Rubella and Congenital Rubella Syndrome Elimination, the Oman Experience
Salah T. Al Awaidy1*, Salim Al Mahrouqi 3, Hosammudin Mohammed Nwar Al Den3 , Suleiman Al Busaidi1, Badder Al Rawahi 3, Maryam Al Shaibi 3, Idris Al Obaidani 3, Said Al Baqlani 2
1Office of H.E. of Health Affairs, Ex EPI National Manager and Director of Communicable Diseases Surveillance and Control, 1996- 2011, Ministry of Health, Muscat, Oman
2Central Public Health Laboratory, DGCDS&C, Ministry of Health, Muscat, Oman
3Department of Communicable Disease Control, DGCDS&C, Ministry of Health, Muscat, Oman
Over the last few decades, Oman has experienced significant rubella epidemics (from 1987 to 1989 and from 1992 to 1994). In 1994, the first dose of rubella-containing vaccine (RCV1) was introduced into the EPI national program as measles-rubella vaccine (MR) at 15 months of age. In October 1997, MR vaccine was replaced by measles-mumps–rubella (MMR) and in 1997, MR vaccine was replaced by measles-mumps-rubella (MMR) vaccine; and by 2001, a policy of two doses of MMR vaccine was introduced at 12 and 18 months of age. This has led to a dramatic decline in the incidence of rubella following widespread use of rubella vaccine with vaccination coverage greater than >95%. Postpartum rubella vaccination has been a national priority since 2001 with a 99.5% postpartum coverage.
The country of Oman recently established a policy for interrupting indigenous rubella virus transmission. We defined rubella elimination as the absence of endemic rubella transmission in a defined geographical area (e.g. region) for ≥12 months without the occurrence of congenital rubella syndrome (CRS) cases associated with endemic transmission in the presence of high-quality surveillance system. Strategies to achieve this goal included: a) vaccination supplemental vaccination activities with the goal of achieving high rates of vaccination coverage; and maintenance of coverage in order to increase populationwide
immunity; b) syndromic surveillance programs to monitor fever and rash syndromes for effective detection of cases and serological surveillance; c) integrating these strategies into measles surveillance system; and d) initiating a CRS surveillance system. As a result of these interventions, there have been fewer than 12 confirmed total rubella cases since 2007. Since 2013, the incidence of rubella has declined markedly to zero case per million persons. Similarly, only one single case of CRS has been notified since 2007. In summary, Oman has made significant progress toward rubella and CRS elimination and has met the elimination goals. Despite these achievements, major challenges have emerged associated with increased globalization leading to outbreaks from imported cases. Efforts are underway to reach communities of unvaccinated immigrant workers and their families coming from areas with potentially low rubella vaccination coverage.
Keywords: Rubella; Congenital Rubella Syndrome; CRS; Epidemiology; Elimination; Incidence; Trends; Oman; Eastern Mediterranean Region
Oman is one of the twenty-two countries in the World Health Organization (WHO) Eastern Mediterranean Region (EMR). It is located in the southeastern corner of the Arabian Peninsula with a coast that extends 3,165 kilometers from the Strait of Hormuz. Oman’s borders include Yemen to the south, and the Kingdom of Saudi Arabia and United Arab Emirates to the west (Figure 1).
Figure 1. Map of Oman.
The population was 3,992,893 in 2014 with immigrant workers and their families, mostly from South and Southeast Asia, accounting for nearly 44. In Oman, children under 5 years of age comprise 9.5 % of the population and those less than 15 years of age comprise only 22% [1,2].
Rubella has been a significant cause of infant and child morbidity and mortality in Oman. During the period of 1975 to 1982, more than 5,000 rubella cases occurred annually in Oman with a mortality rate of approximately of 8-12%. Furthermore, Oman experienced large rubella epidemics in 1992–1994 . Since then, there has been a dramatic decline in the incidence of rubella following widespread use of rubella vaccine. In March 1994, there was a national campaign to deliver measles-rubella (MR) vaccine to the target group aged 15 months - 18 years. Some 700,000 persons received MR vaccine during this campaign, with 94% coverage of the target age group. Concomitantly, the first dose of rubella containing vaccine (RCV1) was introduced into the routine immunization schedule for children at 15 months. This decision was based on the results of a clinical trial conducted in 1992-1993, which showed excellent sero-conversion of Omani children to rubella vaccine at this age . In 1997, MR vaccine was replaced by measlesmumps- rubella (MMR) vaccine; and by 2001, a policy of two doses of MMR vaccine was introduced at 12 and 18 months of age. Coverage with all doses of RCV has been 97% or higher since 1994. In addition, postpartum rubella vaccination has been a national policy since 2001. As a result, a nationwide coverage survey in 2004 demonstrated that 99.5% of postpartum women had received rubella vaccine .
Oman adopted goals for elimination of rubella and congenital rubella syndrome (CRS) in 1996 . The Ministry of Health (MOH)also developed key strategies and a national plan for rubella and CRS elimination that included: a) vaccination supplemental vaccination activities with the goal of achieving high rates of vaccination coverage; and maintenance of coverage in order to increase population-wide immunity; b) syndromic surveillance programs to monitor fever and rash syndromes for effective detection of cases and serological surveillance; c) integrating these strategies into measles surveillance system; d) initiating a CRS surveillance system; and e) improving the availability of high-quality information for health professionals and the
public on the benefits and risks associated with immunization against rubella. As vaccine coverage increased and was maintained above 95% from 1999 to 2004, fewer rubella cases occurred, from <100 cases annually during 1990- 1996 to only 8 cases annually from 1997 to 2006 . And since 2007, only 12 cases or less have been reported totally. As part of the national plan for rubella and CRS elimination, a registry of CRS cases was established in 2000, which includes all children with CRS reported to the Ministry of Health since 1988 .
Further, Oman has established an independent rubella and CRS technical expert committee to review the status of rubella and CRS elimination and provide advice on corrective actions that will be critical for achieving and maintaining successful elimination. Herein, we describe the progress made towards rubella and CRS elimination in Oman and the challenges ahead for this important public health effort.
The Expanded Program on Immunization (EPI) in Oman was launched in 1980 and it is integrated into the Primary Health Care (PHC) services provided by the MOH. Numerous efforts have been made to ensure the expansion of rubella containing vaccine (RCV) at the grass roots level.
All rubella and CRS-related activities (immunization and laboratory testing of suspected rubella cases) are financially supported by the government and provided free of charge throughout government health facilities for all inhabitants (Omanis and non-Omani residents). Immunizations for rubella and other diseases are provided in all primary health care centers and in certified vaccination units at private health facilities. To receive immunization and primary care, each infant and child in Oman is registered with a specific health facility, either at birth or on entry into the country.
This registry is based on vaccine residential address and the use of a unique identification number. Parents or guardians are given immunization cards for their children that are updated at each immunization clinic visit. To improve vaccination records, health facilities also use a hard copy of the registration databases for their catchment population and childhood screening booklets for each infant and preschooler containing information on immunizations and screening findings. A unique defaulter retrieval system was also introduced to complement the program. Parents of any child who missed the vaccination appointment are called by the EPI staff nurse. If there is no response from the parents for more than two weeks, a home visit is conducted by a public health worker . Healthcare workers at primary health centers and school health nurses are advised to trace measles-mumps-rubella (MMR) immunization defaulters.
Furthermore, by 1994, the Ministry of Health had established a policy that required proof of completion of all routine immunizations, including 2 doses of MMR vaccine, for any eligible person and for primary school entry at all levels. Children or any eligible person with incomplete or unknown vaccination status are required to complete their childhood recommended immunization schedule. Vaccination is provided if there is no documented evidence of rubella (RCV1 and RCV2) vaccination. In addition, rubella (monovalent or MMR) vaccination of postpartum women and health care workers has been a national policy since 2001.
The national vaccine store in Oman was the first to meet the new WHO/UNICEF criteria of Effective Vaccine Store Management (EVSM) in the word . The functioning of this national storage facility includes a built-in efficient internal supervisory and monitoring system which permits proper storage and handling of vaccines established at all governorates, and that allows regular external reviews by WHO/UNICEF. In addition, guidelines have been developed to govern vaccine handling safety processes. During immunization practices, “high practice standards” are mandatory by providers including injection safety (availability of injection material and sharps containers) and proper disposal of injection material (safe, complete, and environmentally friendly).
All health facilities submit their vaccination coverage data monthly to the Immunization Unit at the Department of Communicable Disease Control (DCD&C), MOH. Rubella immunization coverage is calculated using the number of doses of MMR administered as the numerator, and the number of surviving infants or the number of infants and children registered at health facilities as the denominator. Data on rubella immunization coverage and other vaccination statistics are analyzed at both district and national levels. Feedback is submitted to all health facilities and respective health authorities every month [8,9]. In addition, administrative coverage is confirmed by periodic validation of the vaccination coverage data using data quality self-assessment (DQS) every 3 years; and coverage evaluation surveys every 5 years.
The national communicable disease surveillance ‘system’ was formally launched in Oman in March 1991 to be in conformity with the ‘communicable diseases law’ issued by royal and ministerial decrees. This surveillance system ensures the collection and use of appropriate and timely data for dealing with the target priority diseases including emerging and re-emerging infections. The priority communicable diseases are grouped into ‘A’, ‘B’ and ‘C’ based on the urgency of reporting and the response. The regrouping of rubella was done in 1996 with shifting from Group ‘B’ to ‘A’ since the launching of the elimination initiative in the same year. Regional epidemiologists are assigned at all governorates to oversee the surveillance activities .
Integrated rubella and measles surveillance and start of CRS surveillance
In 1996, rubella and measles surveillance activities were integrated into one program. In this context, rubella and CRS notification is integrated into the national communicable diseases surveillance system and is in place nationally and monitors rubella and CRS incidence, mortality and other notifiable vaccine-preventable diseases. The MOH requires all health facilities, including private establishments, to notify suspect rubella and CRS cases within 24 hours of suspicion to the governorate communicable diseases surveillance control unit (CDSU). Reporting must be done in a timely manner, including zero reporting of rubella and CRS from all institutions. The MOH periodically sends communications out to all medical practitioners reminding them about the requirement for timely and zero reporting of rubella.
Initially, case-based surveillance was established in 1996 by using standard case definitions developed by WHO. The CDSU surveillance team thoroughly investigates each reported case with particular reference to age, vaccination status, and history of travel. Moreover, attempts are made to find the index case and data are analyzed for evaluation of program routinely. All suspected cases undergo laboratory investigation free of charge.
A” fever and rash” illness surveillance activity was launched in late 2004 throughout the country. The fever and rash case definition includes any individual of any age who develops sudden onset of fever and rash (excluding chickenpox). These are considered suspected cases of fever and rash illness syndrome and are tested for measles and rubella IgM antibody simultaneously based on an algorithm (Figure 2). In addition, fever and rash illness weekly zero reporting from all institutions over the entire country was established. The existing infrastructure for acute flaccid paralysis and neonatal tetanus surveillance was utilized for this purpose.
Figure 2. Fever and rash illness investigation algorithm, Oman.
Laboratory testing of suspected cases includes measurement of Rubella IgM antibodies by enzyme-linked immune sorbent assay (ELISA) at Oman’s Central Public Health Laboratory (CPHL), a WHO Accredited Regional Reference Laboratory for measles and Rubella viruses. Since 2005, all specimens from IgM-positive cases undergo polymerase chain reaction (PCR) confirmation and genotyping. Viral culture and isolation are performed from throat/nasal and urine samples collected from all fever and rash illness cases for the purpose of viral typing. Oman’s CPHL is part of the WHO Measles Rubella Laboratory Network (MRLN) and all rubella laboratory-confirmed cases from designated National Rubella laboratories are forwarded to CPHL for validation and genotyping. The CPHL has performed genotyping of rubella virus for the past 2 decades.
The CRS surveillance system was implemented in 2004 in Oman and has been included in the reportable diseases group A, demonstrating the priority of its reporting to national authorities. National surveillance occurs through passive reporting from all institutions to the governorate communicable diseases surveillance unit (Figure 3). Every clinician, staff nurses, hospitals, and laboratories are mandated to report cases of CRS to their respective governorate. In this program, cases are classified according to the following operational definitions:
Figure 3. Alert for detection of CRS compatible manifestations, Oman.
Suspect case: a child <1 year with a maternal history of rubella in pregnancy and or heart disease, or deafness, or eye signs white pupil (cataract); diminished vision; nystagmus; squint; smaller eye ball (microphthalmos); and larger eye ball (congenital glaucoma).
Clinically confirmed case: a child <1 year with two complications in group (a) OR one from group (a) & (b).
Group (a): cataract(s), congenital glaucoma, congenital heart disease, loss of hearing, pigmentary retinopathy;
Group (b): purpura, splenomegaly, microcephaly, mental retardation, meningoencephalitis, radiolucent bone disease, jaundice with onset within 24 hours after birth.
Laboratory-confirmed case: an infant with a positive blood test for rubella-specific IgM and clinically-confirmed CRS.
Congenital rubella infection (CRI) case: An infant with a positive blood test for rubella-specific IgM who does not have clinically-confirmed CRS.
Epidemiologists in each governorate determine whether the case meets the surveillance case definition (Figure 4) and, if so, the epidemiologist is responsible for gathering necessary epidemiologic data and conducting a follow-up investigation. Active surveillance has been conducted at tertiary and secondary care for CRS using the same infrastructure for acute flaccid paralysis and neonatal tetanus surveillance.
This program mandates that every suspected case of CRS should be reported within the first 24 hours after identification, and in this manner, every case is investigated within 48 hours after its identification.
Figure 4. CRS investigation algorithm, Oman.
The governorate epidemiologist is responsible for completing the surveillance case report form, entering the data in an Excel database sheet, and sending the information to the next level weekly in accordance with the routine disease notification procedures. The laboratory personnel are responsible for the serum sample collection and shipment to the CPHL for rubella-specific ELISA IgM testing. In addition, active surveillance is conducted weekly through: a) review of fetal death registry; b) review of monthly surveillance reports of congenital anomalies & genetic disorders records; c) inpatient and outpatient statistical data review; d) monthly report of eye diseases and deafness registry reports; and e) annual reports when they are compiled by hospital.
As per the national policy an outbreak is defined as the occurrence of one clinically suspected or confirmed rubella case [10,11] and warrants immediate initiation of outbreak control activities. According to the national guidelines for rubella surveillance, all outbreaks should be investigated within 48 hours. Clinical specimens should be obtained from all persons with suspected cases and sent to the CPHL within 3 days. In addition, children 1 year and above and adults are checked for previous vaccination history. If there is no evidence of vaccination, then, vaccination is provided.
All outbreaks of rubella are investigated with particular reference to age, vaccination status and history of travel. Attempts are made to find the index case and data are analyzed for program evaluation.
Vaccination Coverage through routine immunization activities
In 1994, the first RCV1 (MR) dose was introduced into the EPI national program at 15 months of age. In 1997, MR vaccine was replaced by measles-mumps-rubella (MMR) vaccine; and by 2001, a policy of two doses of MMR vaccine was introduced at 12 and 18 months of age. Coverage with all doses of RCV has been 97% or higher since 1994. In addition, postpartum rubella vaccination has been a national policy since 2001 [Figure 5]. Coverage for both RCV1 and RCV2 has been sustained at ≥ 97% nationally and provincially since 1994. The administrative coverage was confirmed by coverage evaluation surveys conducted in 2008.
In addition, postpartum rubella vaccination has been sustained at ≥ 95% nationwide. A coverage survey in 2004 demonstrated that 99.5% of postpartum women had received rubella vaccine 
Vaccination during mass campaigns
In response to the occurrence of widespread outbreaks of rubella cases during the years of 1994-1994, a nationwide catch-up campaign was conducted in 1994 using MR vaccine. This effort targeted children aged 15 months to individuals up to 18 years and attained 94% vaccination coverage. A marked decline of measles cases was observed following this campaign (Figure 5). After this campaign, the Ministry of Health began estimating the number of unvaccinated children annually to predict the risk of outbreaks and to determine the need for national measles campaigns. Further, supplemental immunization activities are conducted regularly in response to any confirmed rubella case to ensure high coverage of 2 doses MMR for persons in areas near confirmed cases. To help achieve the rubella elimination goals, a catch-up MMR immunization campaign was also conducted in 2007 targeting 9933 non-national students between the ages 15-18 years in several private schools in Muscat governorate and achieved 99.6% coverage.
Rubella disease surveillance
Since the following catch-up campaign conducted and the introduction of RCV1 in 1994, the incidence of rubella has fallen from 45-52 cases per 100,000 population between 1985-1994, to 0-0.06- cases per 100,000 population (1995- 2014) (Figure 5).
As vaccine coverage increased and was maintained above 95% (1994-2014) fewer rubella cases occurred from a mean of <400 cases annually during 1990-1996 to a mean of 8 cases annually during 1997-2006 . By 2007 onward, only 12 cases or less were reported. As part of the national plan for rubella and CRS elimination, a registry of CRS cases was established in 2000, which includes all children with CRS reported to the Ministry of Health since 1988 .
As vaccine coverage increased and maintained above 95% (1994-2014) fewer rubella cases occurred from a mean of <400 cases annually during 1985-1994 to a mean of 8 cases annually during 1995-2006 (Table 1). By 2007 onward, only 12 cases or less was reported totally. As part of the national plan for rubella and CRS elimination, a registry of CRS cases was established in 2000, which includes all children with CRS reported to the Ministry of Health since 1988 .
Since 1995, there have been 49 rubella outbreaks involving 63 cases. These outbreaks were reported from mainly Muscat and South Batina governorates and most cases were imported (63%). 58% were reported from the private non- Omani resident schools in Muscat governorate as well as among children less than 1 year of age (36%) and most of the cases (92%) were unvaccinated.
During 2010–2012, 5 laboratory confirmed rubella cases were identified and classified as endemic rubella cases by the rubella national expert committee (Table 1). Of the confirmed cases identified, all (100%) were below 1 year of age and were too young for rubella vaccine administration. All cases during 2010–2012 were sporadic cases and had genotype 2B related to importation from Southeast Asia.
Figure 5. Rubella and CRS incidence and vaccination coverage (RCV1 and RCV2), Oman, 1985-2014
Table 1. Rubella Surveillance Indicators and Rubella Cases, Oman, 2000-2014.
**TMEC: Technical measles expert committee
Table 2. Congenital Rubella Syndrome (CRS) Surveillance Performance Indicators, Oman, 2000-2014.
Rubella surveillance indicators have been monitored since introduction of case-based surveillance in 1996 nationally and provincially (Table 1). During 2004-2013, the suspect rubella reporting rate has ranged from 0.8 to 30 cases per 100,000 persons, and the timeliness of reporting and investigation of suspect cases have generally been above 95%. All persons with suspected cases investigated have had clinical specimens collected, and transport of specimens to and testing by the national rubella and measles laboratory have been prompt (> 95% and > 95% within 7 days,respectively). Similarly, CRS surveillance indicators have been monitored since 2004 nationally and provincially (Table 2) and achieved > 95% for all indicators. In addition, the central public health laboratory is annually validated and accredited by the WHO since 2000 and the proficiency panel test results were always 100%.
Oman has demonstrated exemplary progress towards elimination of rubella and CRS and has fully committed to the national elimination goal and strategies. As a result, Oman has likely achieved interruption of endemic rubella virus transmission, and therefore rubella and CRS elimination, based on sensitivity of the surveillance system, low incidence of confirmed disease (zero case per million), and limited transmission after detection of a confirmed case .
To achieve these goals, Oman has been engaged in rubella and CRS elimination since 1996, and has implemented the recommended strategies for immunization activities and coverage, case-based surveillance, and clinical care, with great success. Oman has achieved low rubella and CRS incidence with the implementation of two central strategies: a) achieving and sustaining high rubella immunization coverage and maintaining high population immunity, among children and susceptible groups and b) a surveillance system that is highly sensitive. This latter intervention is based on the fact that we adopted a background rate of 2 suspected non-measles non rubella cases per 100,000 population as the indicator of surveillance system sensitivity to detect rubella transmission in a highly vaccinated population, on the basis of global experience with rubella surveillance.
Sustaining high rubella immunization coverage was achieved through routine immunization coverage (MMR1 and MMR2), reaching > 97 % coverage nationally and through catch-up immunization campaigns including school-based campaigns. We have also achieved high rubella coverage in women of childbearing age and in health care workers. Furthermore, supplemental rubella immunization activities are conducted expeditiously in response to any confirmed rubella case to ensure high coverage of 2 doses MMR for individuals living in areas near confirmed cases. All of these different immunization activities have contributed to the achievement of high immunization coverage resulting in elevated population immunity to rubella.
Over the last decade, and as a result of the combined interventions implemented nationwide, Oman has achieved all the targeted rubella surveillance performance indicators for the elimination phase. The achievement of timely and sensitive rubella surveillance in Oman resulted from a close collaboration among the EPI unit, the governorate surveillance units.
Additionally, the progress made in Oman towards rubella and CRS elimination has been facilitated to the successful strategic models such as the strong political commitment to the EPI within MOH across the country to ensure high rubella vaccination coverage levels (>98%) both nationally and provincially has resulted from expansion of EPI at the grass roots level and by integration into the Primary Health system, as well as well-trained regional EPI and epidemiologist, health care workers across the country, and free vaccination services to all residents. The implementation of the EPI policies by the EPI static units located within the health institutions, single administrative control for EPI and supply chain management, integration of EPI services into the ‘Primary Health Care’, a decentralized and self-sustaining system, every opportunity of a child’s contact with the health services to be utilized for immunization. In addition to highly dedicated and professional staff for EPI unit and provision of adequate staff in every health facility and for primary vaccine store management and sensitive and specific surveillance system in Oman has shown a remarkable decline in rubella and CRS.
Rubella incidence in Oman has reached record low levels in the last decade. The average annual number of cases has declined by 99% since the 1975s. All confirmed cases have recovered fully and there have been no deaths attributed to rubella during the last decade. The incidence of rubella has declined to zero cases per million persons in 2014. WHO estimates indicate that globally there are still more than 100,000 new cases of congenital rubella syndrome (CRS) occurring each year [13,14]. In Oman, with the exception of 2013, no CRS have been reported since 2007.
Rubella elimination is facing a number of challenges. The absence of a policy that requires rubella vaccination for migratory workers on work or visa permit presents a challenge in a country where about 44% of the population is expatriates. 92% are above age of 20 years  and coming in and out from high rubella endemic countries and many aren’t not vaccinated or not fully vaccinated. In order to facilitate reducing the immunity gap, the MOH should ask all these individuals to provide evidence of receiving 2 RCV doses. In addition, a huge population is entering Oman with visiting visas, i.e. up to 3 months, and vaccination is not required. Unrestricted border crossing from some countries where many children and adults are unvaccinated is another issue that needs to be considered within the framework of rubella and measles elimination activities.
Despite these challenges, Oman is on track to sustain rubella elimination. Indeed, Oman has met the elimination goals and verification will follow after three years of confirmed interrupted endemic rubella virus transmission. Elimination of rubella will depend largely on maintaining political commitment, achieving and maintain high rubella coverage, closing immunity gaps and ensuring high-quality, case-based surveillance throughout.
Oman has interrupted endemic rubella virus transmission for a period greater than or equal to 12 months with no cases of CRS associated with endemic transmission. To sustain these gains, Oman will need to: a) maintain population immunity; b) maintain and improve surveillance system sensitivity for rubella detection including identification of rubella virus genotypes; and c) continue to conduct prompt investigation and response to rubella cases and case-clusters. In addition, national activities should also identify high-risk areas with concentrations of residence of foreignborn workers from countries where rubella is endemic, identify immunization gaps, and conduct targeted immunization activities among these communities. Finally, establishing an independent verification committee to review the status of rubella elimination activities; and to provide advice on corrective actions, will be a critical step towards certification of achieving and maintaining successful rubella elimination in Oman.
We are in debt to H.E. Dr. Ali Bin Moosa, late Dr. Ali Jaffer Mohammed, H.E. Dr. Ahmed Al Ghassani, Mr. Islam Al Bulushi, Mr. Arumugam Raju, Dr. Shyam Bawikar, Dr. Jeffery Sign, all governorate epidemiologists, Rubella technical expert committee members, NITAG committee members, Dr. Ezzedin Mohsni, Magda Salim Al Wahebi, , Mr. Hossam Ashmony Dr. Saroj M. Sherry, Dr. Nadia Teleb VPI Regional advisor, WHO, EMRO, Dr. Robert D. Allison, Dr. Carlos Franco and Dr. Jim Alexender Global Immunization Division, Centers for Disease Control and Prevention, Atlanta, GA, USA for their vision and support.
Conflict of interest
The authors declare no conflict of interest
Cite this article: Al Awaidy S T. Rubella and Congenital Rubella Syndrome Elimination, the Oman Experience. J J Vaccine Vaccination. 2015, 1(2): 009.