The above data clearly portray that measles is still far from the goal of eradication in Lebanon. Lebanon has witnessed several measles outbreaks in the past 20 years with a case fatality rate of 2 per 1000 reported cases. During 1997 and 1998 a first major outbreak took place in the North reporting 980 cases of measles out of which 3 cases were fatal and was followed by annual epidemic waves occurring between 2003 and 2007. In 2013, a second major national outbreak lasting for 31 weeks was recorded with a total of 2025 suspected cases being reported. Following thorough case investigation, 1760 cases were classified as measles, 27 as rubella, and 238 were discarded as non-measles and non-rubella. [10]
In Figure 1, children aging between 1 and 4 years are the most susceptible individuals to contract measles. Early in life, children usually acquire passively transferred maternal antibodies providing them with immunity against the virus. These antibodies are usually cleared within 6 months from the baby’s serum and as a result, children become more susceptible to infection. Although immunized mothers of the post-vaccine era are expected to provide their children with these antibodies, a variety of factors influence their serum levels. Declining maternal immunity is one factor and is best explained by the decreased exposure to wild-type viruses. [12] Another important factor is prematurity which has been established as one of the causes of decreased antibody titers compared to term infants. [12, 13]
The Center for Disease Control (CDC) recommends routine vaccination of children with the measles-mumps-rubella (MMR) vaccine in a 2-dose series scheduled at 12-15 months and 4-6 years with the possibility of giving the 2nd dose as early as 4 weeks after the 1st one. [14] Regarding the MCV vaccine, the WHO recommends that the first dose be given at 9 months where attack rates are high and risk of serious disease among infants exists and at 12-15 months where risk of infant infection is low. Although the second dose is generally administered at school age (4-6 years), it may be given as early as one month following the 1st dose, depending on the measles status in the country. [15] In Lebanon, the Ministry of Public Health adopted a vaccination strategy where which children will receive a zero dose of MCV at 9 months followed by a first dose of MMR at 12 months and a second dose of MMR at 18 months. [16] This appears to be well warranted given the significant number of measles cases in the younger ages as seen in Figure 1.
It is clear that measles is a disease of the pediatric population; however, adult cases must not be overlooked (Figure 1). A deeper investigation that goes beyond surveillance data must be implemented to understand the loopholes in the current vaccination program ranging from parental attitude towards the vaccine to insufficient supplies of the vaccine. A recent study by the WHO revealed that almost 77% of the potentially preventable cases of measles were among children aging less than 15 years who are at the heart of immunization programs. Although the average number of measles cases in individuals older than 14 years in Lebanon (Figure 1) is much less than the 45% reported by the European CDC database in 2017 among individuals older than 14 years, it remains a significant percentage that should not be ignored. [17] A study implemented in China revealed that the seropositivity rate of measles antibodies was significantly lower in subjects aged 15-19 years than those aged 5-9 years. This result was attributed to the waning antibody titers especially that there are no circulating wild-type viruses to confer natural immunity. It is rather challenging to implement a vaccination campaign to target adults as they will be most probably scattered among the population and unreachable taking into consideration the different circumstances and conditions. It would be more feasible to conduct an immunization program that involves high school students when they are still in mandatory education. Not only will it protect these teenagers from future measles infection, but also will contribute to the protection of future babies via increasing the measles maternal antibody levels and reducing the incidence of measles among infants without risking vaccinating pregnant women. A combination measles-rubella vaccine should be encouraged in the revaccination program in an attempt to adopt a cost-effective strategy that will aid in prevention of the Congenital Rubella Syndrome on one hand and measles elimination on the other increasing the chance of a combined eradication program. Revaccination of secondary school students regardless of previous measles vaccination or diseases status resulted in complete protection, raising seropositivity from 91% to 100% making it a very promising initiative. [18]
It appears from Figure 2 that there is a close relationship between measles and mumps incidence in Lebanon, and a clear pattern can be noticed when examining the outbreaks of each of these diseases. One or two years after every increase in measles cases among the Lebanese population over the past 20 years, a parallel increase – although less intense – in mumps cases can be observed. This trend has not been established elsewhere in the literature, yet it might be expected as the two diseases share a common vaccine. Should the rise in measles cases reflect a shortfall in the vaccination strategy, it would be logical to expect a deficiency in the immunity against mumps as well, and thus mumps outbreaks paralleling the measles outbreaks. Taking into consideration that the mumps vaccine is less immunogenic than that of measles [19], this might be of immense importance for public health strategies, as it might help anticipate any mumps epidemic before it occurs. For example, Israel has witnessed an outbreak of 262 mumps cases between January and August 2017 although vaccination levels reached ≥ 96% [20]. This was concomitant with a measles outbreak during the summer of the same year. [21]. While we are still far from defeating measles, we can use the measles epidemics to review our vaccination strategies, reassess the level of herd immunity against the disease, and prepare our healthcare systems for an imminent mumps epidemic as per the established pattern. National catch-up vaccination campaigns using the MMR vaccine after a measles outbreak might also be useful, as it might help curb the expected incoming mumps outbreak.
Figure 3 shows that most of the measles cases were either unvaccinated or had an unspecified immunization status in all the studied years except for 2015. Multiple factors might affect the accuracy of these figures and numbers. One factor that must be taken into consideration in assessing the overall vaccine effectiveness is the number of vaccine doses administered; many of those who claimed they contracted measles despite vaccination might have received an insufficient dose of the vaccine that does not confer immunity. This misunderstanding might thus skew the percentages and falsely elevate the percentage of those contracting measles despite vaccination. Another factor is the high proportion of cases whose vaccination status is unknown (40.74%, Figure 3). This means that only 59.26% of the cases had a documented vaccination status, which still lags behind the target set by the WHO at a minimum of 80%, indicating a failing surveillance system [11]. The proportion of non-vaccinated persons among those individuals might be higher than those who are vaccinated within the same group, obscuring the true estimate of vaccination coverage. Finally, one should take into consideration that there is a high chance that non-vaccinated persons are in fact clustered together and that the estimated vaccination coverage does not reflect the general population but rather represents that of a higher risk subpopulation [22].
Upon examining Figure 3, one cannot ignore the striking number of vaccinated people who contracted measles, as this might jeopardize the integrity of the vaccine in the eyes of the community. The current used vaccine in Lebanon is an-attenuated live measles vaccine that belongs to the Schwartz strain according to the WHO [10]. As mentioned earlier, individuals in Lebanon get a total of 3 vaccines that confer immunity against measles. Moreover, national catch-up campaigns against measles are conducted in case of any outbreaks as was the case in 2001, 2008 and 2013 in an attempt to enhance vaccination coverage and reduce the number of susceptible individuals. In one American study that discussed one of the largest measles outbreaks among highly vaccinated students – whose source case had coincidentally contracted the virus from Lebanon – it was revealed that students who have received both doses of the vaccine outside the United States were more susceptible to the infection than those who received both doses in the United states.[23] This was partly attributed to the quality of storage of the vaccine (the cold chain). Measles vaccine should be stored at 2-8°C and improperly stored vaccine may fail to provide protection against the disease. It has been revealed that new strains like the B3 strain, which is a more transmissible genotype, are becoming increasingly widespread leading to new epidemics worldwide. The quality of vaccine storage should be reviewed in Lebanon in lights of the observed ineffectiveness of vaccination in a significant number of people. Immunological and genetic research is also recommended to evaluate vaccine effectiveness against the aforementioned strains and identify any new strain that might not be covered by the available vaccines. This is to be bolstered by routine re-vaccination of high-risk individuals like health-care workers and contacts of measles cases in a strategy similar to the ring vaccination adopted in eradicating other viruses like Pox virus; this would help limit the dissemination of the virus and eventual eradication [24].
This high number of measles cases in vaccinated individuals might also be attributed to the fact that routine vaccination timeliness and completeness are still public health challenges, and currently timeliness is not routinely used as an indicator to evaluate immunization programs in Lebanon. A recent study by Mansour et al, found several factors that hinder vaccination, and these include socio-demographics, knowledge, beliefs and practices associated with age-appropriate vaccination. Interestingly, erroneously believing that children’s vaccination is up-to-date for their age was negatively associated with the administration of timely vaccines [25]. Mothers may perceive that the vulnerability to disease lessens with older age in the already sensitized child who has completed the primary vaccination series providing them with a sense of safety and subsequent non-compliance to booster shots [26].
The presented data should serve as a guide for the strategies that must be set in the current fight against measles. The WHO has published a strategy which can serve as the base upon which we build one of our own that suits the Lebanese experience [2]. While the Lebanese Ministry of Public Health has already instituted a successful surveillance program and achieved a sufficient percentage of measles vaccination, a clear outbreak plan remains to be set [6]. This plan can mimic the experience in Gabon which showed the importance of continuous surveillance, as well as molecular investigation in the fight against measles. Besides, active surveillance of measles contacts should also be implemented in case national vaccination campaigns are not possible, regardless of the vaccination status; in fact, secondary measles contraction in vaccinated individuals can present itself with symptoms dissimilar to those typical of the disease, allowing viral circulation in the absence of active monitoring [21]. This has been the case during the Israeli outbreak where the primary case presented with only fever and rash which was quite challenging to suspect measles [21]. The surveillance system must also improve in tracking vaccination records through encouraging families to hold onto home-based records [11].
Several infectious diseases outbreaks were noted in Lebanon in correlation with the huge influx of Syrian refugees into the country [8, 27]. No available data are present to describe the levels of measles vaccination in the migrant Syrian community in Lebanon. Data from Syria have shown subpar levels of first dose coverage of the measles vaccine ranging between 50-79% among their population [6]. The Italian experience showed that the migrant communities are not necessarily representative of their source population when it comes to measles vaccine coverage rates [28]. The discrepancy between migrants and their source population reflects the need for special screening and vaccination campaigns in migrants in Lebanon. This would be essential for the policy makers and the Ministry of Public Health to be able to contain ongoing outbreaks and curb future epidemics.
One of the cornerstones in the strategy to eliminate measles will be building public trust in the measles vaccine. Ever since the spread the later-falsified MMR-Autism theory, measles vaccination rates witnessed a hefty drop in some regions in the Western world. For example, the UK was declared endemic for measles in 2008, with some areas of London and Ireland reaching a vaccination level of only 60%. The United States also witnessed several outbreaks in the current decade with vaccination levels as low as 50% – far from the 95% herd immunity threshold [29]. However, the advocates of this theory are decreasing, yet some parents are still exhibiting a general anti-immunization approach [30]. Effective communication teams should be created and invested in to target different audiences and inform them on the importance of vaccination and the dangers of remaining unvaccinated [2]. This is highlighted in a recent study by Hoffman et al, which warned that social media outlets may facilitate anti-vaccination connections and organization by enabling the diffusion of century old arguments and techniques and facilitating anti-vaccination behaviour [31]. Although the subgroups arguing against vaccinations remain limited, such influences need to be combated and counteracted. Health professionals should leverage social networks to deliver more effective, targeted messages to different constituencies.
Last but not least, investing in local capacity building and research projects to understand the epidemiology and behaviour of the measles virus in relation to the population dynamics in Lebanon is of immense importance to establish national strategy and guidelines. This, in addition to the recommendations mentioned above, shall hopefully put the Lebanese community on the right path for true measles elimination.