|Year : 2016 | Volume
| Issue : 1 | Page : 5-11
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
|Date of Web Publication||6-May-2016|
Jalal-Eddeen Abubakar Saleh
WHO Bauchi Zonal Office, Bauchi State
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
|How to cite this article:|
Saleh JEA. Trends of measles in Nigeria: A systematic review. Sahel Med J 2016;19:5-11
| Introduction|| |
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. , 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 to March. Measles carries with it high morbidity and mortality especially when clinical cases are not properly managed. 
The case fatality rate of measles in the developing countries is 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 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 remains one of the leading causes of death among the under-fives, especially in the Sub-Saharan African continent. ,
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. ,,, 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. 
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. ,, 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%. ,,, This calls for the need to review the existing strategies for the control of this fatal but preventable disease. ,,,
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.  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. , 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. 
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. 
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.  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. 
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. 
It is disheartening to note that Nigeria is among the 45 countries that account for 94% of the global deaths due to measles. ,,, 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%. ,,,, Furthermore, the reported CFRs for this disease in Nigeria showed some variations ranging from 1.9% to 12.4%. ,,,, In a study 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. , Etuk et al. also noted a rise in the prevalence of measles in a tertiary health center, in a neighboring state. 
| Methodology/Literature Search 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. , 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. 
In an attempt to look at the epidemiology of measles in South-West Nigeria, Fatiregun, et al. analyzed measles case-based surveillance data from 2007 to 2012.  The authors used a descriptive analysis (persons, place, and time) of measles cases and which was confirmed through laboratory and epidemiological link. Fatiregun et al. predicted expected measles cases in 2015 using 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.  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.  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. 
Although there are safe and effective vaccines against measles, measles remains a significant cause of childhood morbidity and mortality in Nigeria.  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.  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.
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). 
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.  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.  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.  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  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 geographical variations and socioeconomic status. Then one city from each region was randomly sampled, and individuals selected based on age and gender. 
| 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. ,
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. ,,,,,,,,,
In a study conducted by Onyiriuka,  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%). 
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. 
Furthermore, lowest CFRs were seen among vaccinated children regardless of the setting. It is important to 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. 
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.  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.  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. 
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.  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  (CMH χ2 = 40.32, P < 0.0001); however, the seroprevalence among those aged 2-15 years is consistently above 95%. This clearly 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%). 
As observed by Fatiregun et al., of the 10,187 suspected measles cases investigated, there were 1,631 (16.0%) confirmed cases.  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. 
In their study,  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. 
| 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. , However, these 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. ,,,,,,,,,
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.  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. , 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. ,,
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. , 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. ,,, 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,  or whether those vaccinated with the antigen had lower incidence of measles. ,,
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Conflicts of interest
There are no conflicts of interest.
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