http://pediatrics.aappublications.org/cgi/content/full/101/3/383
Robert E. Weibel*, Vito Caserta*, David E. Benor, and Geoffrey Evans*
Acute Encephalopathy Followed by Permanent Brain Injury or Death Associated
With Further Attenuated Measles Vaccines: A Review of Claims Submitted to
the National Vaccine Injury Compensation Program PEDIATRICS Vol. 101 No. 3 March 1998, pp. 383-387



From the * Division of Vaccine Injury Compensation, National Vaccine Injury
Compensation Program, Health Resources and Services Administration, Public
Health Service, Rockville, Maryland; and the  Office of the General
Counsel, United States Department of Health and Human Services, Rockville,
Maryland.


        ABSTRACT
Top
Abstract
Introduction
Methods
Results
Discussion
References

Objective.  To determine if there is evidence for a causal relationship
between acute encephalopathy followed by permanent brain injury or death
associated with the administration of further attenuated measles vaccines
(Attenuvax or Lirugen, Hoechst Marion Roussel, Kansas City, MO), mumps
vaccine (Mumpsvax, Merck and Co, Inc, West Point, PA), or rubella vaccines
(Meruvax or Meruvax II, Merck and Co, Inc, West Point, PA), combined
measles and rubella vaccine (M-R-Vax or M-R-Vax II, Merck and Co, Inc, West
Point, PA), or combined measles, mumps, and rubella vaccine (M-M-R or M-M-R
II, Merck and Co, Inc, West Point, PA), the lead author reviewed claims
submitted to the National Vaccine Injury Compensation Program.

Methods.  The medical records of children who met the inclusion criteria of
receiving the first dose of these vaccines between 1970 and 1993 and who
developed such an encephalopathy with no determined cause within 15 days
were identified and analyzed.

Results.  A total of 48 children, ages 10 to 49 months, met the inclusion
criteria after receiving measles vaccine, alone or in combination. Eight
children died, and the remainder had mental regression and retardation,
chronic seizures, motor and sensory deficits, and movement disorders. The
onset of neurologic signs or symptoms occurred with a nonrandom,
statistically significant distribution of cases on days 8 and 9. No cases
were identified after the administration of monovalent mumps or rubella
vaccine.

Conclusions.  This clustering suggests that a causal relationship between
measles vaccine and encephalopathy may exist as a rare complication of
measles immunization.
Key words: measles vaccine, encephalopathy, encephalitis.

        INTRODUCTION
Top
Abstract
Introduction
Methods
Results
Discussion
References

Live attenuated measles vaccines used in the United States have almost
eliminated natural measles and its complications.1 The Edmonston B strain
of live attenuated measles virus vaccine induced fever >103F in
approximately one third and a measles-like rash in approximately one half
of vaccine recipients.2 This vaccine, first licensed for general use in the
United States on March 21, 1963, was simultaneously administered with 0.02
mL/kg of human immunoglobulin that greatly reduced the occurrence of fever
and rash. Further, or more attenuated, Edmonston-Enders measles vaccines
were developed to eliminate the use of immunoglobulin. The Schwarz strain
(Lirugen) was licensed on February 2, 1965, and used until 1976.
Edmonston-Enders strain (Attenuvax), licensed on November 26, 1968, was
combined with rubella vaccine (MR) or mumps and rubella (MMR) and licensed
on April 22, 1971. MMR soon became the preferred immunization, and by 1976,
Attenuvax became the only measles strain distributed in the United States.
On September 15, 1978, United States licensure of RA27/3 strain of MR
replaced the HPV-77 (duck embryo) strain licensed on June 9, 1969, and II
was added to the trade names.

Postinfectious encephalopathy complicates approximately 1 in 1000 cases of
natural measles and results in a mortality rate of 10% to 20% and permanent
central nervous system impairment in the majority of survivors.3-6
Encephalopathy, in this report, is defined as any significant acquired
abnormality of, injury to, or impairment of function of the brain, with or
without an inflammatory response (ie, encephalitis, encephalomyelitis). The
onset of encephalopathy usually occurs 2 to 7 days after the rash.
Pleocytosis is reported in approximately 20% of these patients. The cause
of this acute monophasic encephalopathy that occurs in the absence of a
detectable virus in the brain is obscure, but may be suggestive of an
autoimmune encephalopathy. This disease is distinct from progressive
subacute sclerosing panencephalitis or subacute inclusion-body encephalitis
in immunodeficient patients caused by a persistent measles virus infection.7,8

Case reports and reviews suggest that similar neurologic complications can,
less frequently, follow the administration of live attenuated measles
vaccine.9-11 In 1973, Landrigan and Witte11 reviewed 84 patients with the
onset of neurologic disorders within 30 days after a live measles
vaccination who were reported to the Centers for Disease Control and
Prevention from 1963 to 1971. Encephalopathy (used interchangeably with
encephalitis) of undetermined cause occurred 1 to 25 days after vaccination
in 59 patients, and of these, 45 patients had an onset 6 to 15 days after
vaccination. Long-term follow-up of 50 of the 59 patients revealed that 5
died, 19 had persistent encephalopathy, and 26 had recovered fully. In a
study of the incidence of encephalitis in Olmsted County, Minnesota, from
1950 to 1981 by Beghi et al,12 78% of the patients recovered completely.

In the National Childhood Encephalopathy Study of the United Kingdom from
July 1, 1976 to June 30, 1979, Alderslade et al13 reported convulsions or
acute encephalopathy, without separating the two conditions, in 17 children
7 to 14 days after receiving the Schwarz strain measles vaccine, and in 10
unvaccinated age-matched controls from the local community. This study,
designed to assess serious neurologic disorders associated with whole-cell
pertussis vaccine, reported the onset of encephalopathy <7 days after the
administration of whole-cell pertussis.

The purpose of this study of claims submitted to the National Vaccine
Injury Compensation Program is to determine whether or not there is
evidence for a causal relationship between the first dose of a currently
used attenuated measles vaccine, MR, MMR, mumps, or rubella vaccine and
encephalopathy of undetermined cause with permanent brain injury or death
that occurred within 15 days after administration.
        STATUTORY FRAMEWORK

The National Childhood Vaccine Injury Act of 1986 established the
compensation program, a federal no-fault system that became effective on
October 1, 1988, to provide compensation for individuals who were injured
or who died as a result of specified immunizations.14 Claims of
encephalopathy, seizure disorder, or death after the administration of
covered vaccines, including measles, mumps, or rubella, can be submitted to
the program and awarded compensation, if the condition meets certain
medical and legal qualifications. For an individual who received a measles,
mumps, or rubella vaccine, the act grants, in the Vaccine Injury Table, the
presumption of vaccine causation if the first manifestation of
encephalopathy occurs, in the absence of an alternate cause, 15 days or
less after receiving any of these vaccines. The injury or its residual
effects, except when death occurs, must persist for >6 months. The standard
of proof is a preponderance of the medical evidence (ie, >50%, or more
likely than not). In addition, a vaccine cause may be demonstrated in the
absence of a Vaccine Table Injury, but legally, this is a more difficult
process for the person seeking compensation. Effective March 10, 1995, the
program changed the time period of a Vaccine Table Injury for these
vaccines and the onset of encephalopathy from <15 days to 5 to 15 days.15

In 1994, an Institute of Medicine Committee published a scientific review
of clinical studies and case series and reports of encephalopathy after the
administration of measles, MR, MMR, and mumps vaccine.9 Their review
identified no conclusive evidence of the occurrence of encephalopathy or
encephalitis after the administration of measles or mumps vaccine.
Nevertheless, the Institute of Medicine Committee acknowledged biologic
plausibility that measles vaccine might cause encephalopathy. The lack of
controlled studies that distinguish background rates of encephalopathy of
undetermined cause in unvaccinated populations makes a determination of
causation difficult.
        METHODS
Top
Abstract
Introduction
Methods
Results
Discussion
References

The medical records and affidavits in each petition are reviewed by
physicians in the compensation program to determine, if possible, the cause
of the injury and to classify the findings. The program's finding as to the
onset of neurologic signs or symptoms is based only on the medical records.
The diagnosis in each case is based on the preponderance of the medical
evidence and the assessments of the treating physicians. When deemed
necessary, a medical expert is obtained to review the case and provide an
expert opinion. All of the cases of encephalopathy discussed in this
article have been reviewed in a consistent manner by the first author.

Children with appropriate development who acquired an acute encephalopathy
of undetermined cause within 15 days after the administration of the first
dose of measles, MR, MMR, mumps, or rubella vaccine between April 1970 and
March 1993 followed by chronic encephalopathy or death were selected for
further analysis. The neurologic criteria used for the diagnosis of acute
encephalopathy of undetermined cause were an abrupt onset of neurologic
symptoms and/or signs with significant brain impairment including behavior
changes with a depressed level of consciousness, ataxia, or seizures.
Children selected for this study had an acute encephalopathic illness
followed by chronic encephalopathy including mental retardation, seizure
disorders, movement disorders, or motor or sensory disorders.

Cases of encephalopathy were excluded if an infectious, toxic, traumatic,
or metabolic cause or a recent exposure to natural measles, mumps, or
rubella was identified or full recovery occurred within 6 months. Seizures
with mental dysfunction attributed to the postictal state or medication
were not considered to be encephalopathy.

All children at the time of the vaccination were considered by the authors
to be susceptible to the vaccines administered and >95% would be expected
to develop an immune response to the vaccines. The evaluation of these
children reflects the standards and technical advancements for diagnoses at
the time of the injury. In a few instances, attempts to isolate virus from
cerebral tissue and cerebrospinal fluid were unsuccessful. Viral isolation
and antibody studies for arboviruses, enteroviruses, and herpesvirus were
negative on all children evaluated.

Identified patients were categorized with the variables of sex, vaccine or
vaccines administered, age at vaccination, postvaccination day of onset,
neurologic symptom at onset, level of consciousness or behavior changes
during the day of onset, fever, measles-like rash, cerebrospinal fluid
analysis, developmental regression during or after the acute illness,
hospitalization, antibody studies, and manifestations of permanent brain
injury or death.
        RESULTS
Top
Abstract
Introduction
Methods
Results
Discussion
References

A total of 403 claims of encephalopathy and/or seizure disorder after
measles, MR, MMR, mumps, or rubella vaccination were identified during this
23-year period. Of these claims, 48 (25 males and 23 females) met the
inclusion criteria and acquired an acute encephalopathy of undetermined
cause 2 to 15 days after receiving measles vaccine, MR, or MMR. This acute
encephalopathy was followed by permanent brain impairment or death. The
patients ranged in age from 10 months to 49 months, with a median age of 15
months and a mean age of 17.5 months. No case of encephalopathy of
undetermined cause within 15 days after the administration of monovalent
mumps or rubella vaccine was identified.

Either Attenuvax or Lirugen was administered to 4 children between 1970 and
1974, and Attenuvax was administered to 4 children between 1977 and 1982.
One child received MR, and 30 children received MMR. Of the remaining 9
children, 2 received MMR and diphtheria, tetanus, pertussis vaccine (DTP),
2 received MMR and Haemophilus influenzae type b vaccine (Hib), 4 received
MMR, DTP, and oral poliovirus vaccine (OPV), and 1 received MMR, DTP, OPV,
and Hib.

The onset of these 48 cases of encephalopathy (Fig 1) occurred 2 to 15 days
after the administration of a measles-containing vaccine. All patients were
apparently well during the first 48 hours after the vaccination
(postimmunization days 0 and 1). The clustering and peak onset of
encephalopathy occurred in 17 patients on days 8 and 9. Of the 12 cases of
encephalopathy that occurred within 7 days after vaccination, 10 received
only MMR; 1 with an onset on day 4 received MMR and Hib; and 1 with an
onset on day 5 received MMR and DTP.


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      Fig. 1.   Onset of encephalopathy by day after the administration of
the first dose of MMR, MR, or further attenuated measles vaccine in 48
children (1970-1993).

The clinical features of acute and chronic encephalopathy or death in these
48 patients (Table 1) were classified into three groups based on the
initial finding of ataxia in 6, behavior changes in 8, and seizures in 34.
The onset of neurologic findings varied in severity from ataxia or behavior
changes to prolonged seizures or coma. Fever preceded the onset of acute
encephalopathy by several hours to several days in 43 of 48 children. A
measles-like rash with a postvaccination onset from day 6 to 15 occurred in
13 children.

                             
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TABLE 1
Clinical Findings of Acute Encephalopathy Among 48 Patients 2-15 Days After
the First Dose of a Further Attentuated Measles Vaccine, MR, or MMR,
1970-1993, and Sequelae

All children with acute ataxia had significant behavior changes, and 3 of
the 6 were hospitalized. Neurologic sequelae in the ataxia group included
mental retardation in 3, seizure disorder in 1, chronic ataxia in 4, and
sensorineural hearing loss in 1.

A case example of this group is a normal 16-month-old female who received
MMR, and 9 days later, she had a fever, a measles-like rash, and ataxia.
Neurologic examinations revealed unsteadiness and truncal titubation,
nystagmus, dysmetria, developmental regression, and pleocytosis with 41
monocytes, and a normal brain scan with magnetic resonance imaging. She was
diagnosed as having brainstem encephalitis. At age 10 years, she had global
developmental delay and cerebellar dysfunction.

The 8 children with initial behavior changes rapidly progressed to coma.
Two died during the acute illness with autopsy findings of massive cerebral
edema and herniation. Of the 6 survivors, 6 had mental retardation, 5
spastic paresis, 1 seizure disorder, 1 choreoathetosis, and 1 died 6 years
after the acute illness.

A case example of this group is a normal 29-month-old male who received MMR
and Hib, and 14 days later, he developed fever, emesis, and progressive
lethargy. The following day, he was hospitalized in coma with pleocytosis
(246 monocytes, 54 lymphocytes), an elevated cerebrospinal fluid (CSF)
protein (49), negative CSF bacterial and viral cultures, and an
electroencephalogram (EEG) with diffuse cerebral slowing. He became rigid
and opisthotonic. Magnetic resonance imaging of the brain revealed
leukodystrophy. At age 5 years, he had hyperactivity and aggressive behavior.

In the 34 children with an onset of generalized or focal seizures, coma and
behavior changes could not be attributed to a postictal state or
medication. These seizures, associated with fever in 32 and a measles-like
rash in 9, rapidly progressed to coma in 29 and depressed or changed
consciousness in 5. Two apparently normal healthy children received MMR
vaccine and died 2 and 12 days later. Autopsy findings revealed cerebral
edema and uncal gyral herniation in one, and viral encephalitis with
hemorrhagic infarctions of the thalamus and pons in the other. All
survivors had chronic encephalopathy with mental retardation in 31, seizure
disorder in 23, and spastic paresis in 10. Three deaths occurred 3 months
to 4 years later.

A case example of this group is a normal 16-month-old female who received
measles vaccine, and 7 days later, she developed a fever and a measles-like
rash. Ten days after the vaccination, she was hospitalized with status
epilepticus, a temperature of 106F, and a normal CSF analysis. The
following day, she had intermittent seizures on anticonvulsant therapy,
coma, and left hemiparesis. An EEG showed totally disorganized activity,
epileptiform discharges, and right hemisphere suppression. At age 10 years,
she had spastic left hemiparesis and cognitive difficulties.

CSF analyses performed on 40 of the 48 children were abnormal in 16.
Pleocytosis, mainly mononuclear cells, ranged from 7 to 246 cells in 11
patients, with an elevated protein of 49 mg to 101 mg in 4 of these 11.
Four patients had only an elevated CSF protein of 117 to 172 mg/dL and 1
had an elevated CSF pressure of 320 mm H2O without further CSF analyses
recorded.

The 48 patients (Table 2) are divided into three time periods based on an
onset day of 1 to 5, 6 to 10, and 11 to 15. The onset of ataxia, behavior
changes, seizures, and CSF pleocytosis occurred in each time period, with
approximately one half of the cases in the 6 to 10 day time period. The
acute illness was associated with fever in all but 5 patients; 3 of the
afebrile children were in the 1 to 5 day time period.

                             
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TABLE 2
Clinical Findings in 48 Patients Through Postvaccination Day 15 by Type of
Neurologic Onset in 5-Day Period Groups

The distribution of encephalopathy by month of onset (Fig 2) is random
throughout the year with a variation of 10 to 13 cases by season. By year
of onset, the number of cases ranged from 0 to 4 each year with a total of
15 in the 1970s, 1 to 5 with a total of 21 in the 1980s, and 1 to 6 with a
total of 12 in the 1990s with a peak in 1989 and 1990 and no trend in the
pattern throughout the years. The medical evaluations reflected the
standards of each time period. Prevaccination clinical records revealed no
evidence of hypersensitivity.


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      Fig. 2.   Onset of encephalopathy by month after the administration
of the first dose of MMR, MR, or further attenuated measles vaccine in 48
children (1970-1993).

Statistical Analysis

A statistical analysis was performed on the distribution of the 48 cases
that met the inclusion criteria. A random distribution would show the onset
of 3.0 cases/day (48  16). The denominator of 16 is used because the
inclusion criterion within 15 days includes 16 periods of 24 hours when the
day of immunization is counted as day 0. A comparison of the observed
number to the expected number per day was performed based on the use of a
standardized morbidity ratio. The distribution was nonrandom with
clustering and 2 statistically significant increases (0.01 < P < .05) of 9
and 8 cases on postvaccination days 8 and 9, respectively.16 Our analysis
found no significant difference between the onset of encephalopathy and age
or sex. In the absence of any obvious bias and confounding, this finding is
evidence for a causal relationship between further attenuated measles
vaccine, alone or in combination, and acute encephalopathy of undetermined
cause followed by permanent brain impairment or death.
        DISCUSSION
Top
Abstract
Introduction
Methods
Results
Discussion
References

Manifestations of acute encephalopathy including loss of consciousness,
ataxia, seizures, and pleocytosis among these 48 children is similar to the
clinical features of acute encephalopathy described after natural measles
and other live measles vaccines.1,2,4,8,10 The earlier onset of these cases
of encephalopathy after the injection of live attenuated measles vaccine as
compared with the onset after natural respiratory exposure to wild-type
measles virus may be related to the route of entry, as is the earlier onset
of measles-like symptoms and immune responses.17 Whether the onset of
encephalopathy within 5 days after a measles vaccination can be caused by
vaccine virus replication and immune responses is not clear.

Encephalopathy after natural measles is known to occur in young children,
and in some, there is full recovery. Among children in England and Wales,
Miller et al6 reported 389 cases of encephalitis after natural measles with
11% of these cases at age 1 to 2 years and 13% at 3 to 4 years. It is
biologically plausible that encephalopathy with variable outcomes could
occur after measles vaccine administered to children of the same age.

A comparison of these cases to claims seeking compensation could be biased,
but there is no evidence for bias in the recording of the onset of acute
encephalopathy in the medical records or the selection of cases analyzed.
Study of this issue is hampered by a lack of background encephalopathic
rates in unvaccinated children. A review of similar cases reported to other
systems could be helpful.

Claims with an onset of acute encephalopathy of undetermined cause within
15 days after a measles, MR, MMR, mumps, or rubella vaccination between
1970 and 1993 followed by permanent brain injury or death have an equal
likelihood of being recommended for compensation by the program physicians
regardless of whether the injury began on day 0 or day 15. If the null
hypothesis is true and the measles, mumps, or rubella vaccine has no causal
relationship to the acute encephalopathy, the number of cases with an onset
of neurologic findings of encephalopathy each day during this period would
be expected to have a random distribution with essentially equal numbers of
cases on each day. Our results of a statistically significant cluster on
days 8 and 9 after measles immunization indicates this may be an effect of
measles vaccine, MR, and MMR.

From 1970 to 1993 in the United States, approximately 75 000 000 children
received measles vaccine by age 4 years based on 83 000 000 births and an
immunization rate of 90%. The 48 cases of encephalopathy probably represent
underreporting to this passive system, which does not require individuals
to file for compensation and requires medical documentation. However, given
the generous compensation offered in this program, it is reasonable to
conclude that most serious cases temporally related to a vaccination have
been captured. In the absence of a specific test to determine vaccine
causation, these 48 cases may include some nonvaccine cases representing
background rates. Nevertheless, with a denominator of 75 000 000 vaccinees
throughout 23 years, the incidence of acute encephalopathy caused by
measles vaccine in this cohort can reasonably be described as very low.
        FOOTNOTES

Received for publication Jul 30, 1997; accepted Sep 23, 1997.

Reprint requests to (R.E.W.) National Vaccine Injury Compensation Program,
Health Resources and Services Administration, Parklawn Building, Room
8A-46, 5600 Fishers Lane, Rockville, MD 20857.
        ACKNOWLEDGMENTS

We thank the program staff and the Centers for Disease Control and
Prevention, National Immunization Program, especially Mary Morrison, BS,
and Robert Chen, MD.
        ABBREVIATIONS

MR, measles-rubella vaccine. MMR, measles-mumps-rubella vaccine. DTP,
diphtheria, tetanus, pertussis vaccine. Hib, Haemophilus influenzae type b
vaccine. OPV, oral poliovirus vaccine. CSF, cerebrospinal fluid.
        REFERENCES
Top
Abstract
Introduction
Methods
Results
Discussion
References

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  14. National Childhood Vaccine Injury Act of 1986, codified as 2111, et
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Injury Table. Federal Register. February 8, 1995;60:7678-7695
  16. Bailar JC, Edemer, F Significance factors for the ratio of a Poisson
variable to its expectation. Biometrics 1964; 20:639-643
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Pediatrics (ISSN 0031 4005). Copyright 1998 by the American Academy of
Pediatrics


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