Achieving and sustaining measles elimination in Hong Kong, from 1967 to 2024: lessons to be learnt

Abstract

Following the development and roll-out of the measles vaccine in 1954, measles incidence dropped to low levels in areas where measles vaccines with high coverage were introduced. The Measles and Rubella Strategic Framework 2021–2030 developed by the Measles & Rubella Initiative aims to eliminate measles globally by 2030. However, there has been a resurgence of measles cases after the COVID-19 pandemic in many countries, including some in the Western Pacific Region. This review describes the journey from 1967, when Hong Kong introduced a single-dose regimen, to 2024 when Hong Kong had been experiencing an increase in imported measles cases despite being verified to have achieved measles elimination in 2016. Hong Kong’s experience in maintaining high vaccination coverage and comprehensive surveillance may provide an exemplary framework for other countries in the Western Pacific Region.

SUMMARY BOX.

• Measles, a highly contagious disease, re-emerges after COVID-19. Although effective measures, including catch-up vaccinations, measles outbreaks still occur regularly around the globe. This requires immediate attention.

• Hong Kong has implemented different measures to achieve and sustain measles elimination, such as high coverage of two-dose measles-containing vaccine, catch-up campaigns, supplementary immunisation activities, comprehensive surveillance system and outbreak preparation. Such measures could act as guidance for other countries.

• Different challenges are faced worldwide, such as inadequate two-dose measles-containing vaccine coverage, waning immunity due to secondary vaccine failure and lack of effective surveillance systems. Tailor-made solutions should be proposed to each area or country so that the challenges can be tackled effectively.

Introduction

Measles, a highly contagious airborne infection, was estimated to have infected over 10 million individuals in 2023 alone, which led to over 100 000 deaths. The number of infections likely will be higher in 2024 and 2025 due to the full relaxation of COVID-19 social-distancing measures and burgeoning international travel.¹ With the enormous burden of measles, the Measles & Rubella Initiative set a goal to achieve and sustain measles elimination globally by 2030.² Currently, the Regional Verification Commissions (RVC) verify measles elimination in any given country, area or region when endemic transmission has been interrupted for at least 12 months in a well-performing surveillance system.³ In the Western Pacific Region (WPR), eight countries and areas were verified to have sustained measles elimination by 2022. The elimination status and recommendations from the RVC for measles elimination for all countries and areas in WPR are summarised in online supplemental table 1.⁴

Measles eradication has been considered biologically feasible since the development of the measles vaccine in the 1950s.⁵ The measles vaccine has been included in the Essential Programme on Immunization (later renamed the Expanded Programme on Immunization) since 1974.⁶ According to the WHO, vaccination of at least 95% of the community with two doses is needed to achieve herd immunity.⁷ However, only 36 out of 204 countries achieved this standard in 2019. Areas with lower sociodemographic indexes had lower vaccine coverage.⁸ Nevertheless, susceptible individuals exist in countries with high vaccine coverage due to waning protection provided by vaccines, leading to secondary vaccine failure. For highly vaccinated populations, susceptible individuals are usually young adults with no previous exposure to wild-type viral infection.⁹

Hong Kong was verified as having achieved measles elimination in 2016.¹⁰ To achieve elimination, important changes were made which were closely related to the local epidemiology of measles. This review describes these changes and the underlying rationale, as possibly these strategies can assist other countries to achieve and sustain measles elimination in the WPR.

Data sources

Data regarding the numbers of measles cases, incidence rates, and mortality rates in Hong Kong were provided by the Centre for Health Protection (CHP), Hong Kong. Data on the measles cases in other countries and areas in the WPR were retrieved from The Global Health Observatory, WHO.¹¹ Yearly population data for countries were extracted from the World Bank Group.¹² WHO/UNICEF Joint Estimates of National Immunization Coverage were used for measles vaccination coverage data.¹³

Introduction of measles vaccination in Hong Kong (1967)

Before the introduction of measles-containing vaccine (MCV) in 1967, the number of cases in Hong Kong was high (figure 1A, online supplemental table 2), and the case fatality rates were 4%–25% from 1961 to 1967.¹⁴ In the Western Hemisphere, Enders and his colleagues extracted measles viruses from a boy named David Edmonston in Boston, USA, in 1954 to develop the measles vaccine, which was approved for use in 1963.¹⁵ At the time, the vaccine safety, effectiveness and the need to be included in the vaccination programme were debated.¹⁶ Given such knowledge gaps, the Medical Research Council in the UK initiated a study in 1964 that confirmed a single dose of live-attenuated measles vaccine was safe and immunogenic.^{17 18}

Figure 1. Number of measles cases and incidence rate in Hong Kong. (A) 1961–2000. The introduction of the measles-containing vaccine in 1967 led to a significant decrease in the number of measles cases. However, the single-dose regimen was insufficient to provide herd immunity, which resulted in fluctuation of measles cases in subsequent years. A massive measles outbreak thus occurred in 1988. In view of the uncontrolled measles situation, the two-dose regimen was implemented in 1996. (B) 2001–2024. In 2003, the SARS epidemic caused a reduction in the number of cases, but the number increased after the epidemic ended. A similar pattern was found for the COVID-19 pandemic. Data in 2024 included January to November only. Blue lines and dots represent the number of cases, while green lines and dots represent the incidence rate in the corresponding year. The incidence rate is expressed as cases per 1 000 000 individuals. MCV1, first dose measles-containing vaccine; MCV2, second dose measles-containing vaccine; SARS, severe acute respiratory syndrome.

Taking into account the measles disease burden and the effectiveness of MCV, Hong Kong decided to introduce a single-dose regimen in December 1967. Measles vaccination was voluntary, with an initial target age of ≥6 months. The target age was later raised to 9 months and then 12 months in 1971 and 1979, respectively. The vaccine coverage rates increased from <70% before 1976 to 70%–80% between 1976 and 1984.¹⁴ There was a 75% reduction in measles cases immediately 1 year after the introduction of vaccination (figure 1A). Simultaneously, the mortality rate reduced to 12 from 176 deaths per million and remained below 10 deaths per million, except in 1974 (12 deaths per million) (table 1). Such improvement in the measles situation boosted confidence in measles vaccination, increasing MCV coverage in Hong Kong.

Table 1. Number of deaths due to measles and mortality rate in Hong Kong from 1951 to 2024.

Year	Number of deaths	Mortality rate	Year	Number of deaths	Mortality rate	Year	Number of deaths	Mortality rate	Year	Number of deaths	Mortality rate
1951	39	19.35	1971	4	0.99	1991	0	0	2011	0	0
1952	77	36.22	1972	9	2.18	1992	0	0	2012	0	0
1953	50	22.3	1973	21	4.95	1993	0	0	2013	0	0
1954	126	53.28	1974	53	12.11	1994	0	0	2014	0	0
1955	88	35.34	1975	2	0.45	1995	0	0	2015	0	0
1956	86	32.89	1976	10	2.21	1996	0	0	2016	0	0
1957	93	33.99	1977	12	2.62	1997	0	0	2017	0	0
1958	191	66.92	1978	1	0.21	1998	0	0	2018	0	0
1959	176	59.31	1979	32	6.49	1999	0	0	2019	0	0
1960	192	62.43	1980	5	0.99	2000	0	0	2020	0	0
1961	435	137.31	1981	0	0	2001	0	0	2021	0	0
1962	326	98.63	1982	5	0.95	2002	0	0	2022	0	0
1963	405	118.39	1983	2	0.37	2003	0	0	2023	0	0
1964	73	20.83	1984	2	0.37	2004	0	0	2024	0*	0*
1965	217	60.31	1985	1	0.18	2005	0	0
1966	384	105.79	1986	0	0	2006	0	0
1967	654	175.67	1987	1	0.18	2007	0	0
1968	46	12.1	1988	8	1.42	2008	0	0
1969	21	5.43	1989	1	0.18	2009	0	0
1970	13	3.28	1990	0	0	2010	0	0

The mortality rates are presented as cases per 1 000 000 individuals.

^*Data in 2024 included January to November only.

First massive outbreak after the introduction of measles vaccination (1988)

Despite a significant reduction in measles cases after 1968, the case numbers fluctuated (online supplemental table 2). Since vaccination led to less measles transmission in the community, unvaccinated individuals had lower chances of encountering measles viruses and acquiring natural immunity.¹⁹ Thus, a susceptible pool was formed, and Hong Kong experienced a large measles outbreak in 1988, with over 3000 individuals infected. Among these infected individuals, only 20% had been vaccinated, which consisted of one dose of MCV at the time.¹⁴ Despite the high case numbers in 1988, the mortality rate was low, with only 1.4 deaths per million, compared with 654 per million in 1967, just before the MCV was introduced (table 1). This was likely due to a combination of improved nutrition, better access to healthcare and the effectiveness of a single dose of MCV in preventing severe measles disease and complications.

Furthermore, there was a shift in the age distribution of measles cases. Fewer measles cases among the age group 1–4 years and a greater proportion of cases in children <1 year of age and people over 4 years of age were observed compared with the period before the introduction of measles vaccination.¹⁴ This phenomenon was reported in other countries as well.²⁰ The shift in the age distribution showed that children with single-dose vaccination were well protected for a few years until waning of protection, indicating vaccine failure. In the USA, of the 101 outbreaks among school-aged children that occurred in 1985–1986, 60% were vaccinated.²¹ Evidently, a single dose of MCV did not provide sufficiently durable protection for all recipients.

Mass measles immunisation campaign (1997)

The outbreak in 1988 put measles back into the spotlight. Annual serological surveys conducted between 1990 and 1996 showed increased samples tested negative for measles antibodies among individuals aged 1–19 years.²² This increase prompted a discussion about the need for a two-dose MCV regimen. Sweden had already implemented this two-dose approach as the primary series, which resulted in a significant drop in the incidence of measles.²³ Under such a premise, Hong Kong added a second dose in 1996, which would be administered to children at 12 years of age. After the rollout of this regimen, the second dose coverage reached 99%.

Due to concerns of a large measles outbreak based on the serological data, the Advisory Committee on Immunisation in Hong Kong recommended a mass measles immunisation campaign in June 1997 to increase the two-dose coverage among children aged 1–19. Under this campaign, 1 100 464 individuals received the MCV from July to November 1997, which was 77% of the target population. The campaign was epidemiologically successful, as evident by a marked reduction in the monthly notification rate in August 1997.²² Between 1998 and 2000, the annual measles incidence rate remained low (<10 per 1 million) (table 1).

Severe acute respiratory syndrome epidemic (2003)

Severe acute respiratory syndrome (SARS) emerged in 2003, resulting in >8000 infections. Its impact on Hong Kong was enormous, as over 1700 citizens were infected, with nearly 300 deaths. During the SARS epidemic, control measures were implemented to prevent transmission, including cessation of school attendance, temperature monitoring of international travellers and district-wide cleansing.²⁴ Indeed, these measures prevented the transmission of SARS but also impacted the transmission of measles, as the incidence rate was reduced by half in 2003 compared with 2002. After the SARS epidemic ended and normal social activities resumed, the measles incidence rate surged, with a 50% increase in 2004. This rising trend continued until 2006, reaching 15.5 cases/million (figure 1B, online supplemental table 2). A surge in the incidences of measles also occurred during the relaxation of public health measures after COVID-19, which will be discussed later.

Hong Kong international airport outbreak (2019)

After 2004, the measles incidence rate remained low with individual imported cases, and the Western Pacific RVC concluded that Hong Kong had achieved the absence of endemic measles transmission≥12 months in the presence of a well-performing surveillance system. Hong Kong was thus verified to have achieved measles elimination in 2016 after reviewing against the five lines of evidence in the global framework.^{10 25} With the global resurgence of measles in 2019, there was a measles outbreak at the Hong Kong International Airport the same year. Thirty-three cases were identified during this outbreak, including 29 airport workers, two healthcare workers, one airport visitor and one traveller. Two-thirds were aged 20–29 years old, of which 12 had records of receiving two doses of MCV.²⁶ Two healthcare workers tested positive for measles immunoglobulin G level in the past, indicating the infection was due to secondary vaccine failure.²⁷

Outbreak responses were implemented after CHP was notified of the first three measles cases. At the airport, ventilation was improved, alcohol-based hand-sanitising dispensers were installed, and reminders on meticulous maintenance of personal hygiene were promulgated to the public. MCV boosters were provided to airport workers without a documented history of measles vaccination. Between 22 March and 17 May 2019, over 8000 airport workers received MCV, and the outbreak was effectively controlled.²⁶ This incident raised awareness among healthcare workers and the public that measles infections within this locality can recur and cause outbreaks even after achieving endemic measles elimination.

The COVID-19 pandemic (2020 and after)

CHP received notification about the first SARS-CoV-2 infection in Hong Kong on 23 January 2020. The government responded by activating the ‘Emergency Response Level’ in public hospitals, setting up quarantine centres, suspending schools, restricting international travel and implementing other public health control measures.²⁸ These measures not only disrupted the transmission of SARS-CoV-2 but also measles. The incidence rate decreased from 12.2 to 0.1/million individuals (figure 1B, online supplemental table 2).

The number of measles cases in Hong Kong remained low until the lifting of travel and social restrictions at the end of 2022, when there was an increasing number of imported cases. Globally, around 40 million children missed their MCV in 2021 alone, and 25 million children did not receive even the first dose. This created immunity gaps, which were associated with 9 million measles cases and 128 000 deaths in 2021 alone.²⁹ A modelling study showed that over 40 000 additional deaths were caused by the disruption of immunisation programmes. Most of the additional deaths were in the African region.³⁰ Vaccination programmes were disrupted not only because of social restrictions but also because of increased vaccine hesitancy in some communities. During the COVID-19 pandemic, misleading information about COVID-19 vaccines spread rapidly through social media. Rumours regarding the safety and effectiveness of COVID-19 vaccines fuelled vaccine hesitancy, disturbing the trust between the public and health officials.³¹ This augmented the ongoing MCV hesitancy caused by the historical misconception that MCV was linked to the development of autism, which is still pervasive in certain communities.³²

Lessons from Hong Kong

The most important success factor contributing to the achievement and maintenance of the elimination of measles in Hong Kong is the consistently high two-dose MCV coverage. This has been enabled by free and accessible vaccine delivery through a network of Maternal and Child Health Centres (MCHC), which is available in every district in Hong Kong, including offshore islands. MCVs are provided to children aged 12 and 18 months under the Hong Kong Childhood Immunisation Programme at every MCHC.³³ Due to the high acceptance rates of MCV, Hong Kong maintained higher than 95% two-dose MCV coverage in the past decade (except in 2020 due to the COVID-19 pandemic) (figure 2A).¹³

Figure 2. Two-dose measles-containing vaccine coverage in the Western Pacific. (A) Coverage of the second dose of measles-containing vaccine in Hong Kong and six countries that had verified measles elimination. Most areas/countries achieved high vaccine coverages. (B) Coverage of the second dose of measles-containing vaccine in eight countries with endemic measles transmission. Most countries had suboptimal vaccine coverages. The dotted line represents the WHO’s recommendation of two doses of measles-containing vaccine coverage (95%). MCV2, the second dose of measles-containing vaccine.

The second factor is the effective surveillance system of measles cases, followed by prompt investigation and effective control of outbreaks. The surveillance system entails numerous components including case-based statutory notifications, acute fever and rash syndromic surveillance, laboratory surveillance (serology, PCR and genotyping) and reporting of suspected outbreaks. Responsive laboratory capacity in the public and private sectors should be maintained to ensure sensitive surveillance. CHP promptly investigates any suspected measles cases, implements control measures and conducts regular exercises for improvement and assessment of responses to imported measles cases. These exercises involve multiple relevant parties, including the airport authority, hospital authority and social welfare department. These simulations can measure the effectiveness in managing measles cases and further strengthen collaboration between the different authorities.³⁴ Such drills should be held regularly to maintain outbreak preparedness.

The third factor is the close surveillance of population immunity against measles using regular serosurveys, followed by timely supplementary immunisation activities (SIA) and catch-up campaigns, if required. Since 2001, CHP has been monitoring the seroprevalence among the community by convenience sampling and testing of blood specimens sent for other clinical indications.³⁵ This could identify potential immunity gaps in the community and initiate SIA. The catch-up campaigns held in 1997 and SIA in 2019 demonstrate the importance of responding to close immunity gaps identified through ongoing monitoring to achieve and sustain measles elimination.

Challenges to achieving worldwide measles elimination and the remedies

Although measles eradication is feasible, there have been challenges to achieve the goal.^{5 36} The biggest challenge is the suboptimal MCV coverage in endemic countries (figure 2).⁴ These areas are mostly in low- or middle-income countries (LMICs) with limited healthcare resources. Additionally, socioeconomic factors, vaccine hesitancy and political stability are crucial factors influencing immunisation coverage.^{37 38} Some organisations, such as Gavi, WHO and the United Nations International Children’s Emergency Fund, are supporting LMICs financially to increase MCV coverage.

Catch-up campaigns are important for closing the immunity gaps. Due to COVID-19, nearly 40 million children missed their measles doses.²⁹ It was estimated that over 15 000 deaths due to measles could be averted between 2020 and 2030 with catch-up immunisation activities.³⁰ These campaigns have been conducted in several countries, notably Mongolia, Vietnam and the Philippines, resulting in significant impact. With such efforts made to raise immunisation coverage, Mongolia is planning to be reverified to have achieved measles elimination in 2025.³⁹

In addition, changing the delivery mode of MCV could potentially boost vaccine coverage. The current major vaccine delivery method is intramuscular injection with needles and syringes, which can be difficult to access in remote and less-resourced regions due to high costs and risk of needlestick injuries. Cold-chain transportation is challenging in many LMICs due to technical difficulties.40,42 On the other hand, microarray patches (MAP) are proven safe and immunogenic, with thermostability that does not require cold-chain technology, and self-administration is possible.^{40 43} For cost-effectiveness, MAP is believed to be a prime candidate to boost vaccination coverage in LMICs.⁴⁴ However, without large-scale investment, MAP will not be available until 2033.⁴⁵

Another challenge is the contribution of waning immunity due to secondary vaccine failure in post-elimination communities. As measles in post-elimination communities becomes rare, most individuals acquire immunity through vaccines. While natural immunity is life-long, vaccine-induced immunity wanes over time.¹⁹ We recently showed that 10% of young adults aged 26–30 years had suboptimal antibody levels in Hong Kong.⁴⁶ A study from Japan found that the measles seroprevalence rate was low among adolescents (69.3% in 10–14 years old; 82.2% in 15–19 years old).⁴⁷ A study from Taiwan demonstrated adolescents had lower seroprevalence rates than the elderly (65.9% vs 89.4%).⁴⁸

If a certain proportion of individuals have inadequate antibody levels, the community can be prone to re-establishment of endemic measles transmission even after being verified to have achieved elimination.⁴⁹ Mongolia was verified to have eliminated measles in 2014, but a nationwide outbreak that occurred in 2015 resulted in its loss of elimination status. An investigation concluded that secondary vaccine failure was an important factor in the outbreak. Whether this was due to substandard vaccine manufacturing, compromised cold-chain maintenance or other reasons remains unclear. In Mongolia, vaccine effectiveness (VE) among children under 15 years of age was high, at 93%–95%. However, VE was only 75%–83% among young adults aged 15–29 years, which is conceptually insufficient for herd immunity, and this was likely the cause of the re-established endemic transmission.⁵⁰

SIAs, whether nationwide or targeted at high-risk populations, have an important role in preventing outbreaks and sustaining measles elimination. Our recent study showed that all individuals with low measles antibody levels achieved high levels 1 month after an MCV booster.⁴⁶ Similarly, a Korean study demonstrated that healthcare workers achieved higher seroprevalence rates after a third dose compared with the second dose (89.5% vs 75.4%).⁵¹ Furthermore, 77.8% of 82 seronegative young adults in Italy who had received two previous doses of MCV seroconverted after receiving a booster dose.⁵²

Targeted SIAs often include high-risk populations, such as refugees, healthcare workers and airport personnel. A New Zealand study revealed that less than one-third of refugees were age-appropriately vaccinated.⁵³ A recent review showed migrants and refugees experienced higher vaccine-preventable disease burdens due to lower immunisation rates.⁵⁴ As the Gaza-Israel conflict and the Russo-Ukrainian War continue, more refugees will be expected. It is a top priority to ensure these refugees receive appropriate protection to prevent imported cases and outbreaks.

Due to the scale of the international travel industry, there is an increased risk of imported measles cases. Individuals without adequate immunity to measles would bring the measles virus back to their home countries, which may lead to large local outbreaks.⁵⁵ In 2016, a measles outbreak occurred at Kansai International Airport, leading to 30 infected cases among airport personnel.⁵⁶ Frequent importations pose a risk of re-establishing endemic measles transmission in countries with immunity gaps, like Cambodia.⁴⁹ Cambodia shares borders with Thailand, the Lao People’s Democratic Republic and Vietnam, all of which had endemic transmission, resulting in numerous imported measles cases. Eventually, endemic transmission was reestablished in Cambodia (online supplemental figure 1 and table 3).⁵⁷

Finally, effective surveillance systems are required. Such a surveillance system for measles should allow rapid case detection, detailed data analysis and outbreak control.⁵⁸ Hong Kong’s experience in maintaining a multifaceted and sensitive surveillance system could serve as an example for some countries in the WPR. The annual measles serosurvey provides valuable data for experts to evaluate the risk of outbreaks and the need for SIAs. WHO recommended strengthening outbreak preparation and response.² This requires identifying the root causes of the outbreaks, improving structures and processes of outbreak control and strengthening cross-border collaborations.

Conclusions

Measles vaccination has had a huge impact on reducing global morbidity and mortality in the past five decades. It is now important that all countries progress towards eradication and sustain the elimination of endemic measles transmission. The experience from Hong Kong clearly illustrates that measles elimination requires several components, including high maintenance coverage with two doses of measles vaccination, addressing immunity gaps and establishing high-quality surveillance and outbreak response systems. To achieve measles elimination in the WPR, collaboration between pre-elimination and post-elimination areas would be required. This review provides important guidance towards achieving measles elimination globally.

Data availability statement

Data are available upon reasonable request.