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Conference report

Measles control in Australia – threats, opportunities and future needs


C. Raina MacIntyre a,h, Elizabeth Kpozehouen a,⇑, Mohana Kunasekaran a, Kathleen Harriman c,
Stephen Conaty d, Alexander Rosewell a, Julian Druce e,g, Nicolee Martin e, Anita E. Heywood a,b,
Heather F. Gidding a,b, James Wood a, Sonya Nicholl f
a
School of Public Health and Community Medicine, UNSW Medicine, The University of New South Wales, Sydney, NSW, Australia
b
National Centre for Immunisation Research and Surveillance, Westmead, NSW, Australia
c
California Department of Public Health, Richmond, CA, USA
d
Public Health Unit, South Western Sydney Local Health District, Australia
e
Victorian Infectious Diseases Reference Laboratory, Australia
f
Immunisation Unit, Health Protection NSW, Australia
g
VIDRL, Doherty Institute, Australia
h
Kirby Institute, Biosecurity Program, UNSW Medicine, The University of New South Wales, Sydney, NSW, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Control of measles was the focus of a national workshop held in 2015 in Sydney, Australia, bringing
Received 23 January 2018 together stakeholders in disease control and immunisation to discuss maintaining Australia’s measles
Received in revised form 7 June 2018 elimination status in the context of regional and global measles control.
Accepted 8 June 2018
The global epidemiology of measles was reviewed, including outbreaks in countries that have achieved
Available online xxxx
elimination, such as the Disneyland outbreak in the United States and large outbreaks in Sydney,
Australia. Transmission of measles between Australia and New Zealand occurs, but has not been a focus
Keywords:
of control measures. Risk groups, the genetic and seroepidemiology of measles as well as surveillance,
Measles vaccine
Infectious diseases
modelling and waning vaccine-induced immunity were reviewed. Gaps in policy, research and practice
Measles elimination for maintaining measles elimination status in Australia were identified and recommendations were
Immunisation developed.
Whole of life immunisation register Elimination of measles globally is challenging because of the infectiousness of measles and the need for
Measles 2-dose vaccine coverage rates in excess of 95% in all countries to achieve it. Until this occurs, interna-
tional travel will continue to permit measles importation from endemic countries to countries that have
achieved elimination. When measles cases are imported, failure to diagnose and isolate cases places the
health system at risk of measles outbreaks. Vaccine funding models can result in gaps in vaccine coverage
for adults and migrants. Australia introduced a whole-of-life immunisation register in 2016 and catch-up
vaccination for at-risk communities, which will improve measles control. Research on diagnosis,
immunology, case management and modelling of vaccination strategies are important to ensure contin-
ued control of measles.

1. Introduction elimination of endemic measles in Australia, ongoing outbreaks


continue to occur due to importation from endemic countries.
In 2014, the World Health Organization (WHO) declared Measles has a reproductive number (R0) of 15–20 [3], therefore
measles eliminated in Australia, reflecting the success of the population immunity of 92–95% is necessary to stop measles trans-
National Immunisation Program and a 1998 measles control cam- mission [4].
paign [1]. This campaign included moving the second dose of MMR Measles remains a global problem, particularly in Asia, with tra-
vaccine to 4 years of age, a catch-up campaign, the establishment vel being the major source of importation into Australia. Under-
of a childhood immunisation register and financial incentives for standing the global epidemiology of measles is important for
parents and doctors for vaccinating children [2]. Despite the measles control. Regionally, movement of people between Aus-
tralia and New Zealand, both of which are declared free of endemic
⇑ Corresponding author at: Level 3 Samuels Building, School of Public Health and measles transmission by WHO, contributes to measles outbreaks in
Community Medicine, University of New South Wales, Australia. both countries [5]. The largest migrant group into Australia is peo-
E-mail address: e.kpozehouen@unsw.edu.au (E. Kpozehouen). ple from New Zealand. Short term travel is also high volume

https://doi.org/10.1016/j.vaccine.2018.06.022
0264-410X/

Please cite this article in press as: MacIntyre CR et al. Measles control in Australia – threats, opportunities and future needs. Vaccine (2018), https://doi.org/
10.1016/j.vaccine.2018.06.022
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between the countries [6]. Australia has special mutual migration population displacement, crowding, interruption of health ser-
arrangements whereby citizens from either New Zealand or Aus- vices, reduced access to health care facilities and increased risk
tralia can visit, live and work in either country for indefinite period of outbreaks, including cross-border transmission [17].
of time [7]. Imported and import-related measles cases account for up to
Larger and more prolonged outbreaks in Australia in recent 100% of all cases in regions with interrupted endemic measles
years have heightened the need to close the immunity gaps in transmission [18]. Between 2001 and 2013 as many as 95–100%
young adults, unimmunised children and selected migrant groups. of measles cases reported in the US and Australia were travel
The uncertainty around long-term waning of vaccine-induced related [18–20], and between 2007 and 2011 secondary measles
measles immunity is also of potential concern [8]. transmission was documented in 19% of international flights carry-
Although there was a 79% decline in worldwide measles deaths ing infectious travellers [18,21]. Since 2005, no endemic transmis-
from 2000 to 2015, 134,200 deaths from measles were docu- sion has been observed in Australia, and the South-East Asia Region
mented globally in 2015 [9]. Measles in endemic countries remains and Western Pacific Region were identified as main regions of ori-
a source of importation into countries which have achieved gin for imported cases, most aged between 17 and 34 years [18]. In
elimination. October 2017, the WHO verification committee declared that New
The United States (US) has seen recent large outbreaks of Zealand has successfully eliminated endemic measles for the first
measles, including 145 cases in Disneyland, California in 2014 time, where no local case of measles has originated in New Zealand
[10], and a 2017 outbreak in the state of Minnesota in a Somali between 2014 and 2017. Important locations for measles acquisi-
community, with 71/79 cases being unvaccinated [11]. The num- tion and subsequent importation into Australia are the Philippines,
ber of reported measles cases in the European Region in 2015 Indonesia, Thailand, France and Romania.
was 30,762, almost twice the number of cases reported in 2014
[12]. Two-thirds of the 53 European region countries have elimi- 3. Measles outbreaks in countries with elimination (Australian
nated measles, but measles remains endemic in 14 countries and US case studies)
[13]. A measles outbreak in Romania began in February 2016 with
8803 cases, including 32 deaths, reported as of 18 August 2017 In countries with verified WHO elimination status, measles is
[14]. In addition, as of 17 August 2017, Italy had reported 4193 re-emerging as a serious public health threat and outbreaks are
cases and 3 deaths since June 2016 [13]. occurring despite good public health infrastructure and health lit-
Measles incidence decreased by 63% during 2013–2016 in the eracy. Post-elimination epidemiology illustrates that even in the
WHO African Region. However, the region does not meet targets absence of endemic measles, transmission can still occur with
for vaccination coverage and surveillance [15]. There has been a imported infections and pockets of susceptible individuals.
gradual increase in coverage for both the first and second doses Among countries with elimination status, the US experienced a
of measles-containing vaccine (MCV), MCV1 and MCV2, in the large, multi-state measles outbreak in 2014–2015 with 145 US
South-East Asia Region, but challenges in achieving measles elim- cases linked to Disneyland, California. The outbreak likely started
ination in this region are exacerbated by under-immunisation and from an international traveller, however the index case was not
unregistered birth cohorts in populous countries such as India and identified [19]. In 2014, the US experienced 23 measles outbreaks
Indonesia. In 2015, 3.23 million and 1.52 million children did not with one large outbreak of 383 cases occurring primarily among
receive MCV1 in India and Indonesia respectively [16]. Asia unvaccinated Amish communities in Ohio [22], which was sparked
remains the most important source of imported measles into by two unvaccinated Amish men who were infected in the Philip-
Australia. pines while doing relief work [22]. The measles virus genotype in
Due to the number of large measles outbreaks that have the 2014 and 2015 US outbreaks was B3, identical to the virus type
occurred in the Asia-Pacific region since 2012, and larger and that was circulating in the Philippines at that time, and which
longer than usual measles outbreaks in recent years in Australia, caused large outbreaks there after Typhoon Haiyan hampered vac-
a workshop entitled ‘‘Current challenges in measles control” was cination efforts. In 2017, an outbreak with 79 cases occurred, 71
held in September 2015 at The University of New South Wales. unvaccinated, in a Somali community in Minnesota [23].
The aim of the workshop was to discuss current challenges in the In the post-elimination era, most measles outbreaks in Australia
control of measles globally and issues around measles elimination have been linked to imported cases with international travel
status in Australia. The workshop gathered various national and [1,24,25]. Global travel has increased exponentially, with 18.9 mil-
international experts and stakeholders in policy, surveillance and lion arrivals to Australia, including returning Australian residents,
research. This report summarises the presentations, discussion non-Australian visitors, and permanent and long-term arrivals in
and recommendations from the workshop. 2016 [26].
In 2012, the largest measles outbreak in Australia since 1997
2. Global context and progress in measles control was sparked by a 25-year-old traveller returning from Thailand
[5]. Of 168 outbreak-related cases, 126 (75%) occurred in South-
Since measles is a target for elimination and eventually eradica- Western Sydney where people of Pacific Island descent and New
tion, many challenges have been identified and have hindered pro- Zealand origin were a major risk group and comprised 21% of the
gress toward these goals. Some of the contributing factors to cases [27]. Over 35% of the cases were infants less than one year
ongoing measles transmission are high population density, regions of age who were too young to be vaccinated, followed by almost
with endemic measles, travel and under-vaccination. There has 30% of the cases in adolescents 15–19 years of age [5]. Immunisa-
been intense competition for human and financial resources tion coverage in Western Sydney was high as recorded on the Aus-
between global health initiatives in Africa and Asia, including polio tralian Immunisation Registry (AIR), but persons of Pacific Island
eradication and introduction of other newer vaccines, resulting in descent may be New Zealand citizens who are not registered on
delays in funding for measles supplementary immunization activ- the AIR and low coverage was reported in the 1990s among infants
ities [17]. who had most likely grown into adolescence by 2012 [27].
Countries in Africa and Asia face weaknesses in health care sys- Although there is little research into vaccination practices
tems, which result in low vaccination coverage [15]. Humanitarian among Pacific Island communities in Australia, in New Zealand,
crises resulting from armed conflicts and natural disasters further children from Pacific Island communities are at increased risk of
adversely affect disease control and eradication efforts, and cause incomplete immunisation [25,28]. In a close-knit culture that

Please cite this article in press as: MacIntyre CR et al. Measles control in Australia – threats, opportunities and future needs. Vaccine (2018), https://doi.org/
10.1016/j.vaccine.2018.06.022
C.R. MacIntyre et al. / Vaccine xxx (2018) xxx–xxx 3

practices communal living and has larger families, control mea- the end of 2012, and the NVC’s report, along with reports from 13
sures such as quarantine may be a challenge to implement without other counties, was considered by the RVC during its third meeting
the support of the community [29]. in October 2013[1].
In the 2012 Sydney outbreak, 20% of cases were infected in To maintain Australia’s elimination status, it is critical to con-
health care facilities [5]. Nosocomial transmission is common in tinue surveillance that is sensitive enough to detect all cases. In
measles outbreaks in the post-elimination era [2]. Such settings addition, cases must be promptly isolated, and contacts must be
are ideal for the transmission of measles due to closed spaces, pres- identified, their immune status assessed, post-exposure prophy-
ence of susceptible individuals, low awareness among health pro- laxis administered and quarantine implemented as needed. It is
fessionals, poor triage and long waiting times [28]. Lack of also important to identify under-vaccinated populations vulnera-
diagnostic experience among clinicians who may have never seen ble to outbreaks after importation of measles cases.
a case of measles could allow the disease to go undetected [29,30]. The genetic characterisation of wild-type (WT) measles virus
A recent review found that up to 50% of transmission in developed provides a means to study the transmission pathways of the virus
countries that hold measles elimination status, occurred in a health and is an essential component of laboratory-based surveillance. It
care setting [31]. aids the differentiation of wild-type virus strains from vaccine
Prior to the 2012 outbreak, other smaller outbreaks of measles strains, which is important in the elimination and post-
were reported in Australia. In 2010, an outbreak of 9 cases was elimination phases. By comparing local sequences to global
linked to an 11-year-old refugee from a measles endemic country, sequences, determination of country of origin may be possible.
Malawi, who travelled on an international flight while infectious. For molecular epidemiologic purposes, genotype designations are
From early February until the end of March 2011, 26 cases were considered the operational taxonomic unit, while related geno-
confirmed, the first outbreak to be reported in the Western Sydney types are grouped by clades. The genotypes imported into Australia
Local Health District area since 2006. Additional sporadic out- since 2008 were mostly from countries in South Asia. Molecular
breaks have occurred in Australia since 2012; a university campus analysis of the 2012 Sydney outbreak identified a single lineage
in Queensland in 2015, and more recently outbreaks in Western of D8 genotype imported from Thailand [5]. However, identifying
Sydney in 2016 and 2017. additional gene targets could lead to further phylogenetic grouping
The reasons for continuing measles outbreaks in countries with and establish more accurate transmission chains. In outbreak set-
verified elimination include an increased volume of travel to and tings, it is critical to rapidly differentiate vaccine strains from WT
from endemic countries, and pockets of susceptible populations strains to enable valuable resources to focus on contact tracing
due to low immunisation rates in certain vulnerable populations and laboratory investigation of WT cases.
such as immigrants and refugees possibly due to difficulty in Mathematical modelling strategies have been used to inform
accessing care, primary vaccine failure, and waning immunity (sec- preparedness planning for outbreaks and interventions. Although
ondary vaccine failure) in the absence of endemic disease. In one limitations exist, one of the most useful outputs of mathematical
study, 8.9% of 763 fully immunised children vaccinated a mean models is the ability to estimate the effectiveness of potential
of 7.4 years earlier, lacked protective levels of circulating alternative vaccination schedules. Modelling can also track
measles-specific neutralising antibodies suggesting that even 2 changes in R0 to predict the risk of epidemics over time. The
doses of the current vaccine may be insufficient at a population Measles Control Campaign in Australia reduced the R0 of measles
level in countries that have achieved elimination status [30]. In from 0.9 to 0.57 and in the same study R was predicted to reach
another study of notified cases of measles in Australia, under- the epidemic threshold in 2007 [43]. In another, R was predicted
vaccination in both infants of vaccine refusers and adults was com- to stay well below the epidemic threshold of 1 until 2012; from
mon, but some cases reported two doses of vaccine [31]. Studies 2009 to 2011, R estimates based on national notification data
have also shown that vaccine-induced immunity might be less pro- remained <1 [38,39].
tective and may wane compared to immunity conferred by natural
measles infection [10,32–35]. 4.1. Policy gaps for measles vaccination in Australia

Low vaccination coverage among risk groups including


4. Methods to maintain measles elimination in Australia – migrants, refugees and health care workers is one of reasons for
Identified gaps and recommendations. the re-emergence of measles [40]. Other reasons include delayed
recognition of measles cases in health care facilities and low accep-
The global, regional and national epidemiology of measles, as tance of mandatory vaccination policies by health care workers
well as measles control guidelines and research gaps were [40–46].
reviewed. Recommendations were drafted based on consideration Policies for quick diagnosis and triage of suspected measles
of epidemiology, research evidence, discussion and consensus. cases and immediate airborne precautions are critical to prevent
The WHO Western Pacific region guidelines on verification of spread of measles in hospitals [42,47]. Large health care facilities
measles elimination established in 2012 included three verification should maintain good triage protocols, up to date electronic occu-
criteria for measles elimination: documentation of interruption of pational health records and mandate vaccination of health care
endemic measles virus transmission for a period of at least 36 workers against vaccine-preventable diseases such as measles
months, presence of a well-performing and high-quality surveil- [41,48] as well require the use of respirators by health care work-
lance system and supportive genotyping evidence [36]. These cri- ers caring for patients with suspected measles, regardless of their
teria were assessed using indicators across five lines of evidence presumed immune status [44,49]. In Australia, national guidelines
including a description of measles epidemiology, quality of epi- recommend that all adults have evidence of measles immunity
demiological and laboratory surveillance, population immunity, such as year of birth before 1966, 2 doses of MMR vaccine or sero-
vaccination program sustainability, and genotyping data [37]. logical evidence of immunity [50], but measles vaccination is not
Genotyping data are important in identifying importation and con- mandatory. Historically, screening of health care workers for
firming lack of sustained endemic transmission. An Australian immunity has been found to be more cost-effective than universal
National Verification Committee (NVC) for the Elimination of vaccination [51]. In 2002, New South Wales introduced policy for
Measles was convened in February 2013 to oversee the compila- screening and vaccination of health care workers against vaccine-
tion of data against the five lines of evidence for the period up until preventable diseases including measles [52].

Please cite this article in press as: MacIntyre CR et al. Measles control in Australia – threats, opportunities and future needs. Vaccine (2018), https://doi.org/
10.1016/j.vaccine.2018.06.022
4 C.R. MacIntyre et al. / Vaccine xxx (2018) xxx–xxx

School-based immunisation campaigns have proven to be effec- birth, death and marriage data, which can provide information
tive in increasing rates of measles immunisation [53]. The Aus- about ethnicity, language spoken at home, ancestry, country of
tralian Measles Control Campaign in 1998 increased birth and parents’ country of birth. For adults, the AIR could inte-
immunisation coverage from 84% to 94% [54]. Immunisation poli- grate information collected from various databases in primary
cies for school children in Australia differ from state to state; care and public health at the district and state levels on migrant
NSW preschools cannot enrol a child unless parents provide infor- and refugee status and other risk factors to understand gaps in
mation about their child’s immunisation status including whether immunisation coverage.
parents are conscientious objectors to vaccination. A recent change
in policy excludes unvaccinated children from childcare in several
States without a medical exemption. There is a school immunisa- 5. Recommendations
tion schedule for high school students, including catch-up immuni-
sation for 2 doses of MMR vaccine for all students [55]. Consensus discussion among participants of the workshop
resulted in the following recommendation to reduce gaps in
4.2. Research to inform measles control measles control policy in Australia:

In Australia, genotyping of measles virus is not routine. Geno- 1. Increase visibility of measles elimination in Australia
typing differentiates wild-type and vaccine strains of measles
and can help track global transmission pathways. From 2008 to Raise awareness of the role of immunisation providers in main-
2015, several different genotypes were imported and transmitted taining elimination status and the importance of MMR vaccination.
into Australia from Asian and European countries, B3, D5 and D8 Low acceptance of mandatory vaccination policies and vaccine rec-
being the most common [56–58]. Investigation of cases of ommendations by health care workers [40–46], are leading reasons
unknown origin will assist in identifying sustained endogenous for under-vaccination particularly among adolescents and adults.
transmission in Australia if it occurs. Improve awareness of measles among health care providers and
Serosurveys conducted in Australia [59] and in other countries ensure systematic triage protocols and outbreak protocols in the
that have eliminated measles [60] support a substantial decline healthcare setting.
in anti-measles IgG antibody levels. This warrants further investi-
gation to determine the extent of waning of vaccine-induced 2. Create a different funding model for maintaining measles
immunity and to what extent individuals with low or undetectable elimination
levels of measles-specific IgG antibodies are protected against
infection if exposed to measles. Create a funding model that works outside the boundaries of
There is a gap in research on role of vitamin A in the manage- the Pharmaceutical Benefits Advisory Committee considering eco-
ment of measles in developing countries and the effect of vitamin nomic and social gains and national and international responsibil-
A in reducing the rate of death in children with measles [61,62]. ities toward maintaining elimination status and access to
There is also a gap in research on the association between measles vaccination [65]. The Australian Department of Health announced
and other diseases such as Kawasaki disease [63]. Two studies free vaccination for refugees and other humanitarian entrants
show that Kawasaki disease could be an unusual response in a sus- through the National Immunisation Program (NIP), which meets
ceptible individual to various infectious agents [63,64]. this gap. From 1 July 2017, MMR is provided free in most states
The workshop recommended cost-effectiveness studies and [66].
research in diagnosis, immunology, and modelling of measles out-
breaks. This includes integrating phylogenetic data with routine 3. Whole-of-life immunisation register
surveillance data; the effect of viral load on infectiousness, disease
severity and response to treatment; and household and commu- The workshop recommended a whole-of-life immunisation reg-
nity transmission studies. ister that has the capacity to document measles immunisation for
The clinical significance of waning vaccine-induced measles all ages, including documentation of immunisation status at school
specific-IgG antibodies should be studied. Opportunistic studies entry. An Australian Immunisation Register was launched in 2016
examining immune responses and symptoms in individuals with [67]. There is no national immunisation policy for entry to pre-
various antibody levels and avidity following exposure to measles school, primary school, secondary school or university, and no
are important to better understand population susceptibility. capacity to record and report immunisation history in education
Disease modelling could estimate of how quickly immunity facilities1. The workshop recommended compulsory recording of
wanes over time and examine heterogeneity in terms of geo- immunisation status rather than compulsory vaccination. Up to a
graphic and age-specific distribution of susceptibility; modelling third of the notified measles cases in travellers are children of
of cost-effectiveness of different vaccination schedules and catch- migrants who were born in Australia and were visiting friends and
up programs will also be useful. relatives in their parents’ country of birth when they became
infected [31]. It was recommended that the whole-of-life immunisa-
4.3. Data gaps and opportunities in routine data collection for tion register include information about child’s and parents’ country
maintenance of measles elimination in Australia. of birth to flag people at risk of under-vaccination. Like health care
workers, school employees may be at increased risk of contracting
The whole-of-life AIR has been established in 2016 in Aus- vaccine-preventable diseases [68]. The workshop recommended
tralia. It is recommended that information about migration status, addressing policy gaps for immunisation for school employees.
year of migration, refugee status, ethnicity and language spoken
at home be included. Including health care workers, child care 1
A new immunisation policy ‘‘No jab, no pay” was announced in 2015 where
workers and high school teachers as occupational risk groups conscientious objection is no longer an approved exception for eligibility for the Child
would also be helpful. GPs should be able to check the measles Care Rebate, Child Care Benefit, and Family Tax Benefit (Part A - Supplementary).
Under the new law parents who do not fully immunise their children up to 19 years of
vaccination status of their patients on the AIR. The workshop rec- age are no longer eligible for child care benefits and family assistance payments with
ommended changes in routine collection of immunisation data. exceptions for children recorded with medical contraindications or natural immunity
For children, it was recommended to link AIR data with perinatal, for certain diseases and those on a recognised catch-up schedule

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10.1016/j.vaccine.2018.06.022
C.R. MacIntyre et al. / Vaccine xxx (2018) xxx–xxx 5

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