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20]

Original Article

Trends of measles in Nigeria: A systematic

review
Jalal-Eddeen Abubakar Saleh
Department of Expanded Program on Immunization, World Health Organization, Bauchi Zonal Office, Bauchi, Nigeria

A B S T R A C T
Background: Measles, a highly infectious viral disease, is endemic in developing countries with a peak of transmission from October
to March. The case fatality rate of measles in the developing countries stands at around 3–5%; this could be as high as 10% during
epidemics. Although natural infection with the measles virus confers life-long immunity, those vaccinated with the vaccine could get up
to 10 years of protection. In spite of the availability of measles vaccines, there have been sporadic measles outbreaks, especially in
developing countries, hence the need to know the underlying cause. Study Design: Systematic review. Method: Relevant literature was
reviewed on trend of measles. The literature accessed from the W.H.O and UNICEF sites, and also using Google search include
case-series studies, community-based studies on age-specific measles case fatality ratios (CFRs), and cohort analysis of surveillance
data. Results: The review shows that lowest measles CFR is seen among the vaccinated children and highest seen among the
unvaccinated children. Additionally, the broad range of case and death definitions of measles as well as the study population and
geography, clearly highlight the complexities in extrapolating results for global public health planning. Conclusion: The outcome of
several studies has shown that measles outbreaks are associated with factors that include: weak measles case-based surveillance
in some areas, lack of awareness about the disease among parents, vaccine stock-out, and lack of adequate cold chain equipment
to preserve the vaccine in remote hard-to-reach areas.

Keywords: Case-based surveillance, case fatality rates, measles, outbreaks, vaccination

INTRODUCTION to March. Measles carries with it high morbidity

Measles is a highly infectious viral disease with an
incubation period of 10–12 days and caused by a
virus that belongs to the group of Morbilliviruses
of the family Paramyxoviridae.[1,2] Transmission is
through aerosol droplets or direct contact with the
nasal and oral secretions of an infected person to
susceptible individuals, especially children between
the ages of 9 months to 15 years. This disease is
considered endemic especially in the developing
countries with a peak of transmission from October
Corresponding Author: Dr. Jalal‑Eddeen Abubakar Saleh,
WHO Bauchi Zonal Office, Bauchi State, Nigeria.
E‑mail: drjalals@yahoo.com
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and mortality especially when clinical cases are not
properly managed.[1]
The case fatality rate of measles in the developing
countries is around 3–5%; this could be as high as
10% during epidemics.[1,3‑5] Although natural infection
with the measles virus confers life‑long immunity,
those vaccinated with the vaccine would get up to
10 years of protection from the measles virus. However,
it is interesting to note that about 85% of children
vaccinated with a dose of the measles vaccine could
also get life‑long immunity. In spite of the global efforts
to vaccinate all eligible children as early as 9 months
of age as the maternal immunity wanes out around
that age, it is disheartening to mention that measles
This is an open access article distributed under the terms of the Creative
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others to remix, tweak, and build upon the work non‑commercially, as long as the
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For reprints contact: reprints@medknow.com

DOI:
10.4103/1118-8561.181887 Cite this article as: Saleh JEA. Trends of measles in Nigeria: A systematic
review. Sahel Med J 2016;19:5-11.

© 2016 Sahel Medical Journal | Published by Wolters Kluwer ‑ Medknow 5

[Downloaded free from http://www.smjonline.org on Wednesday, September 28, 2016, IP: 108.63.167.20]
Saleh: Trends of measles in Nigeria: A systematic review
remains one of the leading causes of death among the
under‑fives, especially in the Sub‑Saharan African
continent.[4,5]
The laboratory confirms measles when a blood sample
taken from a suspected case within 30 days of onset of
rash shows measles IgM antibodies. The caveat here
with regards to IgM antibodies from suspected blood
sample is that measles vaccination as well as measles
infection both results in raised IgM antibodies; thus,
presence of measles IgM in those vaccinated with the
measles antigen 30 days before the sample is collected
does not imply disease but rather vaccination against
measles.[1,3,6,7] Furthermore, an outbreak of measles is
said to occur when there are at least 3 measles IgM
positive as confirmed by the laboratory in a health
facility or district within 1‑month.[8]
In spite of the increase in measles immunization coverage
aimed at building population immunity against the
disease, measles outbreaks still occur especially in the
developing countries; this ranks measles top among
the burden of vaccine‑preventable diseases across
the globe with worst picture seen in the developing
countries that are not unconnected to malnutrition and
overcrowding.[9‑11] The sporadic measles outbreaks seen
are often fatal with high morbidity and mortality in those
under the age of 5 years. Interrupting transmission of
this fatal disease requires an effort to achieve population
immunity of at least 95%.[1,3‑5] This calls for the need to
review the existing strategies for the control of this fatal
but preventable disease.[6,7,12,13]
As noted by Wolfson et al., though there is a reduction in
global deaths from measles in the past decade attributed
to increasing immunization rates and reduction in
measles case fatality ratios (CFRs), difficulties still arise
in estimating the level of measles deaths.[14] This is more
so looking at the fact that incidence‑based methods
of estimation are dependent on accurate measures of
the measles CFRs. Nonetheless, there are variations in
these ratios based on the geographic and epidemiologic
context yearly.
It is overwhelming to note that despite efforts by government
and partner agencies in the developing countries at
increasing immunization coverage, measles infection is still
the leading cause of mortality and morbidity in children
under the age of 5 years in Africa.[5,15] In 2010, there were
at least 139, 300 deaths globally attributed to measles; this
when translated further indicates about 380 deaths every
day and more precisely 15 deaths every hour.[5]
6 Sahel Medical Journal / January-March 2016 / Vol 19 | Issue 1
In 2008, the WHO in Africa region agreed on measles
elimination strategy targeting end of 2012. The aim
is to reduce measles incidence to <5 cases per 106
population per year across all the countries, increase
the first dose of measles‑containing vaccine 1 to >90%
nationally and >80% at district levels, improve on
measles surveillance system performance reporting
nonmeasles febrile rash illness rate of  ≥2  cases
per 100,000 population per year.[7]
There is no doubt that surveillance is a key in the
prevention of measles outbreak. The information
obtained from the epidemiologic surveillance guides
public health specialists and policy makers on how best
to plan for public health interventions, implement work
plans, and evaluate the effectiveness of intervention
programs.[16] The surveillance system for measles,
referred to as “measles case‑based surveillance,” is
a system that detects suspected measles cases and
outbreaks. The system works like other epidemiologic
surveillance systems through reporting and investigating
of suspected cases; the data is used for action such as
evaluating immunization efforts, age groups at risk,
and predicting outbreaks through the identification of
geographical areas.[3]
In Nigeria, measles case‑based surveillance started
in response to measles catch‑up supplementary
immunization activities (SIAs) in the Northern part
in the last quarter of 2005. However, the measles
case‑based surveillance was subsequently implemented
across the country after the SIAs in the Southern
states in late 2006. It is interesting to mention that a
total of 1,346 suspected measles cases were reported
since January 2007 with 196 laboratory‑confirmed
by the laboratory and or epidemiological linkage. Of
these confirmed cases, 62% were 1–4 years and 23%
aged 5–14 years. There is a need to emphasize that the
pattern of measles in Nigeria is predominantly among
the younger un‑immunized population due to immunity
gaps as a result of inadequate routine measles coverage
among others.[17]
It is disheartening to note that Nigeria is among the
45 countries that account for 94% of the global deaths
due to measles.[1,3‑5] While there is a paucity in the
literature in Nigeria on the population‑based prevalence
of measles, several studies from tertiary hospitals show
the prevalence of measles from pediatric admissions
stands at around 1.3–5.1%. [18‑22] Furthermore, the
reported CFRs for this disease in Nigeria showed some
variations ranging from 1.9% to 12.4%.[18‑22] In a study
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Saleh: Trends of measles in Nigeria: A systematic review
conducted by Onyiriuka in a secondary health center, in
a Southern Nigerian city, it was observed that measles
accounted for 3.1% of all pediatric admissions in the
hospital; this figure is higher than the 2.3% reported
in 1998 at a tertiary health center in the same city.[23,24]  et al. predicted expected measles cases in 2015 using
Etuk et al. also noted a rise in the prevalence of measles
in a tertiary health center, in a neighboring state.[19]
M E T H O D O L O GY / L I T E R AT U R E S E A R C H
STRATEGY
In the course of this write‑up, literature search related
to the topic was conducted through various electronic
databases such as PubMed, Medline, EBSCO, Africa
Journal Online, CINAHL for scientific journals for
nursing and allied subjects, Health Source on
Nursing/Academic Edition for literature and journals
with a focus on medical disciplines. The authors
searched for peer‑reviewed scholarly scientific articles
using Google search engine. In addition, publications
that relate to this study were accessed from the websites
of some international organizations such as the WHO,
UNICEF, USAID, UNFPA, UNDP, MDG, and GAVI.
Furthermore, lists of references from original research
publications and reports were also reviewed.
The list of search terms used in the literature search
includes measles, case‑based surveillance, outbreaks,
vaccination, and case fatality rates. Additional sources
of articles obtained and reviewed for this study were
electronically from professional journals.
There are various studies on the trend of measles, causes
of outbreaks, reasons for high vaccination dropout rates
by mothers, and lack of awareness on the benefits of
vaccination as a whole.[25,26] In an attempt to understand
the trend of measles in Nigeria, this retrospective review
examined peer‑reviewed articles on measles in Nigeria
and other studies conducted in some countries across
the globe.
Umeh and Ahaneku used a descriptive analysis of measles
case‑based surveillance data that were collected by the
WHO and the state MOH between 2007 and 2011 to
find out if there was any association between measles
immunization coverage and measles outbreak; the
inclusion criteria were all those that met the measles
diagnostic criteria of clinical confirmation or as confirmed
by the laboratory in the absence of measles vaccination.[27]
In an attempt to look at the epidemiology of measles in
South‑West Nigeria, Fatiregun, et al. analyzed measles
Sahel Medical Journal / January-March 2016 / Vol 19 | Issue 1
case‑based surveillance data from 2007 to 2012.[27] The
authors used a descriptive analysis (persons, place,
and time) of measles cases and which was confirmed
through laboratory and epidemiological link. Fatiregun
additive time series model. Furthermore, in a similar
study on trends and patterns of under‑fives vaccination
in Nigeria, using four National Demographic and Health
surveys datasets involving a total of 44,071 (weighted)
children from 1990 to 2008; the authors examined
child health information including the proportion
of those who had some or completed their routine
childhood vaccinations, the trends, as well as a pattern
of vaccination over 18 years.[29] The authors also selected
certain factors and regressed them to obtain predictors
of child vaccinations in Nigeria.
Considering the importance of timeliness and
completeness of reporting on all suspected infectious
diseases, a retrospective review of surveillance records
was conducted between January 1, 2007 and June 30,
2008. This was done by review of records of suspected
measles from the registers of 23 health facilities in
Nigeria. Odega et al. used a capture‑recapture method
to obtain an estimate of the total number of measles
cases required for the study area within the period
under review.[4] Completeness of reporting was by
calculating the ratio of a number of measles reported
by hospitals to the number of estimated cases using the
capture‑recapture method.[4]
Although there are safe and effective vaccines against
measles, measles remains a significant cause of
childhood morbidity and mortality in Nigeria.[30] In a
review conducted on the current status of measles in a
tertiary health center aimed at strengthening strategies
for intervention, a 10‑year retrospective study spanning
from 1994 to 2004 was conducted.
In another African country, Tunisia, Bahri et  al.[31]
assessed measles surveillance and control from 1979
to 2000; the authors analyzed measles epidemiology
in the country after the introduction of a specific
vaccine in 1979, as well as the results of the serological
investigation of suspected measles cases. Available data
on measles were used to examine the epidemiological
trend from 1979 to 2000. The criteria used include
reported cases, age, date reported, epidemiological link
with similar cases, and laboratory confirmation. The
serological investigation was based on the detection of
measles and rubella IgM using ELISA in 542 suspected
measles cases from 1997 to 2000.
7
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Saleh: Trends of measles in Nigeria: A systematic review
It is vital to estimate measles CFRs using a standardized
approach. Wolfson et al. in their effort to understand
variations in CFRs through review of community‑based
studies four reported age‑specific measles CFRs
published between 1980 and 2008. The authors used
cross‑referenced publications from the same area to
avoid inclusion of duplicate research considering the
time and place of the reported research. The exclusion
criteria include all hospital‑based studies (which are
likely to represent a biased sample in terms of severity),
research with reports on measles outbreaks either in
a refugee camp or internally displaced (are likely to
report on exceptional circumstances), and research
from developed countries (due to sustained measles
vaccination coverage).[14]
It is interesting to note that in spite of the incorporation of
the measles vaccine into routine immunization programs
in Europe over two decades ago, measles persists in the
continent.[32] This was shown in a study by Muscat
et  al. to evaluate measles using an epidemiological
assessment tool. The authors used case‑based data from
2006 to 2007 collected by the national surveillance
institutions submitted by the 32 European countries.[32]
In addition, data were obtained for age group, confirmed
diagnosis, vaccination status, hospital treatment, those
presented with acute encephalitis as a complication,
and those who died as a result of the disease. Cases
were separated based on age as well as graded countries
with indigenous measles incidence per 100,000
inhabitants per year. The data were analyzed based
on clinical diagnosis, laboratory‑confirmed cases, and
epidemiologically linked cases in accordance with the
requirements for national surveillance.[32] The authors
regarded indigenous case as those that not recorded
as imported from another country and also those with
unknown importation status.
In a related cross‑sectional survey of measles antibodies
in the Jiangsu Province of China[33] from 2008 to 2010
to evaluate the effect of high coverage with two doses
of measles vaccine among children, the researchers
were able to understand changes in the epidemiological
characteristics of measles in the Jiangsu Province since
2007. Using ELISA to measure serum level of measles-
specific IgG, Liu et al. noted that there is a high incidence
of measles across the province. This is in spite the over
95% immunization coverage with two doses of measles
vaccine in most regions of the province, there is a high
incidence of measles across the province.  In the study,
selection of participants was done such that the Jiangsu
Province was stratified into three regions to account for
8 Sahel Medical Journal / January-March 2016 / Vol 19 | Issue 1
geographical variations and socioeconomic status. Then
one city from each region was randomly sampled, and
individuals selected based on age and gender.[33]
RESULTS
Most of the researches on measles were centered on
theories that include the theory of planned behavior, the
health belief model, and social cognitive theory. This
helps researchers identify key behavioral, normative, and
control beliefs that affect human behaviors. The theoretical
constructs which the studies were based on contributed
in designing interventions that target audience, as well as
lead to changes in intentions and behaviors.[34,35]
It is clear from the various studies on the trend of
measles that most of the cases were from children who
were either not immunized with the measles vaccine or
had an incomplete course of the routine vaccination.
Furthermore, a greater number of the measles cases were
in those <59 months of age and imported from other
measles endemic countries with regards to cases seen
in Europe. The high mortality recorded was in those
with immunity gap due to either lack of immunization
with the measles vaccine or not completing the measles
vaccination program.[4,14,15,23,27‑31,33]
In a study conducted by Onyiriuka,[23] it is clear that
cases of measles accounted for 3.1% of all admissions
in the Pediatric Department, with the age distribution
as follows: 47.8% between 13 and 24 months of age;
18.1% were under 9 months old. Although 22.1% had
vaccination against measles, 77.9% were not vaccinated
against the disease. It was further observed that a
significant number of the cases occurred in the dry
season (80.5%) as compared to the wet season (19.5%) at
P < 0.001. In addition, the two main reasons shared by
the mothers for not immunizing their children against
the disease were child ill (35.0%) and child <9 months
old (23.3%). The author observed that the two leading
complications as a result of measles infection were
bronchopneumonia (55.1%) and diarrhea with
dehydration (13.0%).[23]
Looking at measles CFRs, Wolfson, et al. show from their
search of 58 publications of 102 different measles study
conducted in 29 countries, CFRs of measles are the
highest during outbreaks and among the unvaccinated
children of under the age of 5 years.[14]
Furthermore, lowest CFRs were seen among vaccinated
children regardless of the setting. It is important to
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Saleh: Trends of measles in Nigeria: A systematic review
mention that the period when these studies took place
is biased toward the beginning of the investigated
period. The majority of the research occurred in rural
areas of India, eight nationally representative, and
25 in urban areas. The authors critically examined
the research and came up with 38.24% retrospective
reviews, 31.37% outbreak investigations, and 30.39%
mainly community‑based surveys. The broad range of
the case and death definitions, study population and
geography highlight the complexities in extrapolating
results for global public health planning.[14]
The results of a study to assess coverage of measles
vaccination in Tunisia showed a gradual increase
in coverage of over 90%; this is consistent with the
decline in the annual reported measles cases thus
limiting frequency of outbreaks.[31] Bahri et al. added
that measles‑specific IgMs were detected in nine of the
patients that received vaccination against measles few
days prior blood collection, as well as anti‑rubella IgMs
were detected in 52% of cases.
The outcome of the 2‑year study conducted by
Muscat et al. shows that of the 12,132 cases of measles
recorded, 85% were from Romania, Germany, UK,
Switzerland, and Italy.[32] Nonetheless, majority were
children and either unvaccinated or could not complete
their vaccination, and about a fifth were at least 20 years
of age. The measles‑related deaths recorded during the
2‑year study were seven. The authors observed that
the high incidence of measles in some of the European
countries was because of suboptimum immunization
coverage. The statistics revealed that out of the 210
measles cases reported as being imported, 117 (56%)
were from European country and 43 (20%) from Asia.[32]
In an attempt to assess children immunized and later
presented with measles, Umeh and Ahaneku noted a
decrease from 81% in 2007 to 42% in 2011. Still, there
was an increase from two cases in 2007 to 53 cases in 2011
with laboratory confirmation; this reflects a remarkable
increase in the overall.[27] It is interesting to note that
75% of the laboratory‑confirmed cases were from rural
areas. Further analysis of the laboratory‑confirmed
measles cases show that 5 (7%) in those <9 months of
age, 48 (64%) in those between 9 and 59 months of age,
and 22 (29%) in those <59 months old.
It has been shown that there is a significant increase
in trend in seroprevalence yearly[33] (CMH χ2 = 40.32,
P < 0.0001); however, the seroprevalence among those
aged 2–15 years is consistently above 95%. This clearly
Sahel Medical Journal / January-March 2016 / Vol 19 | Issue 1
indicates the possibility of vaccine‑induced measles
antibodies waning out over time. Liu et  al. observed
that in 2010, the measles seropositivity in the Jiangsu
Province was 91.7% (95% confidence interval (CI):
90.1–93.2%). The seropositivity rate among those aged
15–29 years, the seropositivity rate was 88.4% (95% CI:
82.7–92.8%).[33]
As observed by Fatiregun et al., of the 10,187 suspected
measles cases investigated, there were 1,631 (16.0%)
confirmed cases.[28] This indicates a rise in annual
incidence from <1 case per million in 2007 to 23 cases
per million in 2011. Furthermore, of the cases confirmed
from six states in the zone, 97.4% were under the age of
20 years. They also noted that the peak of infection was
in the first two quarters of the year. The result shows
an increasing trend in the expected number of cases
based on the projection.
The result of the study by Ushie, Fayehun, and Ugal
shows that in 2008, vaccination was rather more
complete in children from educated mothers, who
were delivered in hospitals, who lived in urban areas,
and whose mothers were employed had significantly
higher chances of completing their routine vaccinations.
It was also observed that there was a low level of
childhood vaccination in the North when compared to
the Southern parts.[29]
In their study,[15] Fatiregun and Odega discovered from
the local government authority (LGA) records that
10% of the cases were older than 14 years as against
the 20% in the same age group found in the health
facility records. Furthermore, 53% of the cases from
the hospital records were from a single area as against
30% of the cases from the LGA records. The authors
conducted further analysis in relation to time, which
revealed that 30% of the cases in the LGA records
occurred in August 2007 while 20% of the hospital
cases were in February and May 2008. The authors
concluded that there was a considerable mismatch of
the two records based on the characteristics used in
the study.[15]
DISCUSSION
The findings from the various research show that
despite the availability of a vaccine that protects
eligible children from measles infection delivered
through routine immunization, Nigeria and some
other developing countries still record sporadic
outbreaks of measles infection.[7,14] However, these
9
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Saleh: Trends of measles in Nigeria: A systematic review
sporadic outbreaks are often fatal with high morbidity
and mortality especially in children under the age
of 5 years. Several researches both on the African
continent and beyond have shown that measles
disease in those immunized tends to be milder in
presentation with little or no complications. However,
greater burden with a wide range of complications and
increase mortality is seen among the un‑immunized
or those who could not complete their routine
immunizations.[4,14,15,23,27‑31,33]
Furthermore, severity of the measles infection is more
in those under 5 years of age as compared to other age
groups. In Nigeria, it is clear that the severity of the
measles disease is more in the Northern part when
compared with the Southern part of the country.[29] It
is disheartening to note that in spite of availability of
health facilities that offer routine immunizations, there
are a great number of parents who do not utilize these
services due to lack of awareness, poor educational
background of the parents, and poor socioeconomic
status, as well. There are areas in the Northern part of
the country that do not offer these services due to either
vaccine stock‑out or lack of logistical support to enable
them go on outreach or mobile services to access the
hard‑to‑reach areas.[8,29] This study further shows that
there is no precision in the values for measles CFRs,
thus creating uncertainties on the actual toll of measles
cases 4 and that the lower incidence of measles is seen
in those vaccinated.[14,23,36]
Despite the global efforts to vaccinate all eligible
children as early as 9 months of age, it is disheartening
to note that measles still remains one of the leading
causes of death among the under‑fives especially in
Sub‑Saharan African.[4,5] It is clear from the outcome
of several studies that measles outbreaks are associated
with factors that include: Weak measles case‑based
surveillance in some areas, lack of awareness about the
disease among parents, vaccine stock‑out, and lack of
adequate cold chain equipment to preserve the vaccine
in remote hard‑to‑reach areas.[6,7,14,17] In addition, there
is a lack of precision in extrapolating the values for
measles CFR further creating uncertainties on the actual
toll of measles cases,[14] or whether those vaccinated
with the antigen had lower incidence of measles.[14,23,36]
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
10 Sahel Medical Journal / January-March 2016 / Vol 19 | Issue 1
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