Progress towards elimination of measles in Kenya, 2003-2016

Introduction Measles is targeted for elimination in the World Health Organization African Region by the year 2020. In 2011, Kenya was off track in attaining the 2012 pre-elimination goal. We describe the epidemiology of measles in Kenya and assess progress made towards elimination. Methods We reviewed national case-based measles surveillance and immunization data from January 2003 to December 2016. A case was confirmed if serum was positive for anti-measles IgM antibody, was epidemiologically linked to a laboratory-confirmed case or clinically compatible. Data on case-patient demographics, vaccination status, and clinical outcome and measles containing vaccine (MCV) coverage were analyzed. We calculated measles surveillance indicators and incidence, using population estimates for the respective years. Results The coverage of first dose MCV (MCV1) increased from 65% to 86% from 2003-2012, then declined to 75% in 2016. Coverage of second dose MCV (MCV2) remained < 50% since introduction in 2013. During 2003-2016, there were 26,188 suspected measles cases were reported, with 9043(35%) confirmed cases, and 165 deaths (case fatality rate, 1.8%). The non-measles febrile rash illness rate was consistently > 2/100,000 population, and “80% of the sub-national level investigated a case in 11 of the 14 years. National incidence ranged from 4 to 62/million in 2003-2006 and decreased to 3/million in 2016. The age specific incidence ranged from 1 to 364/million population and was highest among children aged < 1 year. Conclusion Kenya has made progress towards measles elimination. However, this progress remains at risk and the recent declines in MCV1 coverage and the low uptake in MCV2 could reverse these gains.


Introduction
Elimination of measles is defined as the absence of endemic measles cases in a country or region for ≥12 months while under adequate surveillance [1][2][3]. Measles has been successfully eliminated in the Americas [4]. All other World Health Organization (WHO) regions have set elimination goals for measles. In 2011, the WHO African Region (AFR) adopted a measles elimination goal to be reached by the end of 2020 [5]. Activities for measles control and elimination include routine immunization (RI), supplemental immunization activities (SIAs), case management, outbreak response, and surveillance [5]. RI builds protection against measles virus by providing two doses of a measles-containing vaccine (MCV) to infants aged 9-18 months [6]. SIAs are immunization campaigns targeting children in a defined age group in a specified geographical area. SIAs provide a second opportunity for measles immunization in children not reached by RI or those not seroconverting after routine immunization [7,8]. "Catch-up" SIAs are usually the initial campaigns conducted, targeting children aged 9 months through 14 years, with the aim to achieve high population immunity quickly and interrupt measles transmission, while "follow-up" SIAs are conducted at regular intervals, usually 3-4 years, among children aged <5 years, to reduce accumulation of susceptible children [9].
The WHO Africa Regional Office (AFRO) has established measles elimination indicators, including: 1) measles incidence <1 case per million population at national level; 2) ≥95% MCV1 coverage in RI at national and at sub-national levels; 3) 95% coverage in measles SIAs and outbreak response immunization activities (ORI); 4) ≥80% of districts (sub-national levels) investigating one or more suspected measles cases within a year; and 5) reported non-measles febrile rash illness rate of ≥2 per 100,000 population at national level [5].
In Kenya, the Expanded Program on Immunization (EPI) was started in 1980 with the first dose of measles-containing vaccine (MCV) or MCV1 given at 9 months of age. Accelerated control for measles was started in 2002 when the first catch-up SIA that targeted children aged 9 months to 14 years was conducted, followed by periodic SIAs and the establishment of a case-based surveillance for measles with laboratory confirmation. In addition, the Reach Every District approach has been implemented in the country since 2003 to improve RI coverage. With the promulgation of the new constitution in 2010, Kenya adopted a decentralized government and replaced the eight provinces and existing districts with 47 semi-autonomous counties. In 2013, health services were fully decentralized to the counties to run the devolved functions, following the election of governors. Measles case-based surveillance therefore shifted from being district-reported to county-reported. A second dose of MCV (MCV2) was introduced in 2013 and is recommended for children aged 18 months [10]. Kenya developed a national measles elimination strategic plan 2012-2020 as a road map for eliminating measles transmission. This analysis aims to describe measles immunization performance, the surveillance performance against WHO standards, the epidemiology of measles cases in Kenya and to track the progress towards elimination of measles.

Methods
We conducted a review of RI data, SIAs data and the Kenya linked to a confirmed case when the patient has had contact with or lives in the same locality as a person with laboratory-confirmed measles infection. A suspect case is clinically-compatible when it meets the clinical case definition but a laboratory test or an epidemiological link are is lacking [11,12]. For this analysis, we included all laboratory-confirmed, epidemiologically linked, and clinically compatible measles cases as confirmed measles cases.
Microsoft Excel was used for managing and cleaning the database for analysis. Variables analyzed included age, sex, immunization status, date of rash onset, date seen at facility, date of notification, specimen quality, duration of processing, laboratory results, county of origin, and outcome. Analysis was done using Epi-Info 7, and maps were generated with Arc GIS Version 10.0. Surveillance indicators were calculated in accordance with WHO standard guidelines. They included the following: 1) national-level nonmeasles febrile rash illness (NMFRI) rate (target of ≥2 NMFRI cases per 100,000 population); 2) proportion of sub-counties reporting one or more rash illness case per year (target ≥80% sub-county units); 3) timeliness of specimen arrival to laboratory (defined as

Case-based surveillance indicators:
During the study period, the national non-measles febrile rash illness (NMFRI) reporting rate was ≥2 cases per 100,000 persons all 14 years, and the proportion of counties investigating >one suspect case per year was ≥80% in all but 3 years (Table 1). A high proportion of suspected measles cases were investigated with collection of an adequate serum specimen for laboratory testing. However, there was delay in transportation of collected samples to the laboratory within the targeted period (≤3 days), and there was delay in reporting of laboratory results to the sub-national levels ( Table 1). The proportion of discarded cases remained constant over the years including the years with outbreaks ( Figure 2). The overall incidence for the 14-year period was >5 cases/million; annual incidence ranged from 2-65 cases/million persons (Table 2, Figure 2). There were no significant differences in measles incidence by gender. The highest incidence rates occurred among infants aged <1 year This finding is consistent with findings in Nigeria and Democratic Republic Of Congo, where outbreaks have been observed due to sub-optimal coverage in MCV and SIA [13,14] and in Zambia, where after a successful SIA a resurgence of cases was observed after 3 years [15]. Experience from the United States indicate that coverage of >90% with two MCV doses are required to end transmission of measles [16].  [17]. Interventions such as sending out text message reminders to mothers can be used to improve the uptake [18,19]. In addition, health workers at the immunization service reported cases and may result in missed cases in the community not seeking health services. However, this analysis was conducted on data from a national population-based surveillance system with laboratory confirmation of cases, and it therefore represents the best assessment of the country's burden of measles disease.

Conclusion
In conclusion, although there is evidence of progress towards elimination of measles in the country, the relatively stagnant MCV1 coverage and the low uptake of MCV2 could reverse these trends.
Efforts to improve MCV1 coverage, strengthen MCV2 uptake, and target high-risk areas (age groups and counties with the higher incidence) need to be put in place. In addition, the Kenya immunization program should work with the county health departments to ensure that challenges in vaccination services are addressed. The indicators show that the surveillance system has performed well over the years; however, there is need to strengthen the system to ensure completeness of information collected and improve the effectiveness of laboratory services. Additionally, there is need to identify counties with weak performance for targeted interventions by the surveillance unit. Incompleteness of information may have led to incorrect estimates and follow up should be made to identify where the gaps are, either at the level of data entry at national level or at the health facility during case notification.

What is known about this topic
 Measles is a vaccine preventable disease that is targeted for elimination by 2020;  High vaccination coverage with at least two doses of measles containing vaccine are required to eliminate measles.      [1] IR is Incidence Rate, calculated by dividing the number of confirmed cases by population estimate for the year and multiplied by 1,000,000 2 Confirmed cases include laboratory-confirmed, epidemiologically confirmed and clinical-compatible case 3 Vaccination status data on parentheses is percentage