ABSTRACT
Measles is a well known vaccine preventable disease causing significant morbidity and mortality among children worldwide especially in developing countries like Ethiopia. A surveillance data was analyzed to describe measles cases epidemiologically and identify locations where case loads are high for further investigations. The National Measles/World Health Organization (WHO) guideline was used for case definitions and the final classification of cases. Selected variables from the database of the national measles surveillance data of 2005 to 2009 Ethiopia of were analyzed. Epi Info Version 3.5.1 and Microsoft Excel were also used for statistical analysis. A total of 17,521 cases and 127 deaths (Case Fatality Rate: 0.71%) were reported during 2005 to 2009. A total of incidence 5771 measles cases with an incidence of 7.6 per 100,000 populations were reported in 2008. The highest attack rate (12%) was observed in Hareri region. The majority (50.7% (8894)) of cases were from rural, 51.9% were males and the median age was 4 years old. About 4718 (26.9%) cases did not have a history of vaccination. Most IgM-antibody confirmed cases (40.5% (1216 of 3000)) were reported from Oromia region. The age group 1 to 4 years old constituted 41.7 (7323) and 34.4% (1032) of the suspected and IgM-antibody confirmed cases, respectively. Outbreaks occurred in Guji, West Arsi, West Haraghe and Sidama zones which showed the peaks of epicurve in January and February of 2008 and 2009. Except Tigray, Harar and Dire Dawa, all regions reported outbreaks. Although the national measles vaccination coverage in Ethiopia reached 72.2% in 2008, five regions were under 55% and repeated outbreaks were observed. Therefore, regions should improve measles vaccination coverage and early case detection. The seasonality of disease transmission and causes of outbreaks for the identified locations needs also further investigation and research.
Key words: Measles epidemiology, IgM antibody, surveillance data, Ethiopia.
Measles is a highly infectious viral disease caused by a Morbillivirus, and for which humans are the only reservoirs. In a non-immune person exposed to measles virus, after an incubation period of about 10 to 12 days (range 7 to 18 days), prodromal symptoms of fever, malaise, cough, coryza (runny nose), and conjunctivitis appear. Within 2 to 4 days of the prodromal symptoms, maculo-papular rash appears behind the ears and on the face. The rash spreads to the trunk and extremities and typically lasts 3 to 7 days (WHO Afro Measles surveillance revised, 2004).
Most persons recover from measles without complications. Some complications are associated with measles due to transient suppression of cellular immunity, which is a characteristic feature of the disease. Frequent complications in children less than five years of age include otitis media (5 to 15%) and pneumonia (5 to 10%) (WHO South East Asia regional office, 2009). Transmission is primarily person-to-person via aerosolized droplets or by direct contact with the nasal and throat secretions of infected persons. Individuals with measles are infectious 4 days before through 4 days after rash onset (WHO Afro Measles surveillance revised, 2004).
Despite the existence of a safe, effective, and inexpensive vaccine, measles is still not being controlled in many parts of the world. However, the use of measles vaccine over the last 30 years has reduced global measles morbidity and mortality by 74 and 85%, respectively, compared with the pre-vaccine era (Cutts et al., 1999). The World Health Organization (WHO) estimates that almost one million measles-related deaths occur each year, the majority (85%) in Africa and Asia (MMWR, 1999; Altintas et al., 1996).
Measles is widely known in Ethiopia and it has many names in various ethnic languages, for example, Kufign, Ankelis or Shifto. In 1980, Ethiopia introduced measles vaccination as part of the Expanded Programme on Immunization (FMOH Measles Guideline, 2007). A single dose of measles vaccine is recommended at 9 months of age (Cutts et. al., 1994; Global Advisory Group II Measles Wkly Epidemiol Rec, 1993; De Quadros et al., 1996). Several developed and developing countries follow a strategy that differs in timing and in the number of doses delivered either through routine immunization or supplemental mass immunization campaigns (FMOH Measles Guideline, 2007). In determining the age for vaccination, countries must balance the consequences of an older age (lack of protection in the early months of life) and a younger age (reduced effectiveness). In many countries, where morbidity and mortality due to measles are uncommon in infants, choose an older age for vaccination (e.g., age 12 or 15 months). In other countries, where a high number of deaths due to measles occur in children aged <9 months, a younger age for vaccination has been advocated (Kiepiela et al., 1991; Tades and Ghlorghis, 1985).
However, during supplemental immunization campaigns, a single dose of measles is given, irrespective of the immunization and disease history status, to all children in the target age group (FMOH SIAs Field Guide Ethiopia, 2010). A study conducted in Ethiopia showed also that campaign vaccination elevated immunity in the target ages by between 30 and 50% or an average of around 40% (Nigatu et al., 2008).
In Ethiopia the importance of disease surveillance in guiding health planning and interventions was recognized for a long time and “Quarantine" rules were proclaimed in 1947 with emphasis on surveillance. Another legal notice was issued in 1951, binding all public health practitioners in the country to report communicable diseases. The "Public Health Proclamation No.200/2000” orders any individual who knows the existence of communicable diseases in his/her vicinity to report immediately to the nearest health institution and the institution receiving the report to take the necessary measures and report to the appropriate health authority. In 1948, an anti-epidemic service was established to deal with prevention and control of communicable diseases. In 1951, 35 priority diseases were selected and classified into first and second class to be notified to Ministry of Health (MOH), immediately or weekly as necessary. In the mid-1970`s, the anti-epidemic unit was converted to epidemic control and surveillance unit under communicable diseases control division, and vertical programs were conducting their own disease specific surveillance. After the health system reform in 1994, nineteen diseases (including those which were under vertical programs) were selected for surveillance and measles was also one of the priority (IDSR Ethiopia, 2002).
According to the National Public Health Emergency Management (PHEM) guide line, every suspected measles case should be detected, reported using the cases based form and undergo laboratory investigation (or the first five cases in the situation of outbreaks), and during an outbreak all cases must be entered on a line listing, investigated and reported to next higher level (FMOH Measles Guideline, 2007; FMOH SIAs Field Guide Ethiopia, 2010/2011).
Ethiopia has experienced numerous measles outbreaks and increasing morbidity. As a vaccine preventable disease, measles surveillance data analysis is critical to guide intervention and vaccination activities. So the aim of the study was to assess the measles trend in the country, describe measles epidemiologically and identify locations where occurrence of cases is high for providing further investigation of causes and guide interventions.
Study area, population and period
Ethiopia is administratively sub-divided into nine regional states and two city administrations. According to the third to be 73,918,505 with an annual growth rate of 2.6%. Of which, 50.5% (37, 296, 657) were males, 45.0% were under age 15 years old, 51.9 % were in the age group of 15 to 64 years and those aged 65 years and above were 3.2% (Population and housing census Ethiopia, 2008). The national measles surveillance data was analyzed from November to December, 2010 in Addis Ababa, Ethiopia.
Design and data collection
A descriptive study was undertaken on the national measles surveillance data of 2005 to 2009. Although the type of data was secondary the study passed through the following procedures to have it. First a concept paper was developed and submitted to the school of public health of Addis Ababa University for review. Then, the Ethiopian Public Health Institute (EPHI) public health emergency management (PHEM) center approved the request of a five year national measles data base to carry out this study. The data base has many field names(variables) but the study analyzed selectively such as age, sex, date of onset of illness, reporting zone and province(Regional state), date of sample collection, sent to and received by the national laboratory, no of vaccine doses, type of reporting form, final classification of cases and presence of outbreaks.
Case definitions
The national Public Health Emergency Management and WHO measles guidelines were used for the case definitions and the final classification of cases by the laboratory as it was kept in the data base (Global Advisory Group II Measles Wkly Epidemiol Rec 1993; PHEM Guideline Ethiopia, 2009; WHO Afro IDSR, 2008). According to the Federal ministry of health of Ethiopia-Public health emergency management, measles is one of the immediately reportable diseases under surveillance. Suspected cases and deaths of fever with rash illness filled with case-based reporting form with serum sample collected are sent and tested for IGM antibody at Central (EHNRI) virology laboratory. Line listing was also used during an outbreak for reporting of cases.
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.
Confirmed case
A suspected case with laboratory confirmation (positive IgM antibody) or epidemiologically linked to confirmed cases in an epidemic. All suspected cases of measles are finally classified based on the adequacy of the blood specimen collected, and sample taken or not in to the following categories;
Laboratory confirmed: A suspected measles case that is investigated, including the collection of an adequate blood specimen (5 ml), and has serological confirmation of recent measles virus infection (IgM positive).
Epidemiologically linked: A suspected measles case that has not had a blood specimen taken for serologic confirmation, but is linked to a laboratory confirmed case (definitive serologic evidence of recent measles virus infection). Linked is interpreted as being in the same geographic area (place) during the infectious period (time) of a laboratory-confirmed case (person), that is, in the same district within 30 days.
Discarded: A suspected measles case that has been completely investigated, including the collection of adequate blood specimen (5 ml), but lacks serologic evidence of recent measles virus infection (that is, IgM negative).
Clinical / Compatible: A suspected measles case that has not had a blood specimen taken for serologic confirmation, and cannot be epidemiologically linked to a laboratory-confirmed case.
Statistical analysis: Descriptive statistical analysis was made using Epi Info Version 3.5.1 and Microsoft Excel.
Ethical issue: The national measles surveillance data of the public health emergency management / Ethiopian had been ethically cleared at of the public health emergency management (PHEM) center of the Ethiopian public health Institute (EPHI).
According to the national measles surveillance data which include case based and line listing; a total of 17521 cases and 127 deaths were reported throughout the country in the period between 2005 and 2009. Of the total suspected cases, about 50.7% (8894) were from rural site, 23.7% (4167) from urban and 25.4% (4460) not identified as rural-urban. About 51.9% were males, 0.34% with sex not reported and the median age was 4 years old and the age ranges from under 1 up to 79 years old.
The national measles vaccine coverage increased from 42% in 2002 to 72.2% in 2008 and an increased number of reported cases was also observed from 2005 to 2008 (Figure 1). In the five years of reporting period, only 6.4% (1120) of cases get two or more vaccine doses, 31.3% (5490) get one dose, 26.9%(4718) not vaccinated and 35.3%(6192) with unknown vaccination status. It was observed that the cumulative number of suspected cases for five years was continuously increasing between December and January (Figure 2). The highest number of cases and incidence [5771 cases (7.6 per 100,000 population/year)] was reported in year 2008 (Table 1).
In each month of the five year period, a minimum of 50 suspected cases were reported to the central level. As it is shown in the epidemic curve, sharp peak was from January to February, 2008 and 2009 (Figure 3). Through filtration of the data base for those specific months which showed the highest peaks in the epidemic curve zones/provinces such as; Guji, west Arsi, West Haraghe and Sidama reported the highest number of cases than any other zone in the country (Figure 3).
The outbreak in Guji started on 14/1/2008 and the highest peak was on 21/1/2009 and then continued to 5/2/2008. As it is shown in the Epi-curve (Figure 4), at least 40 cases per day were reported even after the highest peak. A total of 1606 suspected cases were reported during the two months of an outbreak. 94.7% (1520) cases were under 15 years old, 45.6% (733) unvaccinated, 43.7%(702) get one dose, 1.1%(18) 2 doses, 9.5%(153) unknown status of measles vaccination.
In west Arsi, a total of 954 cases were reported in January 3 to 31, 2009 (Figure 5). During this period, 99.6% of the cases reported using a line list form. Measles vaccination status was not known in 99.6% (951) of the cases and only one case was vaccinated for first dose. Sex was evenly distributed (50%) and no death was listed in the data base.
In West Hararghe an outbreak occurred in February, 2007 (Figure 6) and two other outbreaks from March to April and December, 2008. A total of 237 cases reported in December, 2008 which were higher than the cases that occurred in previous three outbreaks (February, 2007, and March to April, 2008). 54.7% (135) of the cases were females, 89.1% (220) were under the age of 15 years and only 17 cases have got one dose of measles vaccine.
In January 2009, there was also an outbreak in Sidama zone/province with 236 reported suspected cases (figure 2.1.7). 50.4% (119) were females, 55.1% (130) unvaccinated, 35 % (92) with vaccination history (one and more doses) and 5.9% (14) with unknown vaccination status and one death. Fourteen cases from Guji, 4 from West Arsi, 6 from West Haraghe and 21 from Sidama zones were confirmed for measles IgM antibody collected during the occurrence of increased number of cases as depicted in the respective Epi-curves shown earlier.
During 2005 to 2009 period, the age group 1 to 4 years old constitute 41.7 % (7323) of the total suspected and 34.4% (1032) of the confirmed cases by laboratory measles IgM antibody. 9.3% (1632) of the suspected and 6.5% (197) of the laboratory confirmed were under 1 years old (Figures 8 and 9).
A total of 11,841 serum samples were collected and sent to the national laboratory (EHNRI).The highest annual proportion of samples collected was 67.3% (3087) in 2009 followed by 86.4%(1224) in 2005. The highest (31.1% (913)) confirmed cases of measles IgM antibody was reported in 2007 and the least (9.7% (447)) was in 2005 (Table 2). 50.9 % (1524) of measles IgM confirmed cases were males during 2005 to 2009.From all regional states, Oromia ranked first by notifying 44.8% (7861) of the national total suspected cases during the five years period. Somali and The Southern Nations Nationalities and Peoples' (SNNP) regional states detected the highest (48.8% (153)) and lowest (12.4% (356)) proportion of confirmed IgM positive of their own total suspected cases respectively. But from total national confirmed IgM positive cases, Oromia regional state also accounted first with a proportion of 40.5% (1216) (Table 3).
All regions/city administrations and 102 zones in the country reported cases in each year and at least in one year respectively. In all five years period, the attack rate for measles sustained more than 2% in Harari regional state. From all regions the highest attack rate (12.9%) was observed in Harari in 2008 and in Gambella. (5.4%) in 2009. Except in 2006, Oromia reported the highest number of cases in all other four years and 44.8% (7861) from the total cases of the country reported in in five years (Table 3). From 102 zones reported during 2005 to 2009, a total of 17521 cases were notified. Guji zone constituted the highest (1724 (9.8%)) number of cases, followed by west Arsi 1423(8.1%), West Hararge 823 (4.7%), Sidama 791(4.5%) and North Gondar 725(4.1%). In 2006, 23.5% (24) of zones had zero report of measles cases followed by 16.7% (17) in 2005, but in 2009 all 102 zones reported suspected measles cases (Figure 10).
From the total of 17522 registered cases, 11842 (67.6%) were reported using case based forms and 5680 (32.4) were using line listing. 64.1% (3643) of the reports using the line listing were from Oromia region. Tigray, Harari and Dire Dawa had zereo report of line listing based data. Fourty five (45.1%) zones reported measles outbreaks from 2005 to 2009, of which Guji reported 1593 (28.2%), West Arsi 1100 (19.4%), West Haraghe 512 (9%), Sidama 320 (5.7%) and North Gondar 260 (4.6%) cases. Except Tigray, Harar and Dire Dawa all regions reported cases of an outbreak at least in two years from 2005 to 2009. Amhara, Oromia and SNNPR reported an outbreak in all four years except in 2005 (Table 4).
From 16 zones, 126 deaths were reported during 2005 to 2009 in which the highest number [23 (18.2%)] of deaths reported from Gujji 23 cases (18.2%) West Harerghe [21(16.6%)], and from zone 2 of Afar [14(11.1%)]. The overall case fatality for the five consecutive years of the country was 0.72%.
Measles immunization coverage of Ethiopia showed a progress from 42% in 2002 to 72.2% in 2008, and it was also indicated that, from 1998 the Federal Ministry of Health continued conducting measles supplemental immunization activities (SIAs). Moreover, recently the African regional goal; a >90% measles immunization national level coverage and a >80% coverage in all districts was adopted by the Federal Ministry of Health of Ethiopia (FMOH SIAs Field Guide Ethiopia, 2010/2011).
Nonetheless notification of measles cases increased year to year with a decline in 2009. It was also depicted by the Epi-curve that Ethiopia experienced outbreaks in 2008 and 2009 of January to February (Figures 3 to 7). This could probably also be due to improvement of measles surveillance activities such as notification of any suspected cases of measles. In Oromia region for example, of the total reported suspected cases of 2005-2009, 46.4% (3654 cases) classified as discarded. This might indicate an increase in awareness of notifying suspected cases of measles. As it was evidenced, among the total cases, 26.9% (4718) were vaccinated and 35.3% (6192) found with unknown vaccination status.
The two highest peaks of the Epi-curve (Figure 3) in January 2008 and 2009 were due to the outbreaks of Guji and West Arsi-Sidama zones. As it was shown in Figures 4 to 7 in Guji, West Haraghe, West Arsi and Sidama zones, an outbreak occurred for days with confirmation of laboratory of Measles IgM antibody in 30 days or less. Cases were not evenly distributed by age, and the most affected age group was observed from 1 to 4 years throughout the five years period (Figures 7 and 8). This could be the immaturity of immune system in this age group and it is also documented that in developing countries the most vulnerable children are between the ages of 9 months and 5 years (WHO, a field manual in emergencies, 2005).
Though an increased number of suspected measles cases notified in 2008 and 2009, the laboratory confirmed cases (10.7 and 9.1%, respectively) were much lower than the rest three years. This could be due to the occurrence of outbreaks in 2008 and 2009, which minimized the number of serum samples to be collected, i.e, no more serum sample collection after five laboratory confirmed cases during an outbreak.
The incidence of suspected measles cases in all five years was more than 2 cases per 100,000 populations/year, which kept Ethiopia as high burden of measles compared to all the other African countries (WHO-AFRO Measles Surveillance Feedback Bulletin, 2007).. The cumulative case fatality rate in five years period was too low (0.71%). This could be under reporting of deaths and weak surveillance activities to detect a case early which is a common situation like other causes of deaths in the country or it could be also due to improvement of case management in health facilities.
All big regions such as Oromia, Amhara, SNNP, and Tigray had low performance or proportion of detection of confirmed IgM positive cases. However except Ben-Gumuza and Harari all other regions and city administrations had good performance. This could be the fact that in big regions the notification of suspected cases was high and especially because of the occurrence of outbreaks in each year result in an increment of a denominator.The highest attack rate (12.9%) in Harari and Gambela (5.4%) could not be also justified at this point; however the probable hypothesis might be cold chain management failure, low coverage of immunization and presence of many susceptible groups in the community. Three regions (Tigray, Harar and Dire Dawa) had zero report of measles cases in line listing form different from the rest of all other regions. The Tigray case could be explained by its consistent and higher vaccination coverage (above 74%) which is better from other regions, but the absence of outbreak in Hareri and
Dire Dawa in five years period couldn’t be explained so far. The seasonality trend of the disease or increase number of cases from December to February could not also be justified within the scope of this work.
The 80% or greater number of districts report of measles cases with a blood specimen collected within 30 days of rash onset is one of the primary indictors for the performance of measles surveillance (FMOH Measles Guideline, 2007).However, it couldn’t be calculated because of the absence of districts list in the current database. But when the study observed by zone; 102 (100%) zones reported at least one measles case in 2009, 83.3% in 2005, 74.5% in 2006, 88.2% in 2007 and 93.1% in 2008. About 11, 829 (99.9%) samples arrived in a good condition (that is, adequate volume, no leakage, not desiccated) to the national measles laboratory, which meets the WHO's target of 90% or more.
A total of 17521 suspected and 3000 (17.1%) laboratory (IgM antibody) confirmed measles cases were notified at central or national level during 2005 to 2009. The overall case fatality rate was 0.71% for the same years period. Generally, there was a trend of increment of cases in January, February and March of the study years. The national vaccination coverage showed progress year to year though the vaccination coverage of five regions was still under 55%. Four zones (Guji, West Arsi, West Haraghe, and Sidama) were identified as places which were responsible for the sharp peaks in the national epidemic curve of the five years period because of the occurrence of outbreaks.
The age group 1 to 4 years was the most affected population by measles from all other age categories and 62.2% of the cases were not vaccinated for measles or with unknown status of vaccination. Oromia regional state constituted most of the suspected and laboratory confirmed measles cases, however the highest attack rate was observed in Hareri region. Tigray Dire Dawa and Hareri regions had no report of cases of an outbreak.
The FMOH and other partners should collaborate and strengthen regions for the improvement of measles vaccination coverage. The seasonality of disease transmission or occurrence of outbreaks could indicate when to conduct SIAs, and the needs for further investigation and research. The surveillance activities need improvement in early detection of cases, for the completeness of variables and specificity of reporting suspected measles cases especially during outbreaks. Improvement in the database management for ease analysis that is, for example health facility names were inconsistent and districts were not filled. Further investigation or research is necessary to find out causes of outbreaks for the identified locations.
The authors have not declared any conflict of interests.
Authors acknowledge the Ethiopian Public health Institute (EPHI) and The Field Epidemiology Training Program (EFETP) for providing the opportunity to work on the national Measles surveillance data.
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