign visitors. This is the lowest percentage of directly imported measles cases since Over 70 % of these importations were associated with countries in the WHO EURO region
*Provisional data through December 31, 2008

31. Measles Importations, U.S. 2008
140 cases
24 importations D5 D4 D4 D4 D5
This map shows the routes of transmission for US imported measles cases during Its quite noticeable how many cases were imported from Europe where many countries are experiencing sizeable measles outbreaks. We had multiple importations in 2008 from Switzerland, Belgium, Italy and Israel. Genotypes D4, D5, and H1 have been isolated from cases this year.
Measles Importations, U.S. 2008

32. Personal Belief Exemptions in Kindergarteners, San Diego County, 2008 *
As part of our investigation into the measles outbreak in San Diego, the local EIS officer in conjunction with the County Health Department have looked more closely at personal exemptions for each school within the county. This map shows the different school districts, district specific exemptions rates ( the white to dark blue shading) and school-specific exemption rates show in the yellow circles. You can see that some school have exemption rates in excess of 20% and that furthermore, this level of exemption might be masked if we were to look at only district specific rates.
In my mind, these data, should al least give us pause about whether or not we should be worried about pockets of personal belief exemptions in the US
* Courtesy of D. Sugerman et al.

33. Europe: Incidence of Reported Measles Cases
by Age-group,
Muscat M et al. lancet 373: