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Article history: Background: All six World Health Organization (WHO) regions have committed to eliminate measles, and
Received 20 March 2018 three WHO regions have committed to eliminate rubella. One of the key tenets of measles and rubella
Received in revised form 7 August 2018 elimination is to have a strong surveillance system in place. The presence of a case-based measles and
Accepted 1 October 2018
rubella surveillance system that is national, population-based, provides laboratory confirmation, and
Available online xxxx
directs action, is one of the requirements for elimination-standard surveillance.
Methods: In order to understand the global landscape for measles and rubella surveillance, a question-
Keywords:
naire was sent to all 194 WHO member states (herein referred to as countries) requesting information
Measles
Rubella
on how surveillance was conducted for measles, rubella, and congenital rubella syndrome. Data were
Surveillance supplemented with information provided to WHO through other reporting mechanisms and by national
Elimination policy documents available to the public. Frequencies and percentages were calculated.
Results: Data were available to review from 164 (85%) countries, although not every country responded
to every question. Case-based, population-based, national surveillance with laboratory confirmation was
reported to be conducted in 136 (86%) of 158 countries for measles and 122 (77%) of 158 countries for
rubella. Congenital rubella syndrome surveillance was reported to be conducted by 126 (77%) of 163
countries. Gaps were noted in the quality of measles-rubella surveillance conducted, and 26 (16%) of
158 countries reported not including all healthcare providers as mandatory reporters.
Conclusions: Many countries reported having some of the essential components in place to conduct
elimination-standard surveillance for measles and rubella; however, in order to achieve elimination,
the quality of surveillance needs to improve to detect all cases. In those countries without these essential
components of elimination-standard surveillance, the first step is to implement these components.
Ó 2018 Published by Elsevier Ltd.
https://doi.org/10.1016/j.vaccine.2018.10.007
0264-410X/Ó 2018 Published by Elsevier Ltd.
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
2 M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx
WHO has provided guidance on surveillance in elimination set- nents of an elimination-standard surveillance platform, namely if
tings for measles, rubella, and congenital rubella syndrome (CRS) the system (1) was case-based, (2) had the ability to laboratory
[3,6]. WHO regions adapted this global guidance based on specific confirm cases, (3) was national, and (4) was population-based.
regional settings; specifically, case definitions and recommenda- These four components are necessary but not sufficient for measles
tions on the algorithm for laboratory testing were adjusted based and rubella elimination-standard surveillance. The data provided
on resources and progress towards elimination [7–12]. Table 1 out- by countries were reviewed, and countries were asked to clarify
lines the global and regional recommendations for conducting and correct discrepancies that were identified. Data on measles
measles-rubella surveillance. and rubella surveillance systems were supplemented by reviewing
Almost all countries conduct measles and rubella surveillance other sources of information provided to the public through official
and report surveillance data to WHO regularly (either weekly or government websites or to WHO. Additional data sources included
monthly). At the global level, WHO collects monthly data on the annual measles verification reports provided to WHO as part of the
number of reported measles and rubella cases; however, little is regional measles verification process for countries in WHO’s Euro-
known at a global level about how surveillance is actually being pean and South-East Asia Region, national surveillance guidelines,
conducted in each country. To understand the global situation and the WHO/UNICEF Joint Reporting Form. Data were stored and
and how much variability in measles and rubella surveillance analyzed using Microsoft Excel 2010 (Seattle, WA, USA), and the
exists, a survey was conducted to determine if countries follow results were mapped using ArcGIS 10.5 (Redlands, CA, USA).
the recommended global and/or regional standards for measles
and rubella surveillance.
2.2. Measles-Rubella surveillance system indicators
Table 1
Recommendations for case definitions and laboratory algorithm for measles and rubella.
Geographic Area Number of Suspected Measles Case Definition Suspected rubella case definition Recommended laboratory
Countries algorithma
Global [3] 194 Fever and maculopapular rash Fever and maculopapular rash Based on incidence, with
OR OR integrated testing (serial or
Suspected by a Healthcare worker Suspected by a Healthcare worker parallel testing)
Region of the Americas [9] 35 Fever and maculopapular rash Fever and maculopapular rash Parallel testing
OR OR
Suspected by a Healthcare worker Suspected by a Healthcare worker
Africa Region [8] 47 Fever and maculopapular rash and one of Fever and maculopapular rash and one of Serial testing
the following: cough, conjunctivitis, the following: cough, conjunctivitis, coryza
coryza (3 C’s) (3 C’s)
OR OR
Suspected by a Healthcare worker Suspected by a Healthcare worker
Eastern Mediterranean 21 Fever and maculopapular rash and one of Suspected to be rubella by a Healthcare Serial testing
Region [10] the following: cough, conjunctivitis, worker
coryza (3 C’s)
European Region [7] 53 Fever and maculopapular rash and one of Maculopapular rash and cervical, Based on incidence, with
the following: cough, conjunctivitis, suboccipital, or postauricular adenopathy, integrated testing (serial or
coryza (3 C’s) or arthralgia/arthritis parallel testing)
South-East Asia Region [11] 11 Fever and maculopapular rash Fever and maculopapular rash Serial testing
OR OR
Suspected by a Healthcare worker Suspected by a Healthcare worker
Western Pacific Region [12] 27 Fever and maculopapular rash Fever and maculopapular rash Based on incidence, with
integrated testing (serial or
parallel testing)
a
Serial testing is defined as measles antibody being tested first, with samples testing negative for measles antibody being tested for rubella antibody, or vice versa, based
on disease incidence. Parallel testing is where all samples are tested for both measles and rubella regardless of results.
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx 3
Fig. 1A. Presence of a case-based, population-based, national measles surveillance system with laboratory confirmation (‘‘recommended measles surveillance system”).
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
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Fig. 1B. Presence of case-based, population-based, national rubella surveillance system with laboratory confirmation (‘‘recommended rubella surveillance system”).
Fig. 2. Non-measles non-rubella discard rate per 100,000 persons, July 2016-July 2017.
specific case definition (‘‘a person with fever and maculopapular recommended case definition for a suspected rubella case (‘‘a per-
rash and one of cough, coryza or conjunctivitis”); this more specific son with fever and maculopapular rash”), while 74 (47%) of 160
case definition was used during the mortality reduction phase of countries reported using the specific definition of ‘‘a person with
measles. Similar findings were reported for rubella surveillance; maculopapular rash and cervical, suboccipital or postauricular
55 (35%) of 160 countries reported using the globally- lymphadenopathy, or arthralgia/arthritis” (Table 2B). ‘‘Suspicion
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx 5
Table 2A
Number and percentage of countries reporting the suspected measles case definition used, by region. The gray shading highlights the case definition(s) recommended in each
region.
a
Healthcare worker suspicion and other could not always be extracted from supplemental data sources, thus resulting in the changing denominator.
by a health care worker (HCW)” was included in the suspected case countries that reported not including all providers, 25 reported
definition in 60 (46%) of 160 countries for measles and 50 (38%) of excluding private facilities, while seven reported excluding some
160 countries for rubella. public health facilities, usually those where health facilities are
One hundred and forty-four (95%) of 152 countries reported challenging to access (e.g., three are island countries with hard-
having mandatory reporting for all suspected measles cases, and to-reach health facilities).
121 (79%) of 153 reported having mandatory reporting for all sus- Most countries reported following the regional or global recom-
pected rubella cases. Eight countries did not have mandatory mendations for laboratory testing of suspected measles and rubella
reporting of either, while 21 countries had mandatory reporting cases, although significant variation existed. Of 157 countries pro-
of suspected measles cases but not of suspected rubella cases. viding data on laboratory testing, 69 (44%) reported conducting
Among 92 countries with data in those regions with a rubella elim- serial testing driven in large part by incidence of disease (namely,
ination goal with data, 76 (83%) had mandatory rubella reporting, testing first for measles, and then for rubella if the sample was
compared to 45 (74%) of 61 countries with data in those regions measles IgM antibody negative, or testing first for rubella and then
without an elimination goal. One hundred and thirty-four (89%) for measles if the sample was rubella IgM antibody negative).
of 151 countries required reporting of measles to be done at least Seventy-one (45%) countries reported conducting parallel testing
on a weekly basis. Among the WHO regions, the Western Pacific (that is, testing all samples for both measles and rubella simultane-
region had the lowest proportion (10/16, 63%) of countries requir- ously irrespective of the result); 32 (20%) countries reported only
ing measles to be reported weekly or more frequently. conducting testing based on the clinician’s request, i.e., samples
One hundred and twenty-seven (80%) of 158 countries reported from suspected measles cases are only tested for measles, and
that all health facilities and healthcare providers, including all pri- those from suspected rubella cases are only tested for rubella. Test-
vate and public-sector health care facilities, were part of case- ing based on the clinician’s request was most frequent in the Euro-
based, national surveillance for measles and rubella. Of 26 (16%) pean region in which 23 (44%) of 52 European countries providing
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
6 M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx
Table 2B
Number and percentage of countries reporting the suspected rubella case definition used, by region. The gray shading highlights the case definition(s) recommended in each
region.
a
Healthcare worker suspicion and other could not always be extracted from supplemental data sources thus resulting in the changing denominator.
data followed this practice. While most parallel testing occurred in Among 61 countries with data in those regions without a rubella
countries with a low incidence of measles, 12 (8%) countries with elimination goal, 26 (43%) countries did not have CRS surveillance,
an incidence of >5 cases of measles per million persons performed and 18 (30%) had case-based surveillance with laboratory confir-
parallel testing. This does not conform to the global recommenda- mation that was either national and population-based or sentinel.
tion for high burden countries to perform serial testing based on
incidence to save limited resources.
4. Discussion
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx 7
Fig. 3. Type of Congenital Rubella Syndrome (CRS) surveillance system in place.* (*‘‘Unknown surveillance” is defined as a country that reported doing CRS surveillance, but
the details on how surveillance was done was not provided. ‘‘Data not available” means that data were not provided by a country on if they do or do not conduct CRS
surveillance.)
their surveillance system quality. Furthermore, even though it is improve their surveillance quality is to change to the more sensi-
recommended that measles and rubella surveillance be integrated, tive case definition. However, many countries do not have the
there are some countries that have yet to do this. In addition, CRS resources to test every acute fever-and-rash case, and, with the
surveillance is lagging behind rubella disease surveillance, with success of immunization, measles is becoming rare in many places.
23% of countries not conducting CRS surveillance. CRS surveillance Given this, countries will have to consider the quality and perfor-
is needed to help provide evidence that rubella has been mance of their surveillance systems, but, at a minimum, need to
eliminated. ensure that their health systems can rapidly identify all measles
The Roadmap to elimination standard measles and rubella surveil- and rubella cases. One tactic that is recommended, given the broad
lance describes practical steps on how countries can improve case definition, is to integrate measles and rubella surveillance
surveillance quality and achieve all the components needed for with other febrile rash surveillance systems (e.g., dengue). Practi-
elimination-standard surveillance [4]. Some countries reported cally speaking, this means that all diseases of public health impor-
having some of the necessary components to conduct tance with a febrile rash presentation are investigated
elimination-standard surveillance, although several variations simultaneously and tested for from one laboratory specimen. This
were identified, particularly in countries in regions without rubella allows for more efficient use of resources both in the laboratory
elimination goals. In those countries without the four specific com- and during case investigations, and, in low incidence settings
ponents of elimination-standard measles-rubella surveillance, where clinicians might not be thinking about measles and/or
efforts should be made to ensure that surveillance is national, rubella, it ensures that cases are still able to be detected.
population-based, case-based, with laboratory confirmation. All Measles and rubella surveillance is facing an impending chal-
public and private health facilities must be involved in surveillance lenge. Currently, much of measles and rubella surveillance relies
to ensure that all cases are identified, reported, and responded to on polio surveillance systems [17,18]. With polio nearing eradica-
appropriately-and that this is done in a timely fashion. tion, polio resources are diminishing, which will threaten already
Most countries were following the suspected case definition of inadequate measles and rubella surveillance systems. This is espe-
their region. Ideally, case definitions should be aligned with global cially true in countries with the highest measles burden as these
case definitions to help prepare for eradication. Countries using the countries rely most heavily on polio surveillance infrastructure.
more specific case definition of ‘‘a person with fever and macu- Countries and stakeholders must recognize that high quality
lopapular rash and cough, coryza, or conjunctivitis” are probably elimination-standard measles and rubella surveillance is vital to
missing some measles cases since the symptoms are not found in achieving measles and rubella elimination. Given limited
all of confirmed measles cases and many rubella cases since these resources, high burden countries should use laboratory algorithms
symptoms are specific for measles and not rubella [16]. This, along based on measles and rubella incidence to save money and reduce
with variable surveillance quality, makes the comparison of dis- unnecessary testing.
ease burden between countries challenging. The globally- This evaluation has important limitations. In the supplemental
recommended suspected case definition of ‘‘a person with acute questionnaire distributed in 2017, only a few questions were asked
fever and rash” along with healthcare worker suspicion is extre- about elimination-standard surveillance; these questions per-
mely sensitive but not specific, with the goal of ensuring that no tained to foundational elements only. There are many attributes
measles case is missed. One way in which some countries can which need to be in place to meet elimination-standard surveil-
Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007
8 M.K. Patel et al. / Vaccine xxx (2018) xxx–xxx
lance that were not able to be assessed by this questionnaire—for on the part of the World Health Organization concerning the legal
example, the ability to detect cases quickly, the ability to conduct status of any country, territory, city or area or of its authorities, or
thorough investigations on every case to understand who is concerning the delimitation of its frontiers or boundaries. Dotted
infected as well as where and why the person in question was and dashed lines on the maps represent approximate border lines
infected, and the use of the data to inform the program and prevent for which there may not yet be full agreement. Ó WHO 2018. All
future cases from occurring. Not every country had data available, rights reserved.
with a noticeable gap in the Eastern Mediterranean Region (only
50% of countries in this region had data available to analyze). Data References
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Please cite this article in press as: Patel MK et al. Global landscape of measles and rubella surveillance. Vaccine (2018), https://doi.org/10.1016/j.
vaccine.2018.10.007