Robert T. Perry, MD1; Jillian S. Murray, MSPH1; Marta Gacic-Dobo, MSc1; Alya Dabbagh, PhD1; Mick N. Mulders, PhD1; Peter M. Strebel, MBChB1; Jean-Marie Okwo-Bele, MD1; Paul A. Rota, PhD2; James L. Goodson, MPH3
In 2000, the United Nations General Assembly adopted the Millennium Development Goals (MDG), with MDG4 being a two-thirds reduction in child mortality by 2015, and with measles vaccination coverage being one of the three indicators of progress toward this goal.* In 2010, the World Health Assembly established three milestones for measles control by 2015: 1) increase routine coverage with the first dose of measles-containing vaccine (MCV1) for children aged 1 year to =90% nationally and =80% in every district; 2) reduce global annual measles incidence to fewer than five cases per million population; and 3) reduce global measles mortality by 95% from the 2000 estimate (1).† In 2012, the World Health Assembly endorsed the Global Vaccine Action Plan§ with the objective to eliminate measles in four World Health Organization (WHO) regions by 2015. WHO member states in all six WHO regions have adopted measles elimination goals. This report updates the 2000–2013 report (2) and describes progress toward global control and regional measles elimination during 2000–2014. During this period, annual reported measles incidence declined 73% worldwide, from 146 to 40 cases per million population, and annual estimated measles deaths declined 79%, from 546,800 to 114,900. However, progress toward the 2015 milestones and elimination goals has slowed markedly since 2010. To resume progress toward milestones and goals for measles elimination, a review of current strategies and challenges to improving program performance is needed, and countries and their partners need to raise the visibility of measles elimination, address barriers to measles vaccination, and make substantial and sustained additional investments in strengthening health systems.
Immunization Activities
To estimate coverage with MCV1 and the second dose of MCV (MCV2) through routine immunization services,¶ WHO and the United Nations Children's Fund (UNICEF) use data from administrative records and surveys reported annually by the 194 WHO countries. From 2000 to 2010, estimated MCV1 coverage increased globally from 72% to 85%, and remained at 85% through 2014 (Tables 1 and 2). The number of countries with =90% MCV1 coverage increased from 84 (44%) in 2000 to 131 (68%) in 2012, then decreased to 122 (63%) in 2014. Since 2003, countries also have reported the number of districts with =80% MCV1 coverage. Among countries with =90% MCV1 coverage nationally, the percentage having =80% MCV1 coverage in all districts increased from 1% (1 of 103) in 2003 to 44% (57 of 131) in 2012, then declined to 40% (49 of 122) in 2014. Among the estimated 20.6 million infants who did not receive MCV1 through routine immunization services in 2014, approximately 11.6 million (56%) were in six countries: the Democratic Republic of the Congo (0.6 million), Ethiopia (0.9 million), India (4.2 million), Indonesia (1 million), Nigeria (3.3 million), and Pakistan (1.6 million).
During 2000–2014, the number of countries providing MCV2 nationally through routine immunization services increased from 97 (51%) to 154 (79%), with six countries (Burkina Faso, Morocco, Niger, Rwanda, Senegal, Tanzania) introducing MCV2 in 2014. Estimated global MCV2 coverage increased from 15% in 2000 to 56% in 2014. During 2014, approximately 221 million children received MCV during mass immunization campaigns known as supplementary immunization activities (SIAs)** conducted in 29 countries, with 23 countries (79%) providing one or more additional child health interventions during the SIA (Figure). Based on doses administered, SIA coverage was =95% in 16 (55%) countries; however, of the five countries conducting post-SIA coverage surveys, only one estimated SIA coverage at =95%.
Disease Incidence
Countries report the number of measles cases from either case-based or aggregate surveillance systems†† to WHO and UNICEF each year. Effective measles surveillance includes case-based surveillance with laboratory testing to confirm cases. In 2014, 187 (96%)§§ countries used case-based surveillance, and 191 (98%)¶¶ had access to standardized quality-controlled testing through the WHO Global Measles and Rubella Laboratory Network.
During 2000–2014, the number of annually reported measles cases worldwide decreased 69%, from 853,479 to 267,482, and measles incidence decreased 73%, from 146 to 40 cases per million population (Tables 1 and 2). The results for 2014 represent little change from those reported in 2013 (280,795 cases and 40 cases per million population), although fewer countries reported in 2014 (169) compared with 2013 (175).*** The percentage of reporting countries with <5 cases per million decreased from 65% (113 of 175) in 2013 to 58% (98 of 169) in 2014. During 2000–2014, the Region of the Americas (AMR) maintained measles incidence at fewer than 5 cases per million.
Measles incidence decreased in four of six WHO regions from 2013 to 2014 (Table 2). In the African Region (AFR), reported cases decreased 57%, from 171,178 cases in 2013 to 73,914 in 2014, largely because of decreases in the Democratic Republic of the Congo (from 88,381 to 33,711) and Nigeria (from 52,852 to 6,855). However, in 2014, outbreaks occurred in Angola (11,699) and Ethiopia (12,739 cases). In the Eastern Mediterranean Region (EMR), the European Region (EUR), and the South-East Asia Region (SEAR), reported cases also decreased in 2014, although large outbreaks were reported in India (24,977), Somalia (10,278 cases), and Russia (4,711) in 2014. Increased numbers of cases were reported in 2014 from AMR, largely because of outbreaks in Brazil (727 cases) and the United States (667); and from the Western Pacific Region (WPR), because of large outbreaks reported in China (52,628), the Philippines (58,848 cases), and Vietnam (15,033).
Genotypes of viruses isolated from measles cases were reported to WHO by 69 (41%) of the 169 countries reporting measles cases in 2014. Of the 24 recognized measles virus genotypes, 11 were detected during 2005–2008 and eight during 2009–2014, excluding those from vaccine reactions and cases of subacute sclerosing panencephalitis (3). In 2014, among 7,155 reported sequences,††† 1,328 (50 countries) were genotype B3, 38 (eight countries) were D4, 1,083 (45 countries) were D8, 92 (12 countries) were D9, four (four countries) were G3, and 4,610 (18 countries) were H1 (Table 2).
Mortality Estimates
WHO has developed a model to estimate measles mortality in countries using numbers and age distribution of reported cases, routine and SIA MCV coverage, and age- and country-specific case-fatality ratios (4,5). New measles vaccination coverage and case data for all countries during 2000–2014 led to a new series of mortality estimates. During this period, estimated measles deaths decreased 79%, from 546,800 to 114,900, and all regions had substantial reductions in estimated measles mortality (Tables 1 and 2). Compared with no measles vaccination, measles vaccination prevented an estimated 17.1 million deaths during 2000–2014 (Figure).
Regional Verification of Measles Elimination
Since the last report, the AMR regional verification committee determined that AMR cannot be declared measles free, because Brazil has had sustained transmission of a single measles virus strain for >1 year. The WPR regional verification committee verified absence of endemic measles in two member states and one area, bringing the total to seven in WPR (6); the EUR regional verification committee verified measles elimination in 22 member states (7).
Discussion
During 2000–2014, increased coverage worldwide with both (1st and 2nd) routine doses of MCV, combined with SIAs in countries that lack high coverage with 2 doses of MCV, contributed to a 73% decrease in reported measles incidence and a 79% reduction in estimated measles mortality. During this period, measles vaccination prevented an estimated 17.1 million deaths. However, on the basis of current trends in measles vaccination coverage and incidence, the WHO Strategic Advisory Group of Experts on Immunization concluded that the 2015 global milestones and measles elimination goals will not be achieved (8).
Measles can serve as an indicator of the strength and reach of the health system, as measles outbreaks reveal populations poorly served by health services. In high-burden, low-coverage countries, outbreak investigations have also found low MCV1 coverage where long-standing policies and practices prevent vaccination of children aged =12 months, discourage opening a 10-dose vial when few children are present, and limit measles vaccination to only one session per month (Global Immunization Division, Center for Global Health, CDC, unpublished data, 2015). Addressing these gaps, maximizing how SIA planning and implementation can improve routine services, and conducting high-quality SIAs should increase coverage and equity for all vaccines and further reduce the number of measles cases and deaths. As coverage improves, establishing a visit during the second year of life integrating MCV2 and other child health interventions should help to further reduce measles burden.
The findings in this report are subject to at least three limitations. First, MCV coverage estimates are affected by inclusion of SIA doses administered to children outside the target group, inaccurate estimates of the target population size, and inaccurate reports of the number of doses delivered. Second, under-ascertainment of measles cases through surveillance systems can occur, because not all patients with measles seek care and not all cases are reported. Third, some countries report aggregate numbers of unconfirmed cases rather than case-based data.
The decrease in measles mortality is among three main contributors (along with decreases in pneumonia and diarrhea) to the decline in overall child mortality and progress toward MDG4 (9). To assess the reasons for the slowing of progress since 2010 and to modify current strategies as needed, the Measles & Rubella Initiative§§§ partners have commissioned a midterm strategy review. Countries and their partners need to raise the visibility of measles elimination, and secure the resources needed to implement strategies required to reach measles control and elimination goals, taking into account the results and recommendations from the review.
1Department of Immunization, Vaccines, and Biologicals, World Health Organization; 2Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, CDC; 3Global Immunization Division, Center for Global Health, CDC.
Corresponding author: James L. Goodson, jgoodson@cdc.gov, 404-639-8170.
World Health Organization. Genetic diversity of wild-type measles viruses and the global measles nucleotide surveillance database (MeaNS). Wkly Epidemiol Rec 2015;90:373–80.
Simons E, Ferrari M, Fricks J, et al. Assessment of the 2010 global measles mortality reduction goal: results from a model of surveillance data. Lancet 2012;379:2173–8.
Chen S, Fricks J, Ferrari MJ. Tracking measles infection through non-linear state space models. J R Stat Soc Ser C Appl Stat 2012;61:117–24.
World Health Organization. Meeting report of the Strategic Advisory Group of Experts (SAGE) on Immunization, October 2015. Geneva, Switzerland: World Health Organization; 2015. Available at http://www.who.int/immunization/global_vaccine_action_plan.
Liu L, Oza S, Hogan D, et al. Global, regional, and national causes of child mortality in 2000–13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 2015;385:430–40.
† Whereas the coverage milestone is to be met by every country, the incidence and mortality reduction milestones are to be met globally.
§ The Global Vaccine Action Plan is the implementation plan of the Decade of Vaccines, a collaboration between WHO, UNICEF, the Bill and Melinda Gates Foundation, Gavi, the Vaccine Alliance, the U.S. National Institute of Allergy and Infectious Diseases, the African Leaders Malaria Alliance, and others to extend the full benefit of immunization to all persons by 2020 and beyond. Additional information is available at http://www.who.int/immunization/global_vaccine_action_plan and at http://apps.who.int/gb/ebwha/pdf_files/wha65/a65_22-en.pdf.
¶ For MCV1, among children aged 1 year or, if MCV1 is given at age =1 year, among children aged 24 months. For MCV2, among children at the recommended age of administration of MCV2, as per the national immunization schedule. WHO/UNICEF estimates of national immunization coverage are available at http://www.who.int/immunization/monitoring_surveillance/data.
** Supplemental immunization activities (SIAs) generally are carried out using two target age ranges. An initial, nationwide catch-up SIA focuses on all children aged 9 months–14 years, with the goal of eliminating susceptibility to measles in the general population. Periodic follow-up SIAs then focus on all children born since the last SIA. Follow-up SIAs generally are conducted nationwide every 2–4 years and focus on children aged 9–59 months; their goal is to eliminate any measles susceptibility that has developed in recent birth cohorts and to protect children who did not respond to MCV1.
§§ Countries without case-based measles surveillance in 2014 were Djibouti, India, Mauritius, Sao Tome and Principe, Seychelles, Somalia, and South Sudan.
¶¶ Countries without access to standardized quality-controlled testing by the WHO Measles and Rubella Laboratory Network in 2014 were Cape Verde, Sao Tome and Principe, and Seychelles.
*** Countries not reporting in 2013 were Cuba (AMR); Bahrain, Libya, and the United Arab Emirates (EMR); Austria, Bosnia and Herzegovina, Italy, Malta, Monaco, San Marino, and Ukraine (EUR); and Brunei Darussalam, Cook Islands, Fiji, the Marshall Islands, Nauru, Samoa, Singapore, and Tuvalu (WPR). In 2014, countries not reporting were Djibouti and Oman (EMR); Albania, Andorra, Croatia, Finland, Italy, Luxembourg, Monaco, Montenegro, Poland, San Marino, and Ukraine (EUR); Indonesia and Thailand (SEAR); and Cook Islands, Fiji, Marshall Islands, Nauru, Niue, Singapore, Solomon Islands, Tonga, Tuvalu, and Western Samoa (WPR).
††† Sequences were for the 450 nucleotide carboxy-terminal of the nucleocapsid gene in the measles virus genome. Genotypes isolated from three cases of subacute sclerosing panencephalitis (D3, D6, and D7) were excluded from the total. Data (as of October 7, 2015) available from the Measles Nucleotide Surveillance (MeaNS) database, available at http://www.who-measles.org/Public/Web_Front/main.php.
§§§ The Measles & Rubella Initiative is a partnership established in 2001 as the Measles Initiative, led by the American Red Cross, CDC, the United Nations Foundation, UNICEF, and WHO. Additional information is available at http://www.measlesrubellainitiative.org.
Summary
What is already known on this topic?
During 2000–2010, global vaccination coverage with the 1st dose of measles-containing vaccine (MCV1) increased from 72% to 85%, and annual measles incidence decreased from 146 reported cases per million population in 2000 to 50 cases per million in 2010. During 2010–2013, MCV1 coverage and measles incidence did not significantly change.
What is added by this report?
During 2000–2014, an estimated 17.1 million deaths were prevented by measles vaccination, and measles incidence decreased 73%, from 146 to 40 cases per million population. The number of countries providing the 2nd dose of measles-containing vaccine (MCV2) nationally through routine immunization services increased to 154 (79%) in 2014, and global MCV2 coverage was 56%. During 2014, a total of 221 million children were vaccinated against measles during supplementary immunization activities.
What are the implications for public health practice?
Although measles vaccination has saved millions of lives since 2000, progress has slowed since 2010. Reaching measles control and elimination goals will require addressing policy and practice gaps that prevent reaching larger numbers of children with measles vaccination, increasing visibility of measles elimination efforts, and ensuring adequate resources for strengthening health systems.
TABLE 1. Estimates of coverage with the first dose of measles-containing vaccine administered through routine immunization services among children aged 1 year, reported measles cases and incidence, and estimated measles mortality,* by World Health Organization region — worldwide, 2000
WHO region
2000
Coverage with 1st dose (%)†
Countries with =90% coverage (%)
Coverage with 2nd dose (%)
Reported cases (No.) §
Incidence¶,**
Countries with incidence <5/million (%)
Estimated deaths (95% CI)
African
53
9
5
520,102
841
8
342,800 (225,400–574,200)
Americas
93
63
45
1,754
2.1
89
NA
Eastern Mediterranean
72
57
28
38,592
90
17
54,300 (32,200–91,100)
European
91
60
49
37,421
50
48
300 (100–2,200)
South-East Asia
63
30
3
78,558
51
0
138,500 (102,100–185,900)
South-East Asia (excluding India)
78
33
9
39,723
80
0
52,700 (32,700–81,300)
India
56
NA
0
38,835
37
0
85,800 (69,400–104,700)
Western Pacific
85
44
2
177,052
105
30
10,800 (5,400–53,600)
Total
72
44
15
853,479
146
38
546,800 (365,200–907,000)
Abbreviations: CI = confidence interval; NA = not applicable; WHO = World Health Organization.
* Mortality estimates for 2000 might be different from previous reports: when WHO and UNICEF rerun the model used to generate estimated measles deaths each year using the new WHO/UNICEF Estimates of National Immunization Coverage (WUENIC) data, as well as updated surveillance data, adjusted results for each year, including the baseline year, are also produced and updated.
¶ Cases per million population; population data from United Nations, Department of Economic and Social Affairs, Population Division (2013).
** Any country not reporting data on measles cases for that year was removed from both the numerator and denominator.
TABLE 2. Estimates of coverage with the first dose of measles-containing vaccine administered through routine immunization services among children aged 1 year, reported measles cases and incidence, and estimated measles mortality, by World Health Organization region — worldwide, 2014
WHO Region
2014
Coverage with 1st dose (%)*
Countries with =90% coverage (%)
Coverage with 2nd dose (%)
Reported cases (No.)†
Decline in cases from 2000 (%)
Incidence§,¶
Decline in incidence from 2000 (%)
Countries with incidence <5/ million (%)
Reported genotypes**
Estimated deaths (95% CI)
Mortality reduction 2000–2014 (%)
African
73
30
11
73,914
86
78
91
51
B3
48,000 (15,400–145,600)
86
Americas
92
77
51
1,817
NA
1.9
11
97
B3 D4 D8 D9 H1
NA
NA
Eastern Mediterranean
77
57
66
18,129
53
29
68
21
B3 D4 D8 H1
13,900 (9,500–38,400)
74
European
94
83
84
14,176
62
19
62
60
B3 D4 D8 H1
100 (0–1,800)
67
South-East Asia
84
45
59
28,403
64
18
64
56
B3 D4 D8
46,900 (27,900–80,800)
66
South-East Asia (excluding India)
85
50
78
3,426
91
12
85
63
B3 D4 D8
8,100 (2,700–25,400)
85
India
83
NA
51
24,977
36
20
47
0
B3
38,800 (25,300–55,400)
55
Western Pacific
97
74
93
131,043
26
71
33
35
B3 D4 D8 D9 G3 H1
6,100 (800–63,300)
44
Total
85
63
56
267,482
69
40
73
58
114,900 (53,700–330,000)
79
Abbreviations: CI = confidence interval; NA = not applicable; WHO = World Health Organization.
TABLE 3. Measles supplementary immunization activities* and the delivery of other child health interventions, by country and World Health Organization region — worldwide, 2014
WHO region/country
Age group targeted
Extent of SIA
Children reached No. (%)†
Other interventions delivered
African
Angola
6 mos–9 yrs
National
9,169,335 (117)
Oral poliovirus vaccine, vitamin A
Benin
9 mos–9 yrs
National
2,621,634 (100)
Burkina Faso
9 mos–14 yrs
National
8,481,625 (106)
Rubella vaccine
Chad
9 mos–9 yrs
National
4,886,532 (103)
Cote d'Ivoire
6 mos–9 yrs
National
9,640,512 (92)
Vitamin A, deworming, medication
Democratic Republic of the Congo
6 mos–9 yrs
Rollover-national§
18,539,883 (101)
Oral poliovirus vaccine, vitamin A, deworming medication
Guinea
6 mos–9 yrs
Outbreak response
1,411,043 (99)
Mauritania
9 mos–14 yrs
National
1,489,563 (105)
South Sudan
6–59 mos; 6 mos–15 yrs
National
2,172,737 (91)
Oral poliovirus vaccine, vitamin A
Tanzania
9 mos–14 yrs
National
20,529,629 (97)
Oral poliovirus and rubella vaccines, vitamin A, deworming medication
Americas
Argentina
1–4 yrs
National
2,347,019 (82)
Oral poliovirus, rubella, and mumps vaccines
Brazil
1–4 yrs
National
9,805,102 (89)
Oral poliovirus, rubella, and mumps vaccines
Paraguay
1–5 yrs
National
533,889 (72)
Oral poliovirus, rubella, and mumps vaccines
Venezuela
1–5 yrs
National
2,466,543 (99)
Oral poliovirus, rubella, and mumps vaccines
Eastern Mediterranean
Afghanistan
9–59 mos; 6 mos–10 yrs
Subnational
842,134 (94)
Iraq
9–36 mos
National
3,295,122 (96)
Lebanon
9 mos–18 yrs
National
1,056,830 (72)
Rubella vaccine
Pakistan
9 mos–9 yrs
Rollover-national§
25,091,751 (103)
Oral poliovirus vaccine
Somalia
9–59 mos
Subnational child health days and SIAs in newly accessible areas
1,251,090 (67)
Oral poliovirus and tetanus toxoid vaccines, vitamin A, deworming medication
Syria
7 mos–5 yrs; =15 yrs in high-risk areas
Subnational
769,408 (74)
Rubella and mumps vaccines
Yemen
9 mos–14 yrs
National
11,368,968 (93)
Oral poliovirus and rubella vaccines
European
Azerbaijan
10–14 yrs
National
164,560 (96)
Rubella and mumps vaccines
Georgia
=14 yrs
National
28,718 (106)
Rubella and mumps vaccines
South-East Asia
Bangladesh
9 mos–14 yrs
National
53,644,603 (102)
Oral poliovirus and rubella vaccines
Western Pacific
Laos
9 mos–9 yrs
National
1,569,224 (101)
Oral poliovirus and rubella vaccines, deworming medication
Micronesia
12 mos–49 yrs; 12 mos–57 yrs
National
71,388 (87)
Rubella and mumps vaccines
Philippines
6–36 mos
Outbreak response
12,098,419 (89)
Oral poliovirus and rubella vaccines (only in national SIA)
9–59 mos
National
Solomon Islands
6 mos–29 yrs
National
394,584 (105)
Rubella vaccine
Viet Nam
9 mos–10 yrs
Subnational
15,147,961 (93)
Rubella vaccine (only in national SIA)
1–14 yrs
National
Total
220,889,806
Abbreviations: SIA = supplementary immunization activity; WHO = World Health Organization.
* SIAs typically are carried out using two approaches: 1) An initial, nationwide catch-up SIA targets all children aged 9 months–14 years, with the goal of eliminating susceptibility to measles in the general population and periodic follow-up SIAs then target all children born since the last SIA. 2) Follow-up SIAs are typically conducted nationwide every 2–4 years and typically target children aged 9–59 months; their goal is to eliminate any measles susceptibility that has developed in recent birth cohorts and to protect children who did not respond to the first measles vaccination. The exact age range for follow-up SIAs depends on the age-specific incidence of measles, coverage with 1 dose of measles-containing vaccine, and the time since the last SIA.
† When coverage >100% the intervention reached more persons than the estimated target population.
§ Rollover national campaigns started the previous year or will continue into the next year.
FIGURE. Estimated number of measles deaths and number of deaths averted by measles vaccination — worldwide, 2000–2014
Alternate Text: The figure is a combination line and bar chart showing the estimated number of measles deaths and number of deaths averted by measles vaccination worldwide during 2000-2014.