wo major milestones in the history
of measles control have recently been achieved. Since November 2002,
measles is no longer endemic in the Western Hemisphere(1) and the 2005
goal set by the World Health Assembly (WHA) to halve measles deaths
worldwide (compared to 1999 levels) was achieved on time(2). The main
intervention that led to these achievements was the tactical scaling-up of
In May 2005, the WHA welcomed the goal of reducing
measles deaths by 90% by 2010 compared to 2000 levels, as part of the
Global Immunization Vision and Strategy (GIVS)(3). This global goal was
endorsed unanimously by the WHA in May, 2008. This editorial explores the
potential impacts of measles control strategies on child survival in India
and on the global goal of reduction in measles mortality.
Measles in India
Measles continues to be an important cause of childhood
morbidity and mortality in many states in India. At a workshop convened
jointly by Government of India (GoI), WHO, and UNICEF on measles, in May
2007, it was estimated that between 100,000 and 160,000 children die from
measles in India each year and that over 90% of deaths occur in 10 states
– Uttar Pradesh (UP), Bihar, Rajasthan, Madhya Pradesh, Jharkhand, Assam,
West Bengal, Andhra Pradesh (AP), Orissa and Gujarat (preliminary results
from a workshop held at National Polio Surveillance Unit, New Delhi, May
A recent (2006) vaccination coverage survey in India
showed overall 71% coverage for measles vaccine (given during 9 to 12
months of age)(4). Accepting 85% vaccine effectiveness for vaccination at
9 months, actual protection was offered to only 60% of annual birth
cohorts (71% × 85% = 60%). In other words, 40% remained susceptible to
measles. Coverage of measles vaccine was less than 50% in UP, Bihar, Assam
and Nagaland and between 50% and 80% in 13 other states(4). Worldwide, of
the estimated 26.2 million infants who missed receiving their first dose
of measles vaccine by age 12 months through routine immunization services
in 2006, 10.5 million were in India(5).
Six states (AP, Gujarat, Karnataka, Kerala, Tamil Nadu,
West Bengal) conduct measles surveillance through clinical and laboratory
outbreak investigations. In these states, nearly 80% cases occur in
children less than 10 years old (data available at National Polio
Surveillance Project [NPSP], New Delhi). Even in the states with moderate
routine immunization coverage, many under-five children with measles had
not been given measles vaccine (e.g. West Bengal 72%, Karnataka
38%, Gujarat 35%). According to the Registrar General and Census
Commissioner of India, UP, Bihar and Assam together had 114 million
children under 15 years of age, in 2006(6). More than half of them had not
received measles vaccine – providing fertile ground for continued intense
transmission of measles virus.
Studies in India have shown median case-fatality ratio
(CFR) of 3.8% (range: 0% to 30%) among children with measles(7). UP had
recorded measles CFR of 4.1% in 1996, through routine reporting(8).
Actually the present surveillance method tends to under-report measles
Given the formidable challenges of wide inter-regional
disparities of immunization coverage, a huge unvaccinated child population
and the large disease burden, can India reduce its enormous measles
morbidity and mortality?
Measles Control Strategies
Since 2000, almost all countries with high mortality
from measles in the past have implemented, under diverse conditions,
control strategies recommended by WHO and UNICEF. Although several factors
had contributed to high measles mortality, experience with implementing
these strategies has taught us that measles deaths can be drastically
reduced even in settings of poverty, malnutrition, and overall high child
mortality rates. The current WHO/UNICEF strategy to reduce measles
mortality consists of four components:
(i) achieving and maintaining high coverage
(>90%) with the first dose of measles vaccine in every district,
delivered through regular immunization services;
(ii) ensuring that all children receive a
second dose of measles vaccine delivered either through periodic
supplementary immunization activities (SIAs)…
and/or routine services;
(iii) effective laboratory-backed surveillance
(of disease and outbreaks) and monitoring of immunization coverage; and
(iv) appropriate clinical measles
case-management, including the provision of vitamin A.
Strategy 1: Strengthening regular immunization system
Strengthening immunization system from the block level
up must remain top priority for improved measles control in India. Only 4
states (Tamil Nadu, Kerala, Himachal Pradesh, Goa) and 4 Union Territories
(Puducherry, Chandigarh, Lakshadweep, and Daman and Diu) have achieved
one-dose measles vaccination coverage of more than 90%. However,
improvement in routine immunization alone will not reduce the susceptible
pool of older children who had missed measles immunization, owing to
underperformance of the system in previous years.
Strategy 2: Providing a second dose of measles vaccine
The average seroconversion rate with measles
vaccination at 9 months is 85% (range 70%-98%)(9,10). Thus, approximately
15% of vaccinated children remain susceptible in spite of receiving one
dose. As the level of ‘herd immunity’ needed to significantly impact
measles transmission is in the range of 93-95%, even 100% coverage with a
single dose of measles vaccine administered at 9 months of age will not
prevent the accumulation of a susceptible pool and consequent periodic
measles outbreaks. Seroconversion rate improves to >95% when the vaccine
is given after one year of age, but the first dose has to be given earlier
to protect infants. Field investigations of recent measles outbreaks in
developing countries have found that, while some cases occurred in
previously vaccinated children (i.e., vaccine failure), most cases
occurred in unvaccinated children, indicating that program failure was the
For these reasons, WHO and UNICEF recommend that all
national immunization programs provide 2 doses of measles vaccine for all
children(11). The purpose of the second dose is to protect children who
received their first dose but failed to respond. In addition, the second
opportunity provides one dose to those who missed the first dose. In
settings with low to moderate routine vaccination coverage (<80%), SIAs
are the preferred method of delivering the second dose, as they usually
achieve coverage levels of >90%. SIAs reach children who lack access to
health services, and have been shown to rapidly reduce measles incidence.
In settings with high routine vaccination coverage (i.e.,
for 3 or more consecutive years), the second dose may be delivered through
Strategy 3: Measles case surveillance with laboratory
Effective surveillance system for measles is critical
to monitor programme impact and to adopt appropriate immunization tactics
to control outbreaks, if any. Surveillance should be backed by proficient
laboratory support. When measles is widely endemic, reporting of
aggregated data to track and investigate outbreaks and to identify
underserved areas is the appropriate approach. Once the measles incidence
is low, for example after conducting an SIA targeting a wide age range (e.g.
1-14 years), it is appropriate to establish case-based surveillance with
investigation and laboratory testing of suspected measles cases and
In 2006-2007, building on the acute flaccid paralysis
reporting sites and laboratory network for polio eradication, the
Government of India initiated outbreak-based measles surveillance in six
states (named above) with technical assistance from NPSP. This system is
already providing essential information needed to define the basic
epidemiology of measles in those states. An added function of the
laboratory is to support vaccination coverage monitoring through measuring
antibody prevalence by age.
Strategy 4: Appropriate treatment including vitamin A
High dose of vitamin A has been shown to decrease
severity of illness and CFR in young children hospitalized with measles in
developing countries. Therefore WHO currently recommends vitamin A for all
children with acute measles.
Experience in applying the above strategies in various
settings has shown that countries with low to moderate levels of routine
immunization coverage can quickly bring down measles mortality through
successful catch-up campaigns as observed in 19 African countries and
Nepal(14,15). Worldwide, their implementation has resulted in 74%
reduction in estimated measles deaths (from 750,000 in 2000 to 197,000 in
2007)(5). The greatest reduction was in African and the Eastern
Mediterranean Regions (where measles mortality decreased by 89% and 90%,
respectively). WHO estimates that approximately two-thirds of the global
burden of measles deaths, namely 136, 000 (range 98,000 to 180,000),
occurred in the SEA Region in 2007, with most of them occurring in India.
From 2000 to 2007, approximately 613 million children aged 9 months to 14
years received measles vaccine through campaigns in the 47 countries with
the highest burden of measles, except in India. Pakistan completed the
catch-up campaign in early 2008. Thus, in 2009, India remains the only
country in the world that has not systematically introduced a second dose
of measles vaccine.
The Roadmap for India
The Government of India convened a group of national
and international experts (India Technical Advisory Group on Measles,
ITAGM) for advice on the most appropriate immunization and surveillance
strategies to reduce measles mortality in the country. During its first
meeting (2008) ITAGM noted the results of the measles disease-burden
workshop (May 2007), especially the finding that ten states in India
accounted for over 90% of all measles deaths and the surveillance data
indicating that nearly 90% of the measles cases are under 10 years of age.
The ITAGM recognized and emphasized the urgency to start accelerated
measles mortality reduction activities in India including conducting
measles catch-up vaccination campaigns in one or more of the medium to
high burden states. In addition, the main ITAGM recommendations called
(a) strengthening of immunization services
with particular attention to states with low coverage, as this would be
critical for sustaining disease reduction that follows catch-up
(b) expansion of the outbreak-based measles
surveillance supported by WHO accredited laboratories – to help plan
optimum catch-up campaigns and assessment of their impact.
At the June 2008 meeting of the National Technical
Advisory Group on Immunization (NTAGI), the recommendations from ITAGM
were discussed and accepted in principle. NTAGI, after reviewing data on
measles epidemiology and CFR, has recommended the following:
• A second dose of measles vaccine should be
introduced in the Universal Immunization Programme (UIP) at the time of
DPT booster dose (at 18 months of age) in states with
evaluated coverage with the first dose of measles vaccine;
• Catch-up measles vaccination campaigns should be
implemented for children up to age 10 years in states with <80%
evaluated coverage with the first dose of measles vaccine and that
detailed action plans for these SIAs should be finalized immediately in
states with low coverage and high measles mortality burden;
• A study to determine measles CFR in high burden
states should be conducted to enable better estimation of the number of
measles deaths in India; and
• Measles surveillance should be enhanced in high
burden states to assist with planning of catch-up campaigns and to
establish baseline data.
The categorization of the states by NTAGI (below and
above 80% coverage) was proposed to provide the broad framework on which
national and state programme managers can draw up operational plans
quickly for the second dose of measles vaccine.
Challenges for India
With the defined roadmap for accelerated measles
control, what are the barriers (perceived and real) to implementation?
Impact on UPI. Concerns have been expressed
regarding potential adverse impact of accelerated measles control
activities, especially the catch-up campaigns, on UIP. Evidence from
experience in other countries showed no such adverse impact. Between 2000
and 2006 — the period of intense measles control activities through
catch-up campaigns in the African region, routine coverage with first dose
of measles vaccine actually rose from 56% to 73%; in the Eastern
Mediterranean region, from 73% to 83%; and in the Western Pacific region,
from 86% to 93%. During the same period, coverage in countries of the
South East Asian Region other than India, rose from 77% to 85%(16).
Will injection safety be compromised during vaccination
campaigns? Actually such campaigns in other countries have served as
an opportunity for promoting injection safety, including safe waste
disposal and management of adverse events following immunization (AEFI),
and for raising standards of training of vaccinators and improving the
cold chain for vaccine storage and transport. Social mobilization efforts
by volunteers have been instrumental for the success of campaigns by
providing information to and creating demand from target populations,
especially the hard-to-reach and marginalised(14-16).
Adverse effects. In 2008, serious AEFI (adverse
events following immunization) were reported resulting in death in a few
children after giving measles vaccine. So there is apprehension among some
in India that campaigns might lead to serious AEFI. Actually death was due
to programmatic errors at local level. Careful planning, sound training,
close monitoring and an efficient AEFI management system during measles
vaccination campaign can effectively mitigate all such risks as
demonstrated repeatedly during measles vaccination campaigns in many
countries around the world.
Impact on polio eradication. Will accelerated
measles control activities now distract attention from the current
priority of polio eradication and add to ‘campaign fatigue’? Each of the
other remaining polio endemic countries has already implemented measles
control strategies; such activities, including campaigns increased
community demand for vaccination(16). Many other countries had implemented
measles vaccination campaigns during their active phase of polio
eradication, taking advantage of the already trained and mobilized work
force with updated maps, local implementation micro-plans, and a
functioning monitoring system.
Measles vaccination campaigns targeting millions of
children from 9 months to 10 years of age in many states of India will be
a huge undertaking. This will require firm commitment of state
governments, careful advance planning, implemen-tation in manageable
phases and full gearing up of the public sector health system at the
sub-district, district, state and national levels. If public-private
participation is desired, it can be locally designed and managed.
Without drastic measles mortality reduction in India,
the global goal to reduce measles mortality by 90% by 2010 will not be
met. Implementation of the NTAGI recommendations for accelerating measles
control in India represents an opportunity to rapidly reduce measles
mortality thereby contributing to achievement of the 4th Millennium
Development Goal (reduce under-5 child mortality by 2/3 by 2015). It is
also an obligation on the part of the Government for the provision of
equitable services to the children of all states.
Conflict of interest: None stated.
† SIAs are generally carried out in two
phases. An initial, nationwide catch-up SIA targeting 90% of susceptible
populations has the goal of eliminating or drastically reducing the
susceptible pool. Periodic follow-up SIAs then target all children born
since the last SIA. They are conducted nationwide every 2-4 years, with
the goal of eliminating susceptibility in recent birth cohorts
1. de Quadros CA, Olivé JM, Hersh BS, Strassburg MA,
Henderson DA, Brandling-Bennett D, et al. Measles elimination in
the Americas: evolving strategies. JAMA 1996; 275: 224–229.
2. Wolfson LJ, Strebel PM, Gacic-Dobo M, Hoekstra EJ,
McFarland JW, Hersh BS. Has the 2005 measles mortality reduction goal been
achieved? A natural history modelling study. Lancet 2007; 369: 191-200.
3. World Health Organization. Global Immunization
Vision and Strategy Document. Available from: http://www.who.int/immunization/givs/en/index.html.
Accessed on 21 July, 2009.
4. Coverage Evaluation Survey 2005, All India: a
Report. New Delhi: Unicef; 2006.
5. World Health Organization. Progress in global
measles control and mortality reduction, 2000-2007. Wkly Epidemiol Rec
2008; 83: 441-448.
6. Census of India 2001. Population Projections For
India And States 2001-2026 (Revised December 2006). Report of the
technical group on population projections constituted by the national
commission on population. New Delhi: Office of the Registrar General &
Census Commissioner, India; 2006.
7. Wolfson LJ, Grais, RF, Luquero FJ, Birmingham ME,
Strebel PM. Estimates of measles case fatality ratios: a comprehensive
review of community-based studies. Int J Epidemiol 2009; 38: 192-205,
8. Singh J, Kumar A, Rai RN, Khare S, Jain DC, Bhatia
R, et al. Widespread outbreaks of measles in rural Uttar Pradesh,
India, 1996: High risk areas and groups. Indian Pediatr 1999; 36: 249-256.
9. Cutts FT, Grabowsky M, Markowitz LE. The effect of
dose and strain of live attenuated measles vaccines on serological
responses in young infants. Biologicals 1995; 23: 95-106.
10. Job JS, John TJ, Joseph A. Antibody response to
measles immunisation in India. Bull WHO 1984; 62: 737-741.
11. World Health Organization. Meeting of the
Immunization Strategic Advisory Group of Experts, November 2008 –
conclusions and recommendations. Wkly Epidemiol Rec 2009; 84: 1-16.
12. World Health Organization. Weekly Meeting of the
immunization Strategic Advisory Group of Experts, April 2009 – Conclusions
and Recommendations. Wkly Epidemiol Rec 2009; 84: 220-236.
13. WHO Module on best practices for measles
surveillance. Available from: http://www.who.int/vaccines-documents/DocsPDF01/www617.pdf.
Accessed on July 29, 2009.
14. Otten M, Kezaala R, Fall A, Mashreasha B, Martin R,
Cairns L, et al. Public health impact in the WHO African Region
2000-2003. Lancet 2005; 366: 832-839.
15. World Health Organization. Progress in Measles
Control: Nepal, 2000-2006. Wkly Epidemiol Rec 2007; 82: 346-351.
16. WHO vaccine-preventable diseases monitoring system, 2008 global
summary. Available from: http://www.who.int/immunization/documents/WHO_IVB_2008/en/index.html).
Accesssed July 29, 2009.