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Epidemiology and transmission of measles

Authors Section Editors Deputy Editor

Jorge L Barinaga, MD, MS Martin S Hirsch, MD Elinor L Baron, MD, DTMH
Paul R Skolnik, MD Sheldon L Kaplan, MD

Last literature review version 17.3:September 2009 | This topic last updated: February 17, 2009 (More)

INTRODUCTION — Measles is a distinct clinical syndrome characterized by fever, malaise, conjunctivitis, coryza, cough, rash, and a pathognomonic enanthem (Koplik's spots). It is caused by the
measles virus, which is a member of the family Paramyxoviridae, genus Morbillivirus.

The epidemiology and transmission of measles and its complications will be reviewed here. The clinical manifestations, diagnosis, prevention, and treatment are discussed separately. See
( "Clinical
presentation and diagnosis of measles" and see "Prevention and treatment of measles").

INCIDENCE — Measles is highly contagious and occurs throughout the world [1] . In the prevaccine era ≥ 90 percent of children had acquired measles by age 15 [2] . The incidence of measles has
decreased substantially where measles vaccination has been instituted [3] .

In the absence of vaccination, measles was primarily a disease of school-aged children in the developed world and of younger children in the developing world4,5]
[ . With routine childhood vaccination at 12
to 15 months, there has been a shift in peak measles incidence during epidemics in the United States to six months of age. This is the time at which transplacentally acquired maternal antibodies are no
longer present if the mother has vaccine-induced immunity [6-8] . This has led to consideration and study of MMR vaccine administration schedules at earlier ages than currently recommended. (See
"Prevention and treatment of measles", section on Measles vaccination).

Measles is still a significant cause of morbidity and mortality as illustrated by the following findings:

Worldwide in 1995, there were approximately 44 million cases of measles and 1.1 million deaths attributable to measles9]
[ . The World Health Organization (WHO) estimated that 777,000 children
died as a result of measles in 2000. In March 2001, WHO and the United Nations Children Fund (UNICEF) announced a joint initiative to decrease by 50 percent the number of global measles deaths
by 2005 [10] .

An analysis of all causes of death for the year 1990 found measles to be the eighth most common cause of death in the world [ 11] , and in 2002 it caused an estimated five percent of all deaths in
children under five years of age [12] .
WHO estimates the total number of measles cases for 2002 by WHO region as: African Region (13,891,000 cases), European Region (936,000 cases), Western Pacific Region (5,370,000 cases),
Southeast Asia Region (9,182,000 cases), Eastern Mediterranean Region (3,636,000 cases), and Region of the Americas (8000) cases13]
[ . Underreporting of measles cases is likely [ 1,14] .
Epidemics of measles continue to occur at approximately six-year intervals in the Netherlands where a religious community numbering approximately 300,000 persons does not accept vaccination.
This group constitutes approximately half of all unvaccinated persons in the Netherlands. During an outbreak of 2961 cases from April, 1999 to February, 2000, 510 patients (17 percent) had one or
more complications, including three deaths and 68 hospitalizations, the majority for pneumonia 15]
[ . Infected patients had a median age of six years. Unvaccinated individuals were 224 times more
likely to become infected than vaccinated individuals, underscoring the effectiveness of measles vaccine in preventing transmission of measles [16] .
The Americas — Much progress has been made in measles control in the WHO Region of the Americas (this Region encompasses all nations in the Western Hemisphere). From 1987 to 1994, nearly every
country in the Region of the Americas attempted to vaccinate all children from nine months to fourteen years of age, regardless of prior history of measles vaccination or measles illness. Vaccination rates
with this approach, termed "catch-up" vaccination, were 94 percent. The only nonparticipants in this vaccination campaign were the United States, the French Antilles and the Netherlands Antilles17][ . Since
1994, a "follow-up" vaccination campaign, in which all children aged one to four years are vaccinated regardless of measles vaccination or disease history, has been underway in Latin American and
Caribbean nations [9] . Additionally, "keep-up" vaccination, in which children aged one-year are vaccinated, has also been pursued18]
[ .

The above-cited vaccination efforts have met with great success, as indicated by a fall in Region of the Americas measles cases from approximately 250,000 in 1990 to a provisional 105 cases in 2003 [18]
. If confirmed, this will be the smallest number of cases ever reported for the Region. All of the outbreaks in the Region, except for one in which the source was unknown, were due to imported measles,
emphasizing the importance of maintaining high population immunity18] [ .

In 1996, the Region of the Americas had a total of 2109 cases of measles [ 17] , a much lower incidence than in the epidemic year of 1990 when 218,000 cases were reported in Latin America and the
Caribbean [9] . However, an outbreak of almost 30,000 cases in 1997, approximately 95 percent of which were from Brazil, illustrated the need for continued vaccination of susceptible populations 19]
[ .
Following this outbreak in Brazil, a national follow-up vaccination campaign was conducted. Only 797 cases were reported in 1999, compared to 2781 cases in 1998. From January 1 through September 16,
2000, only 41 cases were reported, showing the importance of follow-up campaigns of this type [20] .

The final number of reported cases in 1997 was 42,000, mainly from Brazil [21] . The number of cases in 1998 and 1999 dropped substantially to 14,474 and 2828 cases, respectively, with continued
implementation of the measles eradication strategy. In 2001, the number of confirmed measles cases reached a record low of 537, a 99 percent decrease since 1990 [ 22] .

More recently, a measles outbreak occurred in Venezuela in 2002, with subsequent spread to Colombia, and in 2003 Mexico experienced an outbreak. These outbreaks are all thought to have been
secondary to imported measles [18] .

United States — In the prevaccination era there were as many as 500,000 reported cases of measles per year in the United States; by one estimate, there may have been as many as four million
cases per year [ 23] . Several years after the Food and Drug Administration approval of themeasles vaccine in 1963, the number of cases fell by approximately 99 percent.

Measles is no longer considered an endemic disease in the United States by the Centers for Disease Control and Prevention (CDC) 24-26
[ ] . The CDC analyzed data reported from local and state health
departments to estimate the incidence of measles in the United States from 2001 to 2003. A total of 216 cases were reported, resulting in an incidence of less than one case per million population, with 21
states reporting no cases. Approximately 80 percent were import-associated.

Although measles is a rare disease in the United States, isolated outbreaks continue to occur [27-36] . Most of these cases are related to imported measles with spread to unvaccinated susceptible persons
[28-30,37] .

In the first seven months of 2008, for example, there were more US cases of measles infections than during any comparable period since 1996 [ 37] . Of the 131 cases, at least 76 percent may have been
due to secondary transmission within the United States. Of the 123 cases among US residents, 91 percent were unvaccinated or had unknown vaccination status; 85 percent were considered eligible for
vaccination. Two-thirds of those eligible declined because of philosophical or religious beliefs.See
( "Autism and chronic disease: Little evidence for vaccines as a contributing factor", section on Lack of
evidence for association between autism and MMR).

Canada — In 1995, Canada reported 2362 cases of measles, which represented approximately 40 percent of cases reported in the Western Hemisphere for that year. There were 324 cases of measles
in 1996, and 570 cases in 1997. Some of the 1997 cases have been attributed to receipt of only one dose of measles vaccine , instead of the preferred two-dose series. There were 15 cases of confirmed
measles in Canada in 2003, and all were related to imported measles 1
[ 8] .

A goal for measles eradication in Canada by the year 2005 was set and guidelines for vaccination and outbreak control were issued; however, four cases of measles were documented in the greater Toronto
area in November 2005 [19,38] .

European Region — Substantial progress has been made toward better control of measles in the WHO-defined European Region; between 1990 and 2004, a decline in European measles incidence was
reported [39] . This has been attributed to improvements in routine measles vaccination, with the introduction of routine two-dose schedules throughout the region. Vaccination coverage is very high in
certain areas (eg, Scandinavian countries), but less so in others (eg, central and eastern Europe). Between 2006 and 2007, 12,132 cases were recorded. Most cases were incompletely vaccinated children,
although almost one fifth of cases occurred in individuals ≥ 20 years [40] .

South Pacific — Fiji, the most populous country in the South Pacific, introduced a two-dose schedule for measles-rubella vaccine in 2003. In February 2006, three infants were hospitalized with rash and
pneumonia and were subsequently diagnosed with measles infection 4 [ 1] . Over a four-month period, 132 suspected measles cases were reported including 22 that were laboratory confirmed; 31 patients
required hospitalization. The last reported case occurred eight weeks after initiation of an extensive immunization campaign. Low vaccination coverage rates, combined with probable importation, may have
led to this outbreak.

Global eradication — Measles outbreaks are a particular problem in the developing world. These outbreaks have been attributed to low vaccination rates. In July 1996, committees of the World Health
Organization (WHO), the CDC, and the Pan American Health Organization convened to discuss global measles eradication 9] [ . An eradication target-year in the range of 2005 to 2010 was recommended. It
was concluded that, while eradication should be feasible with the current vaccine, the strategy of giving only one dose of vaccine which is used in some parts of the world would be inadequate for this
purpose. It was also emphasized that the perception that measles is a minor illness is erroneous, and this mistaken perception may hinder attempts to eradicate measles.

In 2001 WHO and the United Nations Children's Fund (UNICEF), noting that annually approximately 30 million cases and 875,000 deaths occurred due to measles, published a plan which included among its
goals, a 50 percent reduction in measles mortality by the year 2005 when compared to 1999. The plan aimed "to achieve and maintain interruption of indigenous measles transmission in large geographical
areas with established elimination goals" 4[ 2] . Final data are pending [43] , but preliminary data suggest that the 50 percent mortality reduction goal may have been achieved. For example, a 2004
WHO/UNICEF press release reported a 30 percent global reduction in measles mortality from 1999-2002 44] [ and a year 2005 press release reported a 60 percent reduction in measles cases and deaths in
Africa, where roughly half of all deaths from measles occur [45] . In 2005, the World Health Assembly adopted the WHO/UNICEF Global Immunization Vision and Strategy, which includes a goal of a 90
percent reduction in global measles mortality by year 2010, compared to year 2000 mortality 46] [ .

The following examples show the difficulty of eradication strategies and highlight the need for ongoing efforts to follow the recommendations of the World Health Organization, the Centers for Disease Control
and Prevention, and others to eradicate measles transmission. In Zambia, measles remains one of the five major causes of morbidity and mortality among children aged five years or younger. From 1991
through 1999, the annual numbers of measles cases ranged from 1698 to 23,518. A campaign of supplemental vaccination was carried out among children nine months to four years old. Despite this
intervention, substantial measles transmission continued. A second campaign in four urban areas administeredmeasles vaccine to 197,077 children aged 6 to 59 months, resulting in vaccine coverage rates
of about 81 percent. The number of cases prior to the supplemental vaccination activities during a 12 month period was 2048; after the campaign there were still 496 cases that were counted. Possible
of about 81 percent. The number of cases prior to the supplemental vaccination activities during a 12 month period was 2048; after the campaign there were still 496 cases that were counted. Possible
reasons for a less than optimal outcome were the low vaccine coverage rate, the limited age groups that were vaccinated, and the limitation of vaccination to urban areas [47] .

Unexpected occurrences may also influence the incidence and transmission of measles. During a famine in Ethiopia in the year 2000, malnutrition and displacement from homes occurred with great
frequency. This led to a great increase in mortality rates, with wasting contributing to death in 72 percent of all deaths among children younger than five years. Measles, alone or in combination with
wasting, accounted for 35 (22 percent) of 159 deaths among children younger than 5 years, and for 12 (16.7 percent) of 72 deaths among children 5 to 14 years. It was recommended that mass
vaccination campaigns, extending to children 15 years of age, should be undertaken rapidly, and as a first priority, during emergency famine conditions 48][ .

Despite these figures, a report of a five-year program for mass vaccination and catch-up campaigns in children 14 years of age and younger in southern Africa resulted in an overall vaccination rate of 91
percent and an unparalleled decline in measles cases from 60000 in 1996 to 117 laboratory-confirmed cases in 2000 49]
[ . There were no deaths from measles in 2000 compared to 166 in 1996. These data
demonstrate that with vigilance and an organized program, measles cases can be controlled even in developing countries.

TRANSMISSION — Measles is highly contagious and subclinical illness is unusual. The attack rate in a susceptible individual exposed to measles is 75 percent 5[ 0] . In the decade before the measles
vaccination program began, each year nearly 4 million people in the United States were infected, 48,000 were hospitalized, 1,000 were chronically disabled and nearly 500 died.

The period of contagiousness is estimated to be from five days before to four days after the appearance of rash. Maximum contagiousness is thought to be during the late prodrome phase, when the
patient is febrile and has respiratory symptoms. In contrast, patients with subacute sclerosing panencephalitis cannot transmit measles [51] . (See "Clinical presentation and diagnosis of measles"
).

Infectious airborne droplets produced from the respiratory secretions of a patient with measles can remain in the air for several hours. Thus, person-to-person contact is not necessary to transmit
measles, which has been transmitted in physicians' offices and hospitals.

Large measles outbreaks can occur because of the high transmissibility of the virus in areas of crowding, like schools and densely populated communities. In 2003, an outbreak of greater than 857 measles
cases occurred in the Republic of the Marshall Islands (RMI), and known to have a very high population density 52]
[ . This dramatic number of cases occurred despite high rates of one-dose MMR vaccine
coverage of 80 to 93 percent [53] . The outbreak ended after vaccination of 35,000 persons among a population of 51,000. High rates of transmission were attributed to the large household sizes (median,
11 persons) and the number of persons per room (median, 5.5). In this study, infants below the age of routine vaccination had the highest morbidity and accounted for 34 percent of hospitalizations.

The peak incidence of measles in temperate areas is in the late winter and early spring. However, cases occur throughout the year and, in some nations, no seasonal incidence is apparent.

Although measles is known to have been transferred from monkeys to humans, nearly all clinical cases are acquired from contact with ill persons [54] . There are no known reservoirs of measles outside of
humans [55] .

EFFECT OF IMMUNITY — Natural measles infection is thought to confer life-long immunity. Preexisting immunity due to measles vaccination is also highly protective against clinical measles infection as
illustrated by the marked increase in risk among unvaccinated individuals during measles outbreaks. This was illustrated in an outbreak in the Netherlands in which unvaccinated individuals were 224 times
more likely to become infected than vaccinated persons [16] .

Groups at risk for measles in the United States include children too young to be vaccinated, persons who were never vaccinated, persons who declined vaccination for religious or philosophical reasons,
persons who have not received a second dose of measles vaccine , and persons in whom the vaccine failed to elicit a protective immune response. Travel outside the developed world or contact with ill
persons arriving from the developing world increases the risk of exposure to measles.

In developing countries, HIV infection in the mother and/or the child has been associated with a younger age of measles infection in the child. One possible explanation is a reduction in titer of the child's
transplacentally-acquired measles antibody. (See "Clinical presentation and diagnosis of measles"
, section on Children of HIV-infected mothers).

EPIDEMIOLOGY OF MEASLES COMPLICATIONS — The complication rates associated with measles infection vary according to the particular outbreak and the country in which the measles infection
occurs. In the 1990 United States outbreak, the following complication rates were seen [56] :

Overall complication rate — 22.7 percent

Hospitalization rate — 21.1 percent
Diarrhea — 9.4 percent
Otitis media — 6.6 percent
Pneumonia — 6.5 percent
Encephalitis — 0.1 percent
Death — 0.3 percent
Higher measles complication rates are believed to occur in developing countries [57,58] .

A hospital-based study in Afghanistan found an overall measles mortality of 10.8 percent, and a mortality of 23.4 percent in the most malnourished children. In that study, 85.4 percent of infected
children developed bronchopneumonia, and 30.2 percent developed enteritis.
A study in the former Zaire (now the Democratic Republic of the Congo) in children aged zero to four years concluded that measles infection led to weight loss; the weight was not regained for 2 to
4.5 months [59] .
A population-based study of xerophthalmia in the Pacific island nation of the Republic of Kiribati, which has one of the highest rates of xerophthalmia in the world, found an association between recent
measles infection and corneal xerophthalmia, with an odds ratio of 7.73 [60] . Measles may also contribute to childhood blindness in Africa [61] .

A prevaccine-era measles epidemic in Greenland was followed in detail by the Danish government 62] [ . Measles mortality varied with age, with mortality of 2.7 percent in children less than one year
old, 0.8 percent in those 15 to 34 years old, and 12.5 percent in persons older than 55; the overall mortality was 1.8 percent.

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