Progress Toward Measles Elimination — Western Pacific Region, 2013–2017

José E. Hagan, MD1; Jennifer L. Kriss, PhD2; Yoshihiro Takashima, MD, PhD1; Kayla Mae L. Mariano1; Roberta Pastore, MD1; Varja Grabovac, MSc1; Alya J. Dabbagh, PhD3; James L. Goodson, MPH2 (View author affiliations)

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Summary

What is already known about this topic?

Most countries in the World Health Organization Western Pacific Region (WPR) have made substantial progress toward measles elimination.

What is added by this report?

During 2013–2016, a resurgence of measles occurred in WPR, with large-scale outbreaks in Mongolia, the Philippines, and Vietnam, and increased endemic transmission in China; in 2014, annual incidence increased to 68.9 cases per million. However, with control of the outbreaks, in 2017, incidence decreased to a new historic low (5.2 per million).

What are the implications for public health practice?

Achieving high reported vaccination coverage is not sufficient for achieving regional measles elimination. Efforts by WPR countries are needed to establish high population immunity, build strong immunization systems, maintain high-quality surveillance, and improve outbreak preparedness and response.

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In 2005, the Regional Committee for the World Health Organization (WHO) Western Pacific Region (WPR)* established a goal for measles elimination by 2012 (1). To achieve this goal, the 37 WPR countries and areas implemented the recommended strategies in the WPR Plan of Action for Measles Elimination (2) and the Field Guidelines for Measles Elimination (3). The strategies include 1) achieving and maintaining ≥95% coverage with 2 doses of measles-containing vaccine (MCV) through routine immunization services and supplementary immunization activities (SIAs), when required; 2) conducting high-quality case-based measles surveillance, including timely and accurate testing of specimens to confirm or discard suspected cases and detect measles virus for genotyping and molecular analysis; and 3) establishing and maintaining measles outbreak preparedness to ensure rapid response and appropriate case management. This report updates the previous report (4) and describes progress toward measles elimination in WPR during 2013–2017. During 2013–2016, estimated regional coverage with the first MCV dose (MCV1) decreased from 97% to 96%, and coverage with the routine second MCV dose (MCV2) increased from 91% to 93%. Eighteen (50%) countries achieved ≥95% MCV1 coverage in 2016. Seven (39%) of 18 nationwide SIAs during 2013–2017 reported achieving ≥95% administrative coverage. After a record low of 5.9 cases per million population in 2012, measles incidence increased during 2013–2016 to a high of 68.9 in 2014, because of outbreaks in the Philippines and Vietnam, as well as increased incidence in China, and then declined to 5.2 in 2017. To achieve measles elimination in WPR, additional measures are needed to strengthen immunization programs to achieve high population immunity, maintain high-quality surveillance for rapid case detection and confirmation, and ensure outbreak preparedness and prompt response to contain outbreaks.

Immunization Activities

MCV1 and MCV2 coverage data are reported annually to WHO and the United Nations Children’s Fund (UNICEF) from 36 of the 37 WPR countries and areas.§ WHO and UNICEF estimate vaccination coverage for 27 countries/areas in the region, using annual government-reported survey and administrative data; for the remaining areas and territories, reported coverage data from immunization program monitoring are used. Regional MCV1 and MCV2 coverage rates were maintained at ≥95% and >90%, respectively, during 2013–2016 (Table 1). In 2016, 18 (50%) of 36 countries achieved ≥95% MCV1 coverage, and 11 (31%) reported ≥95% coverage with both MCV1 and MCV2. As of 2017, only two (5%) WPR countries and areas (Solomon Islands and Vanuatu) had not yet introduced MCV2. During 2013–2017, 18 national SIAs were conducted (Table 2); in addition, Japan conducted annual SIAs targeting schoolchildren aged 13 years and 17 years. Reported vaccination coverage was ≥95% in seven (39%) of the nationwide SIAs.

Surveillance Activities

Case-based measles and rubella surveillance data are reported monthly to WHO from all WPR countries and areas; 21 countries and areas of the Pacific Islands report data as one epidemiologic block.** The WHO Global Measles and Rubella Laboratory Network supports surveillance by providing laboratory confirmation and genotyping of reported cases. Suspected measles cases are confirmed based on laboratory findings, an epidemiologic link, or clinical criteria.†† Key indicators of surveillance performance include 1) the number of suspected measles cases discarded as nonmeasles (target: ≥2 per 100,000 population); 2) the proportion of second-level administrative units with two or more nonmeasles discarded cases per 100,000 population (target: ≥80%); 3) the percentage of suspected measles cases with adequate investigation that includes all essential data elements§§ (target: ≥80%); 4) the percentage of suspected measles cases with adequate specimens collected within 28 days of rash onset (target: ≥80%, excludes epidemiologically linked cases); and 5) the percentage of specimens with laboratory results available within 7 days after receipt in the laboratory (target: ≥80%). During 2013–2017, the number of WPR countries and areas¶¶ that met the target for suspected cases discarded as nonmeasles per 100,000 population at the national level decreased from 11 (65%) to nine (53%), but increased from one (6%) to two (12%) at the subnational level. From 2013 to 2017, the percentage of suspected cases with adequate investigations decreased from 92% to 89%; the percentage of suspected cases with adequate specimens collected for laboratory testing decreased from 90% to 89%; and the proportion of blood specimens received by the laboratory with results available within 7 days increased from 84% to 98% (Supplementary Table, https://stacks.cdc.gov/view/cdc/53519).

Measles Incidence and Genotypes

WPR experienced a resurgence of measles during 2013–2016 (Figure), after a record low incidence of 5.9 cases per million population in 2012. During the resurgence, incidence of seasonal endemic measles virus transmission in China increased, and large-scale nationwide outbreaks occurred in other countries with endemic measles (Malaysia and the Philippines). During 2013–2016, after importations from countries with endemic disease, measles outbreaks also occurred in countries that had been verified as having eliminated endemic measles virus transmission (Australia, Cambodia, Japan, and South Korea), including a large-scale outbreak in Mongolia. An increase in importations also led to outbreaks in several countries with endemic, low-incidence measles, including New Zealand, Papua New Guinea, Singapore, Solomon Islands, and Vietnam. Annual regional measles incidence per 1 million population increased from 19.2 in 2013 to 68.9 in 2014, and then decreased to 5.2 in 2017, a historic low (Table 1). The predominantly detected circulating measles virus genotypes were H1 in China, B3 in the Philippines, and both D8 and D9 in Malaysia and Vietnam.

Regional Verification of Measles Elimination

After the request of the Western Pacific Regional Committee (5) for WHO to establish a formal mechanism for verification of elimination through the Regional Verification Commission, verification guidelines were finalized in April 2013 and revised in 2016 to include verification of rubella elimination. As of the September 2017 Regional Verification Commission meeting, a total of eight (47%) WPR countries and areas (Australia, Brunei, Cambodia, Hong Kong [China], Japan, Macao [China], New Zealand, and South Korea) have been verified as having achieved elimination of measles (6). After a nationwide outbreak in Mongolia during 2015–2016 that lasted longer than 12 months, the Regional Verification Commission determined that endemic measles virus transmission had been reestablished in Mongolia (7).

Discussion

The 2013–2016 measles resurgence in WPR was attributed to three factors. First, increased measles virus transmission occurred in countries with endemic disease (e.g., China, Malaysia, and the Philippines). Second, large-scale outbreaks occurred after importation of measles into countries with endemic, low-incidence measles. Third, multiple measles importations into countries or areas that had achieved elimination occurred, particularly in Mongolia, where a large outbreak persisted for >12 months and endemic measles virus transmission was reestablished.

Measles incidence in WPR declined to a historic low of 5.2 in 2017 because of achievement of control of the outbreaks in Vietnam (2013–2014) and Mongolia (2015–2016), burnout of the outbreak in the Philippines (2013–2014), and China’s accelerated control of measles after the 2010–2011 outbreak. However, the resurgence during 2013–2016 revealed ongoing and emerging challenges that need to be addressed. These challenges include changing measles epidemiology, with increased measles incidence occurring among adolescents, young adults, and infants too young to be vaccinated as well as heterogeneity of measles epidemiology among subnational areas and specific groups at risk within countries with large populations. In addition, the resurgence revealed systems weaknesses: immunization programs were unable to achieve and maintain high population immunity through routine immunization service delivery, and some national laboratories had insufficient capacity to conduct timely serologic testing during outbreaks. The challenges identified also included inadequately developed and implemented policies and processes for preventing measles resurgence and morbidity after virus introduction to the population, including delayed outbreak investigation, insufficient outbreak response, and nosocomial measles virus transmission. Finally, the resurgence revealed a need for greater involvement of local governments, private sectors, societies, and communities.

To address these challenges and to accelerate measles elimination efforts in WPR, the WHO Regional Office for the Western Pacific prepared a new strategy and plan of action for measles and rubella elimination in the Western Pacific that was endorsed by the 68th meeting of the WHO Regional Committee for the Western Pacific in October 2017 (5). The document details 31 strategies with accompanying activities in the following eight areas: 1) overall planning; 2) immunization services; 3) epidemiologic surveillance; 4) laboratory support; 5) program review and risk assessment; 6) outbreak preparedness and response; 7) partnerships, advocacy, information, education and communication, and social mobilization; and 8) progress monitoring and verification of elimination. The new regional strategy is designed to address specific challenges facing WPR countries and to serve as a resource for development of national plans of action (and subnational plans for countries with large populations), tailored to country-specific opportunities for achieving and maintaining measles elimination.

Collective efforts among WPR countries are important for achieving regional measles elimination. Working together to follow the recommended strategies and actions in the Regional Strategy and Plan of Action for Measles and Rubella Elimination could help WPR countries in their efforts to strengthen immunization programs to achieve and sustain high population immunity, maintain high-quality surveillance for rapid case detection and confirmation, and ensure outbreak preparedness and prompt response to contain outbreaks.

Conflict of Interest

No conflicts of interest were reported.

Corresponding author: Jennifer L. Kriss, jkriss@cdc.gov, 404-718-5099.


1Western Pacific Regional Office, Expanded Programme on Immunization, World Health Organization, Manila, Philippines; 2Global Immunization Division, Center for Global Health, CDC; 3Department of Immunization, Vaccines, and Biologicals, World Health Organization, Geneva, Switzerland.


* The Western Pacific Region, one of the six regions of the World Health Organization, consists of 37 countries and areas with a population of approximately 1.8 billion, including American Samoa (USA), Australia, Brunei, Cambodia, China, Commonwealth of the Northern Mariana Islands, Cook Islands, Federated States of Micronesia, Fiji, French Polynesia (France), Guam (USA), Hong Kong (China), Japan, Kiribati, Laos, Macao (China), Malaysia, Marshall Islands, Mongolia, Nauru, New Caledonia (France), New Zealand, Niue, Palau, Papua New Guinea, Philippines, Pitcairn Islands (UK), Samoa, Singapore, Solomon Islands, South Korea, Tokelau (New Zealand), Tonga, Tuvalu, Vanuatu, Vietnam, and Wallis and Futuna (France).

Measles elimination is defined as the absence of endemic measles virus transmission in a defined geographical area (e.g., region or country) for ≥12 months in the presence of a well-performing surveillance system.

§ The Pitcairn Islands, with a population of approximately 50 persons, does not report immunization coverage data to WHO/UNICEF.

SIAs are generally carried out using two target age ranges. An initial, nationwide catch-up SIA targets children aged 9 months–14 years, with the goal of eliminating susceptibility to measles in the general population. Periodic follow-up SIAs then target children born since the last SIA. Follow-up SIAs are generally conducted nationwide every 2–4 years and generally 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 epidemiologic block of countries and areas of the Pacific Islands includes American Samoa, Commonwealth of the Northern Mariana Islands, Cook Islands, Federated States of Micronesia, Fiji, French Polynesia, Guam, Kiribati, the Marshall Islands, Nauru, New Caledonia, Niue, Palau, Pitcairn Islands, Samoa, Solomon Islands, Tokelau, Tonga, Tuvalu, Vanuatu, and Wallis and Futuna.

†† Cases that meet the WHO clinical case definition for measles for which no adequate specimen was collected and cannot be epidemiologically linked to a laboratory-confirmed case of measles. Before 2013, in WPR these cases were classified as “clinically confirmed.” Beginning in 2013, this classification was renamed “clinically compatible” and cases were only classified “confirmed” if they were laboratory-confirmed or epidemiologically linked. The change in terms reflects the recognition in WPR that clinically compatible cases represent a weakness in surveillance.

§§ Essential data elements include name or identifier, date of birth or age, sex, place of residence, vaccination status or date of last vaccination, date of rash onset, date of notification, date of investigation, date of specimen collection, and place of infection or travel history.

¶¶ Percentages were calculated using a denominator of 17 (16 countries or areas, plus the epidemiologic block of the Pacific Islands countries and areas).

References

  1. World Health Organization, Regional Committee for the Western Pacific. Resolution WPR/RC56.R8: measles elimination, hepatitis B control and poliomyelitis eradication. Manila, Philippines: World Health Organization, Regional Committee for the Western Pacific; 2005. http://www2.wpro.who.int/rcm/en/archives/rc56/rc_resolutions/wpr_rc56_r08.htm
  2. World Health Organization, Regional Office for the Western Pacific. Western Pacific regional plan of action for measles elimination. Manila, Philippines: World Health Organization, Regional Office for the Western Pacific; 2003. http://iris.wpro.who.int/handle/10665.1/6011
  3. World Health Organization, Regional Office for the Western Pacific. Field guidelines for measles elimination. Manila, Philippines: World Health Organization, Regional Office for the Western Pacific; 2004. http://www.wpro.who.int/publications/docs/FieldGuidelines_for_MeaslesElimination_0F24.pdf
  4. CDC. Progress toward measles elimination—Western Pacific Region, 2009–2012. MMWR Morb Mortal Wkly Rep 2013;62:443–7. PubMed
  5. World Health Organization, Regional Committee for the Western Pacific. Resolution WPR/RC68.R1: measles and rubella elimination. Brisbane, Australia: World Health Organization, Regional Committee for the Western Pacific; 2017. http://www.wpro.who.int/about/regional_committee/68/resolutions/wpr_rc68_r1_measles_and_rubella_elimination.pdf
  6. World Health Organization, Regional Office for the Western Pacific. Meeting report of the sixth annual meeting of the Regional Verification Commission for measles elimination in the Western Pacific. Beijing, China: World Health Organization, Regional Office for the Western Pacific; 2017. http://iris.wpro.who.int/bitstream/handle/10665.1/13936/RS-2017-GE-49-CHN-eng.pdf
  7. Hagan JE, Takashima Y, Sarankhuu A, et al. Risk factors for measles virus infection among adults during a large outbreak in postelimination era in Mongolia, 2015. J Infect Dis 2017;216:1187–95. CrossRef PubMed
TABLE 1. Measles-containing vaccine (MCV) schedule, estimated coverage with the first and second dose of MCV,* number of confirmed measles cases, and confirmed measles incidence, by country/area — World Health Organization Western Pacific Region, 2013, 2016, and 2017Return to your place in the text
Country/Area MCV schedule§ 2013 2016 2017
Coverage (%) No. of measles cases Incidence per million population Coverage (%) No. of measles cases Incidence per million population No. of measles cases Incidence per million population
Age when 1st dose given Age when 2nd dose given MCV1 MCV2 MCV1 MCV2
American Samoa** 12 mos 4 yrs NR†† NR†† 0 0 NR†† NR†† 0 0.0 0 0.0
Australia 12 mos 18 mos 94 92 154 6.7 95 94 99 4.1 81 3.3
Brunei 12 mos 18 mos 96 92 0 0.0 98 97 1 2.4 0 0.0
Cambodia 9 mos 18 mos 76 49 0 0.0 81 58 56 3.6 10 0.6
China 8 mos 18 mos–24 mos 99 99 27,825 20.1 99 99 24,839 17.7 5,993 4.3
CNMI** 12 mos 4 yrs 68§§ 65§§ 0 0.0 62 72 0 0.0 0 0.0
Cook Islands 15 mos 4 yrs 97 95 0 0.0 90 90 0 0.0 0 0.0
Fiji 12 mos 6 yrs 94 94 0 0.0 94 94 5 5.6 1 1.1
French Polynesia** 12 mos 18 mos 99§§ 98§§ 0 0.0 99§§ 98§§ 0 0.0 0 0.0
Guam** 12 mos 4 yrs–6 yrs 51§§ 44§§ 0 0.0 92 NR†† 0 0.0 0 0.0
Hong Kong (China)** 12 mos 6 yrs 95 95 38 5.3 95 95 9 1.2 4 0.5
Japan 12 mos 5 yrs 95 93 207 1.6 96 93 157 1.2 187 1.5
Kiribati 12 mos 6 yrs 91 84 0 0.0 80 79 0 0.0 0 0.0
Laos¶¶ 9 mos 12 mos 82 NA*** 68 10.5 76 NA*** 8 1.2 3 0.4
Macao (China)** 12 mos 18 mos 99 96 3 5.2 94 92 0 0.0 2 3.2
Malaysia 12 mos 7 yrs 95 99 182 6.1 96 99 1,587 50.9 1,648 52.1
Marshall Islands 12 mos 13 mos 79 56 0 0.0 75 49 0 0.0 0 0.0
Micronesia 12 mos 13 mos 91 75 0 0.0 70 74 0 0.0 0 0.0
Mongolia 9 mos 2 yrs 97 97 0 0.0 98 90 28,813 9,517.4 9 2.9
Nauru 12 mos 15 mos 97 88 0 0.0 98 96 0 0.0 0 0.0
New Caledonia** 12 mos 16 mos 96 86 0 0.0 96 86 0 0.0 0 0.0
New Zealand 15 mos 4 yrs 92 86 25 5.5 92 89 104 22.3 15 3.2
Niue 15 mos 4 yrs 99 99 0 0.0 99 99 0 0.0 0 0.0
Palau 12 mos 15 mos 99 98 0 0.0 96 95 0 0.0 0 0.0
Papua New Guinea 9 mos††† 18 mos 89 NR†† 9 1.2 70 NR†† 0 0.0 7 0.8
Philippines 9 mos 12 mos–15 mos 87 54 5,798 58.9 80 66 641 6.2 1,224 11.7
Samoa 12 mos 15 mos 90 72 0 0.0 68 44 0 0.0 0 0.0
Singapore 12 mos 15 mos–18 mos 95 90 66 12.3 95 88 157 27.9 80 14.0
Solomon Islands 12 mos NA*** 93 NA*** 0 0.0 99 NA*** 1 1.7 0 0.0
South Korea 12 mos–15 mos 4 yrs–6 yrs 99 95 107 2.1 98 97 18 0.4 7 0.1
Tokelau** 12 mos 15 mos 100 100 0 0.0 100§§ 100§§ 0 0.0 0 0.0
Tonga 12 mos 18 mos 86 86 0 0.0 84 85 0 0.0 0 0.0
Tuvalu 12 mos 18 mos 96 84 0 0.0 96 92 0 0.0 0 0.0
Vanuatu 12 mos NA*** 53 NA*** 0 0.0 53 NA*** 0 0.0 0 0.0
Vietnam 9 mos 18 mos 98 86 1,232 13.5 99 95 368 3.9 667 7.0
Wallis and Futuna** 12 mos 18 mos >100§§ >100§§ 0 0.0 79§§ 80§§ 0 0.0 0 0.0
Western Pacific Region 97 91 35,700 19.2 96 93 56,836 30.1 9,938 5.2

Abbreviations: CNMI = Commonwealth of the Northern Mariana Islands; MCV1 = first dose of MCV; MCV2 = second dose of MCV; WHO = World Health Organization.
* WHO-United Nations Children’s Fund (UNICEF) estimates.
Includes confirmed cases by laboratory or epidemiologic linkage and clinically compatible cases meeting the WHO clinical case definition of measles for which no adequate specimen was collected and that cannot be epidemiologically linked to a laboratory-confirmed case of measles.
§ MCV schedule is the 2017 schedule.
2017 MCV1 and MCV2 coverage estimates not available.
** Country or area reported coverage for MCV1 and MCV2 based on administrative data.
†† NR = not reported (country did not report coverage in the year specified).
§§ No data available for assessment year; data from previous year is reported instead.
¶¶ Laos introduced MCV2 in 2017.
*** NA = not applicable (dose was not included in the vaccination schedule for that year).
††† Additional 6-month dose provided nationally.

TABLE 2. Characteristics of measles supplementary immunization activities (SIAs),* by year and country/area — World Health Organization Western Pacific Region, 2013–2017Return to your place in the text
Year Country/Area Age group targeted Vaccine used Extent of SIA No. (%) of population reached in targeted age group
2013 Cambodia 9 mos–14 yrs MR National           4,576,633 (>100)
Federated States of Micronesia 12 mos–47 mos MMR Subnational           3,435 (95)
Philippines 6 mos–59 mos M National           1,937,471 (ND)
Singapore 6 yrs–7 yrs MMR National           38,436 (95)
Vanuatu 12 mos–59 mos MMR National           33,604 (>100)
Vietnam 1 yr–15 yrs M Subnational           163,870 (94)
2014 Federated States of Micronesia 6 mos–57 yrs MMR National           71,388 (87)
Laos 9 mos–9 yrs MR National           1,569,613 (100)
Malaysia 6 mos–17 yrs M Subnational           54,656 (63)
Philippines 9 mos–59 mos MR National           10,402,489 (91)
Philippines 6 mos–36 mos M Subnational           1,695,930 (78)
Vietnam 9 mos–24 mos M National           875,386 (94)
2015 Malaysia 9 mos–17 yrs MMR Subnational           21,518 (90)
Mongolia 9 mos–17 yrs M National           347,685 (94)
Papua New Guinea 9 mos–14 yrs MR National           801,436 (62)
Vanuatu 6 mos–59 mos M Subnational           24,336 (98)
Vanuatu 1 yr–15 yrs MR National           103,676 (>100)
Vietnam 1 yr–14 yrs MR National           19,740,181 (98)
2016 Cambodia 9 mos–59 mos MR National           766,743 (91)
Malaysia 1 yr–17 yrs MR Subnational           139,954 (85)
Mongolia 18 yrs–30 yrs MR National           549,846 (88)
Papua New Guinea 9 mos–15 yrs MR Subnational           436,854 (63)
Vietnam 16 yrs–17 yrs MR National           1,787,588 (95)
2017 Cambodia 6 mos–59 mos MR National           1,452,821 (75)
Fiji 12 mos–11yrs MR National           ND
Laos 9 mos–4 yrs MR National           ND
Papua New Guinea 6 mos–45 yrs MR Subnational           ND
2013–2017 Western Pacific Region           47,595,549 (93§)

Abbreviations: M = monovalent measles vaccine; MMR = measles, mumps, and rubella vaccine; MR = measles and rubella vaccine; ND = no data.
* SIAs generally are carried out using two approaches. An initial, nationwide catch-up SIA targets all children aged 9 months–14 years; it has the goal of eliminating susceptibility to measles in the general population. Periodic follow-up SIAs then target all children born since the last SIA. Follow-up SIAs generally are conducted nationwide every 2–4 years and generally 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 measles-containing vaccine through routine services, and the time since the last SIA.
Targeted age groups varied by province.
§ Average SIA coverage, weighted by size of target population.

Return to your place in the textFIGURE. Confirmed measles cases,* by month of rash onset — World Health Organization Western Pacific Region, 2013–2017
The figure above is a histogram showing confirmed measles cases, by month of rash onset, in the World Health Organization Western Pacific Region during 2013–2017.

* Confirmed and clinically compatible measles cases reported by countries and areas to the World Health Organization (WHO). A case of measles was laboratory-confirmed when measles-specific immunoglobulin M antibody was detected in serum, measles-specific RNA was detected by polymerase chain reaction, or measles virus was isolated in cell culture from a person who was not vaccinated during the 30 days before rash onset. A case of measles was confirmed by epidemiologic linkage when linked in time and place to a laboratory-confirmed measles case without serologic confirmation. During 2013–2017, a case of measles meeting the WHO clinical case definition but without a specimen collected could be reported as clinically compatible.


Suggested citation for this article: Hagan JE, Kriss JL, Takashima Y, et al. Progress Toward Measles Elimination — Western Pacific Region, 2013–2017. MMWR Morb Mortal Wkly Rep 2018;67:491–495. DOI: http://dx.doi.org/10.15585/mmwr.mm6717a3.

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