Descriptive characterization of measles in Kebbi State, Nigeria, 2013-2017

Hashim Abdulmumin Bala^1,&, Mohammed Yahaya^1,2, Nyampa Barau¹, Lukman Surajudeen³, Ismail Raji Abdullateef¹, Charles Rahab Amaza^1,4

 

¹Nigeria Field Epidemiology and Laboratory Training Program, Abuja, Nigeria, ²College of Health Sciences, Usmanu Danfodiyo University Sokoto, ³World Health Organization, Birnin Kebbi, Kebbi State, Nigeria, ⁴Nigeria Centre for Disease Control (NCDC)

 

 

^&Corresponding author
Hashim Abdulmumin Bala, Nigeria Field Epidemiology and Laboratory Training Program, Abuja, Nigeria.

 

 

 

 

Measles is an acute viral infectious disease and an important cause of childhood morbidity and mortality. It is a highly infectious viral disease and is endemic in developing countries. In Nigeria, and some other countries in sub-Saharan Africa (SSA), measles has peak transmission from October to March [1-3]. In the early 2000s, measles was a leading cause of vaccine-preventable child mortality among under-fives [4].

 

Measles can be serious. Children younger than 5 years of age and adults older than 20 years of age are more likely to suffer from complications. Common complications are ear infections and diarrhoea. Serious complications include pneumonia encephalitis and death [5]. Long-term complications such as subacute sclerosing panencephalitis (SSPE) is a very rare, but fatal disease of the central nervous system that results from a measles virus infection acquired earlier in life [5].

 

As of January 2022, 254 cases of measles were confirmed in Nigeria. In 2020, there were over 9,000 such cases in the country. According to the World Health Organization (WHO), in 2018, about 140,000 people died from measles worldwide [6]. Many deaths were registered in countries with low-income and weak health facilities. Measles is considered one of the most contagious diseases [6].

 

Before a vaccine was available, measles infection was prevalent globally, especially during childhood. Presently, it is a very common and fatal disease in developing countries. The World Health Organization estimates there were 145,700 deaths globally from measles in 2013 [7]. Globally, an estimated 254,928 cases and 89,780 deaths occurred annually, and the case fatality ratio was about 0.1% in the developing world, and 0.05 to 6% in endemic countries, according to the WHO [8]. Measles is endemic in Nigeria and exhibits a seasonal pattern. More cases are seen during the dry season especially in the first half of the year, with peak transmission occurring between October and March [8]. The Nigerian Centre for Disease Control (NCDC) reported more than 22,000 suspected cases of measles since the beginning of 2019 [4]. It is a highly infectious viral disease and is endemic in developing countries with a peak of transmission from October to March [4]. The case fatality rate of measles in developing countries is around 3-5%, but it could be as high as 10% during epidemics [1]. Although natural infection with the measles virus confers life-long immunity, those vaccinated with the vaccine could get up to 10 years of protection [1].

 

Even though a safe and cost-effective vaccine is available, and even though the global vaccine coverage of children who received the measles vaccine by their first birthday is up to 85%, it remains a leading cause of death in children [9].

 

In Nigeria, measles case-based surveillance started in 2006 [10], following the measles vaccination catch-up campaign conducted nationwide in 19 states in Northern Nigeria and 17 states in Southern Nigeria in December 2005 and October 2006, respectively. There was a reduced incidence of measles. These campaigns offered the country an opportunity to introduce a case-based surveillance system involving case investigation and specimen testing [10,11]. Kebbi State like all other States in Nigeria, follows the IDSR guidelines, and uses IDSR tools and forms for their surveillance system.

 

Timely measles and rubella surveillance are critical to disease control. Identifying and confirming suspected measles and rubella cases through surveillance allows early detection of outbreaks, analysis of ongoing transmission to mount more effective vaccination measures and estimation of the underlying true incidence based on the patterns in reported data [11]. As of March 2023, the measles vaccine administrative coverage was reported to be about 128%.

 

Routine vaccination for children drastically reduces measles cases. Nonetheless, there has been a global resurgence of measles cases since 2018 which highlights the need for evaluating vaccine-induced immunity in an era of high vaccination coverage, especially among international travellers [12]. Despite substantial progress made toward global measles elimination since 2000, there has been a global resurgence of measles since 2018, and confirmed cases increased by 1.8 times in 2019, with Africa accounting for 55% of all measles cases worldwide [12]. Before the introduction of MCV in the 1960s, more than 2 million deaths occurred globally each year, and more than 95% of individuals had been infected with the measles virus by the age of 15 years [13]. As routine immunization coverage increased from 2000 to 2017, global coverage with the first dose of MCV among children of 1 year of age increased from 72% to 85% [14], and measles incidence decreased significantly [12].

 

Most Member States submit monthly reports on suspected and confirmed measles and rubella cases identified through their national disease surveillance systems to WHO. In general, the number of reported cases reflects a small proportion of the true number of cases occurring in the community. Many cases do not seek health care or, if diagnosed, are not reported [15].

 

The objectives of this study are to describe the distribution of measles cases reported in Kebbi State, by time, person, and place, to determine its trends, and to determine factors associated with the outcome status of measles cases in the State. These are with the view to providing a situation assessment of the spread of the disease in Kebbi State and informing policy that will promote a reduction in the number of reported cases in the years ahead [15].

 

 

Study setting

 

The study was carried out in Kebbi State, North-west Nigeria. Nigeria is the most populous country in Africa, with a population of 204,982,098 as of Monday, April 13, 2020, and a growth rate of 3.8% (12). We conducted a descriptive secondary data analysis from Kebbi State's weekly surveillance data. The data source was from the Epidemiology Unit of the Kebbi State Ministry of Health.

 

Kebbi is a state in the northwestern part of Nigeria; it was created out of Sokoto state on August 27^th 1991. It has 21 Local Government Areas (LGAs), 225 political wards, and 122 districts spread over four Emirate Councils namely Argungu, Gwandu, Yauri, and Zuru. The state is divided into three senatorial zones (North, Central, and South). Farming is the major occupation and Birnin Kebbi town is the state capital. The major ethnic groups in the LGA are Hausa, Fulani, Kabala, Fakkawa, and Zabarmawa. Seventy percent of the people live in rural communities, where the predominant economic activities are fishing, farming, and trading. The major religion is Islam, followed by Christianity. However, few groups of people practice African traditional religion. Like other Northern States in the country, the measles vaccine coverage in Kebbi State is generally low compared to their southern counterparts [16].

 

We reviewed all reported measles cases (both suspected and confirmed) in the IDSR for the period of 2013 to 2017. IDSR weekly epidemiological data for the years under review was obtained from epidemiology Unit, Kebbi State Ministry of Health, Nigeria.

 

Measles surveillance in Nigeria

 

Measles surveillance in Nigeria is through the IDSR platform. The IDSR is a national disease reporting platform, covering priority diseases from all health facilities across the country. Information flows from the health facilities, through the ward focal persons to the local government areas (LGA) disease surveillance and notification officers (DSNOs), to the State DSNOs, and then to the Federal Ministry of Health. Feedback goes in the opposite direction. The IDSR collects information on disease cases and deaths, facility location, and laboratory outcomes [1, 10].

 

Measles case definitions

 

Suspected case: any person with fever and maculopapular (non-vesicular) generalized rash and cough, coryza or conjunctivitis (red eyes), or any person in whom a clinician suspects measles.

 

Laboratory confirmed case: a suspected case with laboratory confirmation (positive serum IgM antibody for measles) [1, 10].

 

An epidemiologically linked or epidemiologically confirmed case is a suspected case, which has contact with a laboratory-confirmed case [1, 10].

 

Clinically confirmed: a case that meets the clinical case definition and for which no adequate blood specimen was taken [1, 10]. Discarded case: a suspected case that does not meet the clinical or laboratory definitions [1, 10]. Measles alert threshold: 5 or more suspected cases reported from an LGA/health facility in a month. Measles epidemic threshold: 3 or more measles IgM+ confirmed cases in an LGA/health facility in a month.

 

Data collection management

 

The data was collected in Microsoft Excel format, from January 2013 to December 2017

 

Each variable was clearly defined and coded to ensure a consistent definition of variables both from the data source and the study. Headings/labels were provided for each variable/information entered. The State data manager was consulted for any further clarifications required.

 

The LGA DSNOs and the State DSNO were constantly contacted to verify any missing information to minimize missing variables. Where missing data was not accounted for, we stated that as a limitation and was also factored in the analysis.

 

The same measures stated above were employed to ensure the internal validity of the data. Data cleaning and consistency checks were made to ensure internal validity. We used box plots to look for extreme values, which we verified from the data manager. For external validity, we recommended a thorough evaluation of the measles surveillance system in Kebbi State.

 

Data analysis

 

Descriptive analyses were conducted to describe the epidemiology of measles in Kebbi State in Time, Place, and Person. Graphs and charts were used to visually depict the data. Cross tabulations and Chi-square tests were used to find associations between variables. MS Excel was used for descriptive analyses. We used Epi info version 7.0 to conduct a bivariate analysis.

 

Availability of data and materials The data for this study are available at the hands of the corresponding author, and the data are not shared with any third party. The six-year AFP data reviewed for this study was obtained from the Epidemiology Unit of the Kebbi State Ministry of Health. Other information obtained was from the use of a self-administered questionnaire, as well as KIIs.

 

Ethical considerations

 

Ethics approval for this research work was granted by the Ethics and research committee of the Kebbi State Ministry of Health. Participants were adequately informed about the study, verbally. Confidentiality of their responses was assured; no personal identifiers were used on questionnaires.

 

The data was a property of the Kebbi State government which permitted us to use the data for a secondary data analysis. Ethics approval for this research work was granted by the ethics and research committee of the Kebbi State Ministry of Health (MOH/KBSREC/106/46/2019). Data was anonymised to ensure case privacy and preserve confidentiality.

 

 

The data collected from the surveillance system was 98% complete. Between January 2013 and December 2017, 9819 suspected measles cases were reported. Their ages ranged from 1 month to 59 years (the mean age was 4.5 ± 4.3 years). Most cases were below five years of age (72%, 7087/9819), followed by those within the 5-9 years´ age group (18%, 1781/9819). The least age group affected was 10-14 years (3%) (Figure 1).

 

Overall, between 2013 and 2017, there were more male (51%, 5052/9819) than female (49%, 4767/9819) suspected cases. However, in 2014 and 2017, more females were reported (51% and 52%, respectively).

 

Over the five study years, the highest number of cases were recorded in 2013 (71%, 7013/9819), and the lowest number of cases were reported in 2015 (4.2%, 415/9819).

 

During each of the five study years, most cases occurred during the first half of the year, with March having the highest number of cases (30.3%, 2974/9819) and December having the lowest number of cases (1%). The exception was in 2015 when most cases were reported between October and November.

 

All the local government areas (LGA) in Kebbi state reported suspected measles cases (Figure 2). Overall, Birnin Kebbi had the highest incidence of suspected cases (19%, 1855/9819), followed by Augie (10%, 997/9819) and then Gwandu (7%), Bagudo (7%), and Ngaski (7%). Zuru LGA had the least number of suspected cases (1%, 65/9819).

 

Most of the suspected cases had never received a single dose of measles vaccine (92%, 9081/9819) while only 72 cases (0.7%) had received at least 2 measles vaccine doses (Table 1).

 

Overall, only 21% (2108/9819) of the suspected cases had their blood samples collected for investigation (Table 2). Yauri had the highest proportion of cases whose blood samples were collected (62%, 184/298), with the least samples collected from Birnin Kebbi LGA (3%, 51/1855). The highest number of investigated cases per year was in 2016 (39%,), closely followed by 2017 (27%,), and the least was in 2014 (6%,).

 

The incidence rate was 831 per 100,000 (for age group 1-4 years), and 29.8 per 100,000 (for 15 years and above).

 

Suspected measles case fatalities and associated factors

 

A total of 121 deaths were recorded among the 9819 suspected cases, giving a case fatality rate of 1.2% (Table 3). Most deaths were among those less than the age of five years (48%, 58/121), and the least deaths were among those aged fifteen years and above (2%, 3/121). There were more deaths among males (53%, 64/121) than females (47%, 57/121). The highest mortality was recorded in 2014 at 5.3% (28/527) and the least was in 2016 at 0% (Table 3). Most of the deaths were reported among those who were never vaccinated (79%, 96/121), 4% among those who received only 2 doses, and no deaths were recorded among those who received more than 2 doses of the measles vaccine (Figure 3).

 

The overall case fatality rate during the study period was 1.2% (121/9819). The highest case fatality rate was found among the age group 5-9 years (3.0%, 52/1756) and the lowest was 0.8% (58/7505) among the less than 5 years´ age group.

 

The highest case fatality was reported in 2014 at 5% (28/555) and the least was in 2016 at 0% (Table 3). Sakaba LGA had the highest case fatality rate (8.4%), followed by Bagudo LGA (4%) while the least was recorded in Jega (0.0%) and Kalgo (0.0%) LGAs.

 

Both the age of the case and the number of measles vaccine doses received were found to be statistically significantly associated with the outcome of the cases. Cases who died were more likely to be aged less than 5 years (OR 3.59, 95% CI: 2.50-5.19) and to have never received any measles vaccine (OR 3.35, 95%CI: 2.1-5.2) (Table 4).

 

 

Measles cases can occur at any time of the year at varying degrees. In this review, cases of measles were found to occur in all the months of the year, with a peak incidence occurring during the first quarter of the year. This corresponds to the dry season in Kebbi State. There was however a study that describes the relationship between measles incidence and the cool dry season and the hot dry season [17]. Furthermore, it was shown that April and May are the months with the highest occurrence of measles cases. The relative risk of measles incidence is associated with high temperatures of 38-40°C and relative humidity of 19-30% within which the highest risk of measles prevalence is observed in the study area [17]. It was also revealed in another study in Ondo State, south-western Nigeria that High transmission of measles occurred from January to May during the dry season. This highlights the importance of the thermal environment in disease spread since it accounted for more than 40% variation in measles transmission within the study period [18]. This finding is also in line with similar findings in other regions, where most cases occur during the dry seasons [5, 19, 20]. However, this contrasted with findings in a different study, where most cases were prevalent during the last quarter of the year (38.5%), followed by the 1st quarter of the year (30.3%) of cases [20]. The different seasonal trends have been reported in other studies, in Taiwan [21], Ethiopia, Kenya, and Benin (WHO). Other studies in Nigeria [22-24] made similar observations. This seasonal variation in the incidence of measles may be attributed to the dry season which enhances the easy movement of infective droplets and transmission; the increased festivities promoted social interaction and consequently, the spread of measles. The implication is that healthcare providers should anticipate an increase in the number of cases of measles and prepare for their management during the dry season. This also entails public health authorities updating the health risk calendars and using the information to strengthen routine immunization program activities including vaccination ahead of the peak transmission season to prevent outbreaks of measles and other vaccine-preventable diseases.

 

However, this difference may be because this study was conducted in a tertiary hospital, it may not be a true representative of all the cases occurring within the community of which most cases were reported from PHCs [21].

 

Measles can be contracted at any age. Infants and children are often the only age groups affected by measles, but the disease also spreads among teenagers and adults. It was shown by the European CDC that a very high proportion of measles cases occur among those above 14 years of age (63% in 2014, 52% in 2015, 33% in 2016, and 45% in 2017) in some EU and EEA countries [21].

 

Findings from this study showed that most cases affected those below the age of five. This is a similar picture found in southwestern Nigeria and another similar study. [16,21,22] Similarly, a study in Lagos and another study in Niger state, revealed that 76% and 77% respectively of cases were below the age of 5 years [23] and [20]. While a study in Namibia shows that most of the confirmed cases were less than 10 years of age [24, 25]. The result is also aligned with findings from a systematic review of trends of measles in Nigeria where many of the cases were below 59 months [26], and in another study in the USA [27]. The 79.8% measles cases recorded in this study, in children 0-59 months is higher than what is reported in other developing countries such as 32% in Ethiopia [28] 15% in Kenya [28], and 46.5% in southwest Nigeria [29]. The reason for this variation seen from different parts of Africa may be attributed to variations in measles surveillance sensitivity, or logistics challenges involved in reaching populations that are over 80% rural with vaccines and other interventions. Furthermore, there is documented evidence of low vaccination coverage in the Northern parts of Nigeria, where Kebbi State is situated [1]. The high incidence of measles among the age group 0-5 years in this review could be attributed to low literacy level, low socio-economic reasons, overcrowding, poor access to healthcare facilities, and missed opportunities during routine immunization programmes [30].

 

The high prevalence of measles among the under-5s could have been due to the low immunization rate among the under-fives in Kebbi state. Between 2013-2017, there was no change in the age distribution of the suspected measles cases. This is like the study in southwestern Nigeria where measles surveillance data was analysed over 6 years [19]. Findings from these studies show that under-fives are the most prone to this infection, therefore there is a need to garner more efforts to ensure that the WHO recommendation that all children receive at least two measles doses by their second birthday is achieved. Countries that are not able to attain the recommended coverage of 95% in this target age group will get an accumulation of unvaccinated cohorts at the younger age groups and will have measles cases reported among children under five years of age. This occurrence of measles cases in under-fives is best addressed by optimizing routine immunization coverage and coverage for the second measles dose as part of supplementary immunization activities [31].

 

The present study shows that more males (51%) were affected than females (49%). This finding was consistent throughout the five years except in 2014 when more female cases were reported. This was in line with other findings in other regions [20, 27, 32]. Also, another study reported that the overall number of reported cases for the study period was marginally higher for males than females. However, in yet another study, findings revealed that more females (52.1%) were affected than males (47.9%) over 4 years (2006-2010), even though no statistically significant difference was found [33].

 

Historically, males have had higher case fatality rates than females [25]. An analysis of vital statistics data from several countries (primarily in the Americas and Europe) for the years 1950-1989 suggests that women and girls may have slightly higher mortality rates after measles than do men and boys but recent surveillance data from the United States and the United Kingdom show equal rates of complications for men and women. Pregnant women have an increased risk of complications, including death, following measles. [25]. In this study, mortality due to measles was found to be higher among males (53%) than females. This is a similar finding in other parts of Nigeria [32, 34].

 

Our current MCV coverage is 42% [34]. In this study, most of the suspected cases of measles reported never receiving a single dose of the measles vaccine. A similar pattern was seen in another study, where about 82% of suspected cases were unvaccinated against measles [35]. The overall prevalence of measles in this study shows a significantly higher infection rate (92%) among the unvaccinated populations compared to the 7% observed among the vaccinated populations. Low vaccination rates and increasing vaccine hesitancy, especially in low- and middle-income countries, contribute to the persistence of measles as a major cause of childhood morbidity and mortality. National-level MCV1 estimates from the Global Burden of Diseases, Injuries and Risk Factors Study (GBD) 2019 identified only 72 out of 204 countries in which routine coverage reached approximate herd immunity targets (≥95%) in 2019, and global MCV1 coverage [36]. Several studies have reported a higher proportion of cases among unvaccinated individuals. In Sub-Saharan Africa, the measles vaccine coverage is 70%, while that of Nigeria is 54% [16]. Fears and misconceptions are common reasons for low or non-vaccination found in a study conducted in SSA. Activities to improve vaccination coverage were identified, including structural reforms such as siting health centres within or proximal to target communities, improving female literacy, and conducting measles vaccination campaigns [16]. A recent study reported among 194 WHO member states, where less than half (47%) achieved ≥ 90% MCV1 coverage in 2021; however, among these countries, only 24 (26%) reported MCV1 coverage of ≥80% in all districts. In 2021, 24.7 million infants did not receive MCV1 through routine immunization services, an increase of 2.4 million (11%) from 2020. Nigeria was among the 10 countries with the highest number of infants who did not receive MCV1 (3.1 million), India (2.5 million), Democratic Republic of the Congo (1.7 million), Ethiopia (1.7 million), Indonesia (1.2 million), Pakistan (1.2 million), Philippines (1.0 million), Angola (0.8 million), Brazil (0.7 million), and Tanzania (0.5 million). These countries accounted for 59% of all children who did not receive MCV1 [37].

 

In Europe, case-based surveillance studies showed that 40% in 2005, 68% in 2006, and 80% in 2007 of cases were among unvaccinated populations indicating immunity gaps [33]. In the United States of America, 89% was reported among unvaccinated individuals [38]. However, the 34.4% observed among vaccinated individuals in the study is very high considering the acceptable measles vaccine failure rate of 2-10% [39] and may be attributed to a failure in seroconversion due to several factors such as vaccine failure, improper handling, and poor cold chain maintenance, use of inappropriate route and dosage, none use of indigenous virus strains in the formulation and production of these vaccines and none adherence to appropriate age to be vaccinated, missed opportunities [38].

 

The World Health Organisation (WHO) has lamented that Nigeria accounts for the highest cases of measles on the globe [37]. The CFR seen in this study is lower than that recorded in the past for Nigeria [40], this is probably due to an increase in the immunization coverage generally. Also, the CFR is lower among other hospital-based reviews seen in some other reviews [23, 34, 41]. This can, however, be explained by the fact that cases seen in the hospitals are usually severe cases, hence with higher CFRs. In 2010, the World Health Assembly established 3 milestones towards the future eradication of measles to be achieved by 2015: (i) Increase routine coverage with the first dose of measles-containing vaccine (MCV1) by more than 90% nationally and more than 80% in every district, (ii). reduce and maintain annual measles incidence to less than 5 cases per million: and (iii). reduce estimated measles mortality by more than 95% from the 2000 estimate. By 2018, the global push to improve vaccine coverage resulted in a 73% reduction in deaths. During 2000- 2018, with support from the Measles & Rubella Initiative and Gavi, the Vaccine Alliance, measles vaccination prevented an estimated 23.2 million deaths; most of the deaths averted were in the African region and countries supported by the Gavi Alliance [42].

 

An association between outcome status and age of onset has been established in this study. Also, an association between the doses of vaccine received and the outcome was observed. The association between measles death with age under five years and not being vaccinated as reported in the present study aligns with observations in countries that have not optimized coverage for the two doses of measles within the first two years of childhood, where the bulk of measles cases are reported in infants and preschool children [31]. These, however, have one probable explanation, which is a result of the number of doses of MCV received. Those under the age of 5 years have probably received a smaller number of doses of MCV compared to other groups. This has been demonstrated in several studies [43-45].

 

Study limitations The study utilised secondary data, so we had little or no control over the information given to us.

 

Some data was missing, like vaccine status, which we had to factor into our analysis

 

We had challenges retrieving a lot of missing data. Sometimes we had to review IDSR forms to verify some information and retrieve some of the missing data, which was herculean.

 

 

This study confirms the endemicity of measles in Kebbi State. It showed that Birnin Kebbi, Augie, and Gwandu LGAs had the highest rate of reported measles cases in the State. Low measles vaccination coverage is a likely reason for the increased measles case reporting rate in the most affected LGAs. Increase community sensitization and mobilization by the State government on the need for measles vaccination should be intensified. Using the available required data inputs and routinely collected data from the immunization and surveillance programs, as well as the trends of measles seen from this study, informed decisions can be made by the State government towards improving vaccination coverage in the State. There is also a need to improve the surveillance system through improving reporting to 100%.

 

 

The authors declare no competing interests.

 

 

HAB (Principal author): proposed, designed, and implemented the study, did the analysis and writing up of the manuscript. YM, RI, and BN made significant contributions to the conception and design of the proposal, analysis, and interpretation of data. They also critically edit and approved the final manuscript. LS and RCA participated greatly in the cleaning and analysis of data, QGIS design. All authors read and approved the final manuscript.

 

 

The authors acknowledged the support of the following organizations and distinguished personalities for their support and contributions towards this work; African Field Epidemiology Network (AFENET), Nigerian Field Epidemiology and Laboratory Training Program (NFELTP), Kebbi State Ministry of Health, Dr. Celestine Ameh, Dr. Chukwuma Umeokonkwo.

 

 

Table 1: Distribution of cases based on the number of doses received, Kebbi State, 2013-2017

Table 2: Distribution of suspected measles cases that were investigated between 2013 and 2017 in Kebbi State

Table 3: Outcome status of suspected measles cases per year, in Kebbi State, 2013-2017 (N=9,819)

Table 4: Factors associated with outcome status among suspected measles cases in Kebbi state between 2013 and 2017

Figure 1: Age distribution of suspected measles cases between 2013 and 2017 in Kebbi state

Figure 2: Distribution of suspected measles cases in Kebbi State between 2013 and 2017

Figure 3: Distribution deaths based on the number of doses received

 

 

1. Ibrahim BS, Usman R, Mohammed Y, Ahmed ZD, Okunromade O, Abubakar AA, Nguku PM.Burden of measles in Nigeria: a five-year review of case-based surveillance data, 2012-2016 . Pan Afr Med J [Internet]. 2019 Jan 22 [cited 2025 Mar 3];32(1):5. https://doi.org/10.11604/pamj.supp.2019.32.1.16169 PubMed | Google Scholar


2. Mandomando I, Naniche D, Pasetti MF, Cuberos L, Sanz S, Vallès X, Sigauque B, Macete E, Nhalungo D, Kotloff KL, Levine MM, Alonso PL. Assessment of the epidemiology and burden of measles in southern Mozambique . The American Society of Tropical Medicine and Hygiene [Internet]. 2011 Jul 1 [cited 2025 Mar 3];85(1):146-51. https://doi.org/10.4269/ajtmh.2011.10-0517 Purchase or subscription required to view full text. PubMed | Google Scholar


3. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, Rudan I, Campbell H, Cibulskis R, Li M, Mathers C, Black RE. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000 . The Lancet [Internet]. 2012 May 10 [cited 2025 Mar 3];379(9832):2151-61. https://doi.org/10.1016/S0140-6736(12)60560-1 Erratum in: Corrected: Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. The Lancet [Internet]. 2012 Oct 13 [cited 2025 Mar 24];380(9850):1308. https://doi.org/10.1016/S0140-6736(12)61762-0 Purchase or subscription required to view full text. Google Scholar


4. Portnoy A, Jit M, Ferrari M, Hanson M, Brenzel L, Verguet S.Estimates of case-fatality ratios of measles in low-income and middle-income countries: a systematic review and modelling analysis. The Lancet Global Health [Internet]. 2019 Feb 20 [cited 2025 Mar 3];7(4):e472-81. https://doi.org/10.1016/S2214-109X(18)30537-0 PubMed | Google Scholar


5. CDC. Measles — United States, January 4-April 2, 2015 . MMWR [Internet]. 2015 Apr 17[cited 2025 Mar 3]; 64(14):373-376. PubMed | Google Scholar


6. CDC. Measles Outbreaks and Progress Toward Measles Preelimination --- African Region, 2009—2010. MMWR [Internet]. 2011 Apr 1[cited 2025 Mar 3];60(12):374-378. Google Scholar


7. CDC. Epidemiology and Prevention of Vaccine-Preventable Diseases [Internet]. 14th ed. Hall E, Patricia Wodi P, Jennifer Hamborsky J, Valerie Morelli Sarah Schillie VMS, editors. Atlanta (GA): Public Health Foundation; 2021 Aug [cited 2025 Mar 3]. 358 p. Google Scholar


8. Elimian KO, Ochu CL, Ilori E, Oladejo J, Igumbor E, Steinhardt L, Wagai J, Arinze C, Ukponu W, Obiekea C, Aderinola O, Crawford E, Olayinka A, Dan-Nwafor C, Okwor T, Disu Y, Yinka-Ogunleye A, Kanu NE, Olawepo OA, Aruna O, Michael CA, Dunkwu L, Ipadeola O, Naidoo D, Umeokonkwo CD, Matthias A, Okunromade O, Badaru S, Jinadu A, Ogunbode O, Egwuenu A, Jafiya A, Dalhat M, Saleh F, Ebhodaghe GB, Ahumibe A, Yashe RU, Atteh R, Nwachukwu WE, Ezeokafor C, Olaleye D, Habib Z, Abdus-Salam I, Pembi E, John D, Okhuarobo UJ, Assad H, Gandi Y, Muhammad B, Nwagwogu C, Nwadiuto I, Sulaiman K, Iwuji I, Okeji A, Thliza S, Fagbemi S, Usman R, Mohammed AA, Adeola-Musa O, Ishaka M, Aketemo U, Kamaldeen K, Obagha CE, Akinyode AO, Nguku P, Mba N, Ihekweazu C. Descriptive epidemiology of coronavirus disease 2019 in Nigeria, 27 February-6 June 2020 . Epidemiol Infect [Internet]. 2020 Sep 11 [cited 2025 Mar 3];148:e20. https://doi.org/10.1017/S095026882000206X PubMed | Google Scholar


9. Ozawa S, Mirelman A, Stack ML, Walker DG, Levine OS.Cost-effectiveness and economic benefits of vaccines in low- and middle-income countries: A systematic review. Vaccine [Internet]. 2012 Nov 8 [cited 2025 Mar 3];31(1):96-108. https://doi.org/10.1016/j.vaccine.2012.10.103 Google Scholar


10. Isere EE, Fatiregun AA. Measles case-based surveillance and outbreak response in Nigeria; an update for clinicians and public health professionals. Ann Ib Postgrad Med [Internet]. 2014 Jun [cited 2025 Mar 3];12(1):15-21. Google Scholar


11. Orenstein WA, Hinman AR. Measles: the burden of preventable deaths. The Lancet [Internet]. 2012 Apr 24 [cited 2025 Mar 3];379(9832):2130-1. https://doi.org/10.1016/S0140-6736(12)60638-2 Purchase or subscription required to view full text. Google Scholar


12. Lee YC, Lee YH, Lu CW, Cheng SY, Yang KC, Huang KC.Measles immunity gaps in an era of high vaccination coverage: A serology study from Taiwan. Travel Medicine and Infectious Disease [Internet]. 2020 Jun 20 [version of record 2020 Jun 27; cited 2025 Mar 3];36:101804. https://doi.org/10.1016/j.tmaid.2020.101804 Google Scholar


13. Nishiura H, Kayano T, Kinoshita R. Overcoming the difficulty of achieving elimination status for measles and rubella due to imported infections: Estimation of the reproduction number R for measles and rubella. Travel Medicine and Infectious Disease [Internet]. 2019 May 8 [version of record 2019 Aug 5; cited 2025 Mar 3];30:137-8. https://doi.org/10.1016/j.tmaid.2019.05.004 Purchase or subscription required to view full text. Google Scholar


14. Zhao S.Epidemiology of an unexpected measles outbreak in Hong Kong, from March to April, 2019. Travel Medicine and Infectious Disease [Internet]. 2019 Jun 15 [version of record 2019 Aug 5; cited 2025 Mar 3];30:133-6. https://doi.org/10.1016/j.tmaid.2019.06.002 Purchase or subscription required to view full text. Google Scholar


15. WHO. Immunization Analysis and Insights Geneva, Switzerland [Internet]. Geneva (CH): WHO; c2025 [cited 2025 Mar 3].


16. Majekodunmi OB, Oladele EA, Greenwood B. Factors affecting poor measles vaccination coverage in sub-Saharan Africa with a special focus on Nigeria: a narrative review . Transactions of The Royal Society of Tropical Medicine and Hygiene [Internet]. 2022 Mar 16 [cited 2025 Mar 3];116(8):686-93. https://doi.org/10.1093/trstmh/trac013 Purchase or subscription required to view full text. Google Scholar


17. Akinbobola A, S. Hamisu A. Predicting measles occurrence using some weather variables in Kano, North Western Nigeria . AJPHR [Internet]. 2018 Aug 3 [cited 2025 Mar 3];6(4):195-202. https://doi.org/10.12691/ajphr-6-4-4


18. Omonijo AG, Matzarakis A, Oguntoke O, Adeofun CO.Effect of thermal environment on the temporal, spatial and seasonal occurrence of measles in Ondo state, Nigeria. Int J Biometeorol [Internet]. 2011 Sep 18 [cited 2025 Mar 3];56(5):873-85. https://doi.org/10.1007/s00484-011-0492-8 Purchase or subscription required to view full text. Google Scholar


19. Fatiregun AA, Adebowale AS, Fagbamigbe AF. Epidemiology of measles in Southwest Nigeria: an analysis of measles case-based surveillance data from 2007 to 2012 . Transactions of The Royal Society of Tropical Medicine and Hygiene [Internet]. 2014 Jan 28 [cited 2025 Mar 3];108(3):133-40. https://doi.org/10.1093/trstmh/tru004 Purchase or subscription required to view full text. Google Scholar


20. Adeboye M, Adesiyun O, Adegboye A, Eze E, Abubakar U, Ahmed G, Usman A, Amos S, Rotimi B. Measles in a tertiary institution in bida, niger state, nigeria: prevalence, immunization status and mortality pattern. OMJ [Internet]. 2011 Mar 25 [cited 2025 Mar 3];26(2):114-7. https://doi.org/10.5001/omj.2011.28 PubMed | Google Scholar


21. Chen CJ, Lin TM, Yeh YL. Analysis of the secular trend and seasonal variation of measles mortality rate in Taiwan [abstract]. Ann Acad Med Singap [Internet]. 1984 Apr [cited 2025 Mar 3];13(2):136-41. Google Scholar


22. Ogunmekan DA, Bracken P, Marshall WC.A seroepidemiological study of measles infection in normal and handicapped persons in Lagos, Nigeria [abstract]. J Trop Med Hyg [Internet]. 1981 Aug 1 [cited 2025 Mar 3];84(4):175-8. Google Scholar


23. Akande TM. A review of measles vaccine failure in developing countries . Nig Med Pract [Internet]. 2007 [cited 2025 Mar 3];52(5):112-6. https://doi.org/10.4314/nmp.v52i5.28917 Purchase or subscription required to view full text. Google Scholar


24. CDC. Progress toward measles elimination – European Region, 2009-2018 . MMWR Morb Mortal Wkly Rep [Internet]. 2019 May 3 [cited 2025 Mar 3];68(17):396-401. https://doi.org/10.15585/mmwr.mm6817a4 PubMed | Google Scholar


25. Crentsil SL, Nyarko K. Trends of measles in Namibia, a secondary data analysis: 2012-2015 [abstract]. PAMJ Conference Proceedings [Internet]. 2017 Oct 26 [cited 2025 Mar 3];1(3):73. https://doi.org/10.11604/pamj-cp.2017.3.73.171


26. Saleh JE. Trends of measles in Nigeria: A systematic review . Sahel Med J [Internet]. 2016 Jan-Mar [cited 2025 Mar 4];19(1):5-11. http://doi.org/10.4103/1118-8561.181887


27. Perry RT, Halsey NA. The clinical significance of measles: a review. Orenstein WA, editor. The Journal of Infectious Diseases [Internet]. 2004 May 1 [cited 2025 Mar 4];189(Supplement_1):S4-16. https://doi.org/10.1086/377712 Purchase or subscription required to view full text. PubMed | Google Scholar


28. WHO. New measles surveillance data for 2019 [internet]. Geneva (CH): WHO; 2019 May 15 [cited 2025 Mar 3]; [about 6 screens].


29. Adewumi MO. Neutralizing antibodies against poliovirus serotypes among children in southwest Nigeria . Journal of Tropical Pediatrics [Internet]. 2005 Jul 13 [cited 2025 Mar 4];52(2):92-5. https://doi.org/10.1093/tropej/fmi075 Purchase or subscription required to view full text.


30. Adeoye I, Dairo M, Adekunle L, Adedokun H, Makanjuola J. Investigation of a measles outbreak in a Rural Nigerian community-The Aladura experience . African Journal of Microbiology Research [Internet]. 2010 Mar 4 [cited 2025 Mar 4];4(5):360-6. Google Scholar


31. World Health Organization. Measles vaccines: WHO position paper - April 2017=Note de synthèse de l´OMS sur les vaccins contre la rougeole- avril 2017. Weekly Epidemiology Record [Internet]. 2017 Apr 28 [cited 2025 Mar 3];92 (17): 205-228. Available from: English, French. WHO Reference Number: WER N° 17, 92, 205-227. Download PDF to view full text. Google Scholar


32. Oyefolu AOB.Measles morbidity and mortality trend in nigeria: a 10-year hospital-based retrospective study in Lagos State, Nigeria. Journal of Microbiology and Infectious Diseases [Internet]. 2016 Mar 1 [cited 2025 Mar 4];6(1):12-18. https://doi.org/10.5799/jmid.328761 Download PDF to view full text. Google Scholar


33. Rammohan A, Awofeso N, Iqbal K. Gender differentials in the timing of measles vaccination in rural India . DemRes [Internet]. 2014 Jun 11 [cited 2025 Mar 4];30(67):1825-48. https://doi.org/10.4054/DemRes.2014.30.67 Download PDF to view full text. Google Scholar


34. Sule Ujah J. Women Empowerment in Nigeria Issues, Prospects and Challenges. KSUJPA. 2012 Jan; 1(2): 213-220. Google Scholar


35. Onyiriuka A. Clinical profile of children presenting with measles in a Nigerian secondary health-care institution. JIDI [Internet]. 2011 Jun 30 [cited 2025 Mar 4]; 3(6): 112-16. https://doi.org/10.5897/JIDI.9000012 Download PDF to view full text. Google Scholar


36. McLean HQ, Fiebelkorn AP, Temte JL, Wallace GS, Centers for Disease Control and Prevention. Prevention of measles, rubella, congenital rubella syndrome, and mumps, 2013: summary recommendations of the Advisory Committee on Immunization Practices (ACIP) . MMWR Recomm Rep [Internet]. 2013 Jun 14 [cited 2025 Mar 3];62(RR04):1-34. Erratum in: Erratum: Vol. 62, No. RR-4 . MMWR Recomm Rep [Internet]. 2015 Mar 13 [cited 2025 Mar 3]; 64(09):259-259. PubMed | Google Scholar


37. Minta AA, Ferrari M, Antoni S, Lambert B, Sayi TS, Hsu CH, Steulet C, Gacic-Dobo M, Rota PA, Mulders MN, Wimmer A, Bose AS, O'Connor P, Crowcroft NS. Progress Toward Measles Elimination — Worldwide, 2000-2023 . MMWR Morb Mortal Wkly Rep [Internet]. 2024 Nov 14 [cited 2025 Mar 3];73(45):1036-1042. http://dx.doi.org/10.15585/mmwr.mm7345a4


38. WHO. Immunization Analysis and Insights [Internet]. Geneva (CH): WHO; c2025. WHO/UNICEF estimates of national immunization coverage; [cited 2025 Mar 3]. Google Scholar


39. Troiano G, Nardi A. Vaccine hesitancy in the era of COVID-19 . Public Health [Internet]. 2021 Mar 4 [version of record 2021 May 7; cited 2025 Mar 4];194:245-51. https://doi.org/10.1016/j.puhe.2021.02.025 PubMed | Google Scholar


40. CDC. Measles outbreaks and progress towards meeting measles pre-elimination goals. Morb Mortal Wkly Rep [Internet]. 2011 Apr 1 [cited 2025 Mar 3]; 60(12);374-378. Google Scholar


41. Etuk I, Ekanem E, Udo J. Comparative analysis of measles morbidity and mortality in calabar during the expanded programme on immunization and the national programme on immunization eras . Nig J Paed [Internet]. 2004 May 26 [cited 2025 Mar 4];30(3):81-5. https://doi.org/10.4314/njp.v30i3.12070 Download PDF to view full text. Google Scholar


42. WHO. Measles: Key facts [Internet]. Geneva (CH): WHO; 2024 Nov 14 [cited 2025 Mar 3]. Google Scholar


43. Marin M, Nguyen HQ, Langidrik JR, Edwards R, Briand K, Papania MJ, Seward JF, LeBaron CW. Measles transmission and vaccine effectiveness during a large outbreak on a densely populated island: implications for vaccination policy . Clinical Infectious Diseases [Internet]. 2006 Feb 1 [cited 2025 Mar 4];42(3):315-9. https://doi.org/10.1086/498902 Subscription or purchase required to view full text. Google Scholar


44. Ernest SK. Measles in ilorin: an epidemic in the middle of eradication plans . Af J Clin Exp Micro [Internet]. 2004 May [cited 2025 Mar 4];5(2):203-7. https://doi.org/10.4314/ajcem.v5i2.7378 Google Scholar


45. Velicko I, Müller LL, Pebody R, Gergonne B, Aidyralieva C, Kostiuchenko N, Spika JS. Nationwide measles epidemic in Ukraine: The effect of low vaccine effectiveness. Vaccine [Internet]. 2008 Dec 9 [cited 2025 Mar 4];26(52):6980-5. https://doi.org/10.1016/j.vaccine.2008.09.012 Subscription or purchase required to view full text. Google Scholar