Epidemiology of measles

Measles is extremely infectious and its continued circulation in a community depends on the generation of susceptible hosts by birth of children. In communities which generate insufficient new hosts the disease will die out. This concept was first recognized in measles by Bartlett in 1957, who referred to the minimum number supporting measles as the critical community size (CCS).^[1] Analysis of outbreaks in island communities suggested that the CCS for measles is c. 250,000.^[2]

In 2011, the WHO estimated that there were about 158,000 deaths caused by measles. This is down from 630,000 deaths in 1990.^[3] In developed countries, death occurs in 1 to 2 cases out of every 1,000 (0.1% - 0.2%).^[4] In populations with high levels of malnutrition and a lack of adequate healthcare, mortality can be as high as 10%. In cases with complications, the rate may rise to 20–30%.^[5] Increased immunization has led to an estimated 78% drop in measles deaths among UN member states.^[6][7] This reduction made up 25% of the decline in mortality in children under five during this period.

Reported cases^{[8][9][10][11][12][13]}

WHO-Region	1980	1990	2000	2005	2014
African Region	1,240,993	481,204	520,102	316,224	71,574
Region of the Americas	257,790	218,579	1,755	66	19,898
Eastern Mediterranean Region	341,624	59,058	38,592	15,069	28,031
European Region	851,849	234,827	37,421	37,332	16,899
South-East Asia Region	199,535	224,925	61,975	83,627	112,418
Western Pacific Region	1,319,640	155,490	176,493	128,016	213,366
Worldwide	4,211,431	1,374,083	836,338	580,287	462,186

Even in countries where vaccination has been introduced, rates may remain high. In Ireland, vaccination was introduced in 1985. There were 99,903 cases that year. Within two years, the number of cases had fallen to 201, but this fall was not sustained. Measles is a leading cause of vaccine-preventable childhood mortality. Worldwide, the fatality rate has been significantly reduced by a vaccination campaign led by partners in the Measles Initiative: the American Red Cross, the United States Centers for Disease Control and Prevention (CDC), the United Nations Foundation, UNICEF and the WHO. Globally, measles fell 60% from an estimated 873,000 deaths in 1999 to 345,000 in 2005.^[14] Estimates for 2008 indicate deaths fell further to 164,000 globally, with 77% of the remaining measles deaths in 2008 occurring within the Southeast Asian region.^[15]

In 2006–07 there were 12,132 cases in 32 European countries: 85% occurred in five countries: Germany, Italy, Romania, Switzerland and the UK. 80% occurred in children and there were 7 deaths.^[16]

Five out of six WHO regions have set goals to eliminate measles, and at the 63rd World Health Assembly in May 2010, delegates agreed a global target of a 95% reduction in measles mortality by 2015 from the level seen in 2000, as well as to move towards eventual eradication. However, no specific global target date for eradication has yet been agreed to as of May 2010.^[17][18]

On January 22, 2014, the World Health Organization and the Pan American Health Organization declared and certified Colombia free of the measles while becoming the first Latin American country to abolish the infection within its borders.^[19][20]

In Vietnam, in the measles epidemic in the beginning of 2014, as of April 19 there were 8,500 measles cases and 114 fatalities,^[21] and as of May 30 there were 21,639 measles cases and 142 fatalities.^[22]

Outbreaks

In 2007, a large outbreak in Japan caused a number of universities and other institutions to close in an attempt to contain the disease.^[23][24]

Many children in ultra-Orthodox Jewish communities were affected due to low vaccination coverage.^[25][26] As of 2008, the disease is endemic in the United Kingdom, with 1,217 cases diagnosed in 2008,^[27] and epidemics have been reported in Austria, Italy and Switzerland.^[28]

On February 19, 2009, 505 measles cases were reported in twelve provinces in northern Vietnam, with Hanoi accounting for 160 cases.^[29] A high rate of complications, including meningitis and encephalitis, has worried health workers,^[30] and the U.S. CDC recommended all travelers be immunized against measles.^[31]

Beginning in April 2009 there was a large outbreak of measles in Bulgaria, with over 24,000 cases including 24 deaths. From Bulgaria, the strain was carried to Germany, Turkey, Greece, Macedonia, and other European countries.^[32]

Beginning in September 2009, Johannesburg, South Africa reported about 48 cases of measles. Soon after the outbreak, the government ordered all children to be vaccinated. Vaccination programs were then initiated in all schools, and parents of young children were advised to have them vaccinated.^[33] Many people were not willing to have the vaccination done, as it was believed to be unsafe and ineffective. The Health Department assured the public that their program was indeed safe. Speculation arose as to whether or not new needles were being used.^[34] By mid-October, there were at least 940 recorded cases, and four deaths.^[35]

In early 2010, there was a serious outbreak of measles in the Philippines with 742 cases, leaving four unvaccinated children dead in the capital city of Manila.^[36]

As of May 2011, over 17,000 cases of measles have so far been reported from France between January 2008 and April 2011, including 2 deaths in 2010 and 6 deaths in 2011.^[37] Over 7,500 of these cases fell in the first three months of 2011, and Spain, Turkey, Macedonia, and Belgium have been among the other European countries reporting further smaller outbreaks.^[38] The French outbreak has been specifically linked to a further outbreak in Quebec in 2011, where 327 cases have been reported between January and June 1, 2011,^[39] and the European outbreaks in general have also been implicated in further small outbreaks in the USA, where 40 separate importations from the European region had been reported between January 1 and May 20.^[40]

Some experts stated that the persistence of the disease in Europe could be a stumbling block to global eradication. It has proven difficult to vaccinate a sufficient number of children in Europe to eradicate the disease, because of opposition on philosophical or religious grounds, or fears of side-effects, or because some minority groups are hard to reach, or simply because parents forget to have their children vaccinated. Vaccination is not mandatory in some countries in Europe, in contrast to the United States and many Latin American countries, where children must be vaccinated before they enter school.^[32]

In March 2013, an epidemic was declared in Swansea, Wales, UK with 1,219 cases and 88 hospitalizations to date.^[41] A 25-year-old male had measles at the time of death and died from giant cell pneumonia caused by the disease.^[42] There have been growing concerns that the epidemic could spread to London and infect many more people due to poor MMR uptake,^[43] prompting the Department of Health to set up a mass vaccination campaign targeted at one million school children throughout England.^[44]

In late 2013, it was reported in the Philippines that 6,497 measles cases occurred which resulted in 23 deaths.^[45]

In 2014 many unvaccinated US citizens visiting the Philippines, and other countries, contracted measles, resulting in 288 cases being recorded in the United States in the first five months of 2014, a twenty-year high.^[46]

In January 2015, it was reported that nineteen people from three states who visited Disneyland or Disney California Adventure between Dec. 15 and Dec. 20 fell ill with measles. Sixteen of the cases were in California, two in Utah, and one in Colorado. Officials in California said that of the 16 cases in the state they have only verified that two were fully vaccinated against the disease. Some were partially vaccinated and at least two were too young to be vaccinated.^[47] Between the dates of January 1 and 28, 2015, most of the 84 people who were diagnosed with measles were either infected during their visit to Disneyland or by someone who visited the theme park.^[48]

Americas

Indigenous measles was declared to have been eliminated in North, Central, and South America; the last endemic case in the region was reported on November 12, 2002, with only northern Argentina and rural Canada, particularly in Ontario, Quebec, and Alberta, having minor endemic status.^[49] Outbreaks are still occurring, however, following importations of measles viruses from other world regions. In June 2006, an outbreak in Boston resulted after a resident became infected in India.^[50]

Canada

The Canadian government defines endemic measles as a situation where a chain of transmission continues uninterrupted for 12 months.^[51] By this standard, Canada has been free of endemic measles since 1998, but sporadic imported outbreaks have continued.^[51]

Southern regions of the province of Quebec witnessed a measles outbreak affecting 94 persons in the Spring and Summer of 2007. The outbreak lasted 25 weeks, included more than one strain of the measles virus and had 12-17 generations of spread.

In 2008, Canada had more than 30 confirmed cases in Ontario in 2008, with more than half reported in Toronto.^[52]

In 2011, Quebec experienced the largest outbreak of measles in the Americas since 2002.^[53] The outbreak began on 8 January with unvaccinated individuals acquiring the disease whilst traveling to France, a country with high measles incidence, and returning home to Quebec.^[54] Public health officials responded to the outbreak by launching a mass vaccination campaign,^[55] and on 22 December, the outbreak ended with a total of 776 cases having occurred. 615 cases (79%) had not been vaccinated, including 29 infants too young to receive the vaccine. 11% of cases required hospitalization, and complications occurred in 64 cases (8%), with pneumonia being the most common complication observed (3% of cases). No deaths were reported.^[53]

A measles outbreak was declared on 8 March 2014 in regions east of Vancouver in the Fraser Valley area where vaccination rates were known to be low in school and religious groups. A total of 228 cases were confirmed. On March 24, Fraser Health Authority said the outbreak have been contained and confined to the original community.^[56]

United States

Indigenous measles were declared to have been eliminated in North, Central, and South America; the last endemic case in the region was reported on November 12, 2002.^[57] Outbreaks are still occurring, however, following importations of measles viruses from other world regions. In June 2006, an outbreak in Boston resulted after a resident became infected in India,^[58] and in October 2007, a Michigan girl who had been vaccinated contracted the disease overseas.^[59]

In 1991 in the Philadelphia region, thousands of children were sick with measles. The epicenter of this outbreak was traced to the Faith Tabernacle Congregation, a Faith Healing church that actively discouraged parishioners from vaccinating their children. A Court Order was obtained to forcibly treat and vaccinate children whose parents would not agree to seeking medical care. Nine children eventually died as a result of this outbreak.^[60]

Between January 1 and April 25, 2008, a total of 64 confirmed measles cases were preliminarily reported in the United States to the Centers for Disease Control and Prevention,^[62][63] the most reported by this date since 2001, and the highest total number in six years.^[64] Of the 64 cases, 54 were associated with importation of measles from other countries into the United States, and 63 of the 64 patients were unvaccinated or had unknown or undocumented vaccination status.^[65] By July 9, 2008, a total of 127 cases were reported in 15 states, making it the largest US outbreak since 1997 (when 138 cases were reported).^[66] Most of the cases were acquired outside of the United States and afflicted individuals who had not been vaccinated.

By July 9, 2008, a total of 127 cases were reported in 15 states (including 22 in Arizona),^[67] making it the largest U.S. outbreak since 1997 (when 138 cases were reported).^[68] Most of the cases were acquired outside of the United States and afflicted individuals who had not been vaccinated. By July 30, 2008, the number of cases had grown to 131. Of these, about half involved children whose parents rejected vaccination. The 131 cases occurred in seven different outbreaks. There were no deaths, and 15 hospitalizations. Eleven of the cases had received at least one dose of measles vaccine. Children who were unvaccinated or whose vaccination status was unknown accounted for 122 cases. Some of these were under the age when vaccination is recommended, but in 63 cases, the vaccinations had been refused for religious or philosophical reasons.

In early 2008 there was an outbreak of measles in San Diego, California. The outbreak is traced to an unvaccinated 7-year-old child who went on a family trip to Europe.^[69][70] The CDC refers to this as an "import-associated outbreak".^[69] The final diagnosis included 11 additional cases of measles in unvaccinated children in San Diego.^[69] All of the confirmed patients were not vaccinated because they were younger than 1, the minimum age for measles inoculation, or because their parents declined to have them vaccinated.^[71] The typical vaccine would be the MMR vaccine. The incident drew attention to the controversy over MMR vaccination. This was San Diego County's first measles outbreak since 1991.^[71]

In February 2008 there was an outbreak of measles in Pima County, Arizona. There were 13 laboratory confirmed and 4 probable measles cases, though 22 cases were previously reported.^[72] The outbreak started with a visitor from Switzerland and resulted in a public health emergency declaration by Pima County.^[72] The last confirmed Pima County case occurred in 1994, and the last outbreak occurred in 1991.^[73]

On May 24, 2011, the Centers for Disease Control and Prevention reported that the United States has had 118 measles cases so far this year. The 118 cases were reported by 23 states and New York City between Jan 1 and May 20. Of the 118 cases, 105 (89%) were associated with cases abroad and 105 (89%) of the 118 patients had not been vaccinated.^[74]

In 2013, at least 20 members of the Eagle Mountain International Church in North Texas were diagnosed with measles after a few members of the congregation traveled abroad on a mission trip and contracted the disease. The church is part of Kenneth Copeland Ministries, which used to advocate abstaining from vaccinations and immunizations for fear they cause autism.^[75] The church has sponsored several vaccination drives.^[76] Senior Pastor Terri Pearsons, who had previously expressed concerns about potential links between the measles vaccine and autism, was encouraging parishioners to get vaccinated. However, she said she still has some concerns about vaccines, particularly for young children with a family history of autism, and where several immunizations are given at the same time. William Schaffner, professor at the Vanderbilt University School of Medicine, described the pastor as "misinformed" and said that young children are among the most vulnerable to measles.^[77]

In February and March 2014, 20 confirmed cases appeared in New York City.^[78]

In December 2014, a measles outbreak began at Disneyland in Southern California. At least 173 people have become infected with measles in 21 states, as of May 2015. Health officials say 39 cases have been traced to direct exposure at the park, with 117 infections linked by primary or secondary exposure. Among the 110 California patients, 49 (45%) were unvaccinated; five (5%) had 1 dose of measles-containing vaccine, seven (6%) had 2 doses, one (1%) had 3 doses, 47 (43%) had unknown or undocumented vaccination status, and one (1%) had immunoglobulin G seropositivity documented, which indicates prior vaccination or measles infection at an undetermined time. 12 of the unvaccinated patients were infants too young to be vaccinated.^[79][80] Medical professionals, such as David Gorski, have criticized physicians and pediatricians in the area who do not adhere to the CDC's recommended vaccination schedule or discourage vaccination, among them Bob Sears and Jay Gordon for reducing vaccination rates and thus weakening herd immunity, and creating a situation in which an outbreak was more likely.^[81][82] California passed a mandatory vaccination law in June.^[83]

In Spring 2015, a death of an immune-suppressed woman in Washington State caused by measles was diagnosed after autopsy. This was the first U.S. measles death since 2003.^[84]

Asia

Israel

Approximately 1000 cases of the disease were reported in Israel between August 2007 and May 2008 (in sharp contrast to just some dozen cases the year before). Many children in ultra-Orthodox Jewish communities were affected due to low vaccination coverage.^[85][86]

Japan

In 2007, a large measles outbreak in Japan caused a number of universities and other institutions to close in an attempt to contain the disease.^[87][88]

Philippines

In 2014 the Philippines experienced a large ongoing measles outbreak. According to the World Health Organization there were 57,564 suspected cases of measles, including 21,403 confirmed cases, 110 measles deaths, were reported in the Philippines from January 1 through December 20, 2014. Most of the cases were among unvaccinated people.^[89]

Europe

In 2008, Europe faced a measles epidemic, including large outbreaks in Austria, Italy, and Switzerland.^[90] In 2010, 30,367 cases were reported from across the 32 European countries reporting to euvac.net (72% of which were reported from Bulgaria, and 17% from France), and 21 measles-related deaths (17 in Bulgaria, 2 in France, and 1 in Romania).^[91] The World Health Organization reported over 26,000 measles cases in 36 European countries from January to October 2011, with 83% occurring in western Europe.^[92] There were nine deaths, of which six were French, and 7,288 hospitalizations.^[92] In February 2014, 26 cases in Barcelona, Spain.^[93]

Ukraine

Ukraine has had a multiple large outbreaks of measles. In 2001-2002, there were around 25,000 cases and 14 deaths reported.^[94] In 2006 with 44,534 reported cases with at least 2 deaths.^[95] 13,517 cases were reported in 2012.^[96]

Germany

Germany has faced repeated outbreaks in the 21st century. 6,037 cases were reported in 2001 with at least two deaths.^[97] More than 1,500 cases were reported in 2006.^[98] 1,600 cases were reported in an outbreak in 2013.^[98] An outbreak in 2015 had more than 1,700 cases had been reported by May 11 with one death.^[99]

Netherlands

In September 2008 an outbreak occurred among anthroposophists' children in the cities of The Hague and Utrecht. Some 90 infections of unvaccinated children were recorded by the Dutch National Institute for Public Health and the Environment (RIVM) by September 29. It was expected the outbreak would spread to the region of the Veluwe, locally known as a bijbelgordel ("Bible Belt") with a large population of unvaccinated children on religious grounds.^[100]

In June 2013, another outbreak occurred in the Bible Belt in The Netherlands. According to newspaper Algemeen Dagblad, there were 161 infections, of which 5 infected victims were hospitalized critically ill. 2 of the victims had meningitis, two others had pneumonia and from one of them, the complications are still unknown.^[101]

United Kingdom

After the MMR vaccine controversy began, the MMR vaccination compliance dropped sharply in the United Kingdom, from 92% in 1996 to 84% in 2002. In some parts of London, it was as low as 61% in 2003, far below the rate needed to avoid an epidemic of measles.^[102] By 2006 coverage for MMR in the UK at 24 months was 85%, lower than the about 94% coverage for other vaccines.^[103]

After vaccination rates dropped, the incidence of two of the three diseases increased greatly in the UK. In 1998 there were 56 confirmed cases of measles in the UK; in 2006 there were 449 in the first five months of the year, with the first death since 1992.^[104] Cases occurred in inadequately vaccinated children.^[104] The age group affected was too old to have received the routine MMR immunizations around the time the paper by Wakefield et al. was published, and too young to have contracted the natural disease as a child, and thus to achieve a herd immunity effect. With the decline in infection that followed the introduction of the MMR vaccine, these individuals had not been exposed to the disease, but still had no immunity, either natural or vaccine induced. Therefore, as immunization rates declined following the controversy and the disease re-emerged, they were susceptible to infection.^[105][106] Measles cases continued in 2006, at incidence rates 13 times greater than 1998 levels.^[107] Two children were severely and permanently injured by measles encephalitis despite undergoing kidney transplantation in London.^[108] Disease outbreaks also caused casualties in nearby countries including Ireland.

In 2008, for the first time in 14 years, measles was declared endemic in the UK, meaning that the disease was sustained within the population. This was caused by the preceding decade's low MMR vaccination rates, which created a population of susceptible children who could spread the disease. In May 2008, a British 17-year-old with an underlying immunodeficiency died of measles.^[109]

An outbreak centered on the Swansea area of Wales started in November 2012; as of 22 April there have been 886 cases.^[110]

Ireland

1,500 cases and three deaths were reported in the Irish outbreak of 2000, which occurred as a direct result of decreased vaccination rates following the MMR scare.^[108]

Bulgaria

Beginning in April 2009 there was a large outbreak of measles in Bulgaria, with 23,791 cases, including 24 deaths, reported up to 28 July 2010.^[111] From Bulgaria, the strain was carried to Germany, Turkey, Greece, Macedonia, and other European countries.^[112]

France

Between January 2008 and May 2012, 22,000 measles cases were reported in France. 5,000 patients were hospitalised including 1,023 with severe pneumonia, 27 with encephalitis and/or myelitis, and 10 died.^[113] An awareness campaign about MMR vaccination was launched.^[92]

Portugal

Most recent reported cases of measles in Portugal are originally imported from other European countries (United Kingdom, France and Romania), Africa (Angola, South African and Ethiopia) and Asia (China).^[114] Since 2004, Portugal reported 22 confirmed cases of measles. Virus isolates from 2005 and 2008 outbreaks belong the genotype D4.^[115] Vaccination coverage in Portugal is ≥95% (since 2006) but pockets of reduced immunization coverage (85-94%) still persist in the population.^[116]

Oceania

Australia

Fourteen cases have been reported in multiple Australian and New Zealand cities including Melbourne and Auckland in the period between December 7, 2013 and January 3, 2014. The outbreak is believed to have begun at the 2013 World Supremacy Battlegrounds dance festival held in Sydney, Australia.^[117]

New Zealand

Ten cases were reported in Christchurch in July 2009.^[118]

An outbreak between 25 May 2011 and 24 July 2012 in the Auckland region had 489 confirmed or probable cases of measles, 82 of which required hospitalisation.^[119] The outbreak was started with an unimmunised child becoming infected on a family trip to England, then developing measles back in Auckland.^[119]

In June and July 2014, 124 confirmed cases of measles were reported in Hamilton. Eighty percent of persons infected were aged between 10 and 20, and all but four were not immunised. Most of those infected were linked with Fraser High School in the city's west, resulting in the school cancelling all school trips and cultural and sporting events.^[120][121]

References