ABSTRACT

This study searched grey literature and PubMed for strategies to sustain the elimination of measles, rubella, and congenital rubella syndrome and prevent their reintroduction in the Caribbean. Strategies were categorized at the macro, meso, and micro health levels. Macro strategies include: strong, clear, unified political and technical leadership and support; country ownership and subregional coordination of resources, policies, and programs; government investment in national immunization programs; and timely payment to the Pan American Health Organization Revolving Fund for affordable, good-quality vaccines. Including the private health sector and health workers in the tourism industry to identify and manage suspected imported cases, and finding and vaccinating every unvaccinated child, university student or frontline worker are key meso strategies. Strong social and communication programs are the key micro strategies needed to promote vaccine confidence and gain public trust. Priority macro strategies include a strengthened legislative framework supporting immunization, and policies to ring-fence the immunization budget, mitigate the rapid turnover of staff, and train new immunization managers. Establishing infrastructure to vaccinate adolescents and adults, including through the private sector, increasing the capacity to test for measles and rubella, and updating digital surveillance systems for timely decision-making are also critical meso strategies to prevent the reintroduction of these diseases. Partnerships, commitment, and collaborative efforts that contribute to elimination must be sustained, and health strategies strengthened to keep the Caribbean free of endemic transmission of measles, rubella, and congenital rubella syndrome.

Keywords
Measles; rubella; rubella syndrome, congenital; vaccination; immunization programs; Caribbean Region

RESUMEN

En este estudio se realizó una búsqueda en la bibliografía gris y en PubMed sobre estrategias para mantener la eliminación del sarampión, la rubéola y el síndrome de rubéola congénita y prevenir su reintroducción en el Caribe. Las estrategias se clasificaron en los niveles de salud macro, meso y micro. Las macroestrategias incluyen: liderazgo y respaldo políticos y técnicos fuertes, claros y unificados; asunción de responsabilidades por parte de los países y coordinación subregional de recursos, políticas y programas; inversión gubernamental en programas nacionales de inmunización; y pago puntual al Fondo Rotatorio de la Organización Panamericana de la Salud para vacunas asequibles y de buena calidad. Las mesoestrategias clave consisten en incluir al sector privado de la salud y a los trabajadores de salud del sector turístico en la detección y el manejo de los casos sospechosos importados, y en encontrar y vacunar a todas las personas no vacunadas de la población infantil, la población universitaria o el personal de primera línea. Las microestrategias clave para promover la aceptación de las vacunas y lograr la confianza del público consisten en programas sociales y de comunicación potentes. Las macroestrategias prioritarias incluyen un fortalecimiento del marco legislativo que respalde la inmunización y políticas para blindar el presupuesto de inmunización, mitigar la elevada rotación de personal y capacitar a nuevos gerentes de los servicios de inmunización. La creación de infraestructuras para la vacunación de la población adolescente y adulta, incluso en el sector privado, el aumento de la capacidad para realizar pruebas de detección del sarampión y la rubéola, y la actualización de los sistemas digitales de vigilancia para la toma de decisiones oportunas son también mesoestrategias fundamentales para prevenir la reintroducción de estas enfermedades. Deben mantenerse las asociaciones, el compromiso y los esfuerzos de colaboración que contribuyen a su eliminación, y deben reforzarse las estrategias de salud orientadas a mantener al Caribe libre de transmisión endémica del sarampión, la rubéola y el síndrome de rubéola congénita.

Palabras clave
Sarampión; rubéola (sarampión alemán); síndrome de rubéola congénita; vacunación; programas de inmunización; Región del Caribe

RESUMO

Este estudo pesquisou na literatura cinzenta e na base de dados PubMed estratégias para manter a eliminação de sarampo, rubéola e síndrome da rubéola congênita e evitar sua reintrodução no Caribe. As estratégias foram agrupadas nos níveis macro, meso e micro do sistema de saúde. Entre as macroestratégias estão: liderança e apoio político e técnico sólidos, explícitos e unificados; apropriação pelos países e coordenação sub-regional de recursos, políticas e programas; investimento do governo em programas nacionais de imunização; e pagamento pontual ao Fundo Rotativo da Organização Pan-Americana da Saúde para vacinas de boa qualidade a preços acessíveis. As principais mesoestratégias são a inclusão da rede privada de saúde e de profissionais de saúde no setor de turismo a fim de identificar e manejar suspeitas de casos importados e localizar e vacinar todas as crianças, estudantes universitários ou trabalhadores na linha de frente não vacinados. A existência de fortes programas sociais e de comunicação são as principais microestratégias necessárias para promover a aceitação das vacinas e conquistar a confiança da população. As macroestratégias prioritárias compreendem o fortalecimento de um marco legislativo em apoio à imunização, além de políticas para proteger o orçamento para a imunização, reduzir a alta rotatividade de pessoal e capacitar novos gestores na área de imunização. Criar uma infraestrutura para vacinar adolescentes e adultos, inclusive por meio do setor privado, aumentar a capacidade de testagem para sarampo e rubéola e atualizar os sistemas digitais de vigilância para que as decisões sejam tomadas em tempo hábil também são mesoestratégias essenciais para evitar a reintrodução dessas doenças. É preciso manter parcerias, compromissos e esforços colaborativos que contribuam para a eliminação e fortalecer as estratégias de saúde a fim de manter o Caribe livre da transmissão endêmica de sarampo, rubéola e síndrome da rubéola congênita.

Palavras-chave
Sarampo; rubéola (sarampo alemão); síndrome da rubéola congênita; vacinação; programas de imunização; Região do Caribe

The English-speaking Caribbean has an impressive record of eliminating diseases preventable by vaccination: it was the first subregion in the world to eliminate poliomyelitis in 1982, measles in 1991, diphtheria in 1995, congenital rubella syndrome (CRS) in 1999, and rubella in 2000 (¹1. Smith H, Irons B. The Expanded Program on Immunization (EPI). In: the CAREC story. The Caribbean Epidemiology Centre: contributions to public health 1975–2012. Washington, D.C: Pan American Health Organization; 2017 [cited 2023 Dec 14]. Available from: https://www.paho.org/spc-crb/dmdocuments/history-of-carec/The%20EPI.pdf
https://www.paho.org/spc-crb/dmdocuments... –³3. Irons B, Smith HC, Carrasco PA, De Quadros C. The immunisation programme in the Caribbean. Caribb Health. 1999;2(3):9–11.) (Table 1). These achievements paved the way for the elimination of rubella (2015) and measles (2016) in the Americas (⁴4. Pan American Health Organization and World Health Organization Region of the Americas. Region of Americas is declared free of measles. PAHO and WHO; 2016 [cited 2023 Dec 13]. Available from: https://www.paho.org/en/news/27-9-2016-region-americas-declared-free-measles#:~:text=Washington%2C%20D.C.%2C%2027%20September%202016,brain%20swelling%20and%20even%20death
https://www.paho.org/en/news/27-9-2016-r... ). Measles is endemic in many countries and has re-emerged in countries where it was previously eliminated (⁵5. Borba RC, Vidal VM, Moreira LO. The re-emergence and persistence of vaccine preventable diseases. An Acad Bras Cienc. 2015;87(2 Suppl):1311–22. https://doi.org/10.1590/0001-3765201520140663
https://doi.org/10.1590/0001-37652015201... ). Nevertheless, the Caribbean remains measles- and rubella-free despite an influx of millions of tourists annually.

The 25 Dutch- and English-speaking Caribbean Community (CARICOM) countries, territories, and municipalities have a combined population of about 8 million people and host a large transitory population of tourists. After international travel restrictions were lifted after the coronavirus disease 2019 (COVID-19) pandemic, the Caribbean recorded 28.3 million registered tourist visits in 2022, 50% more than in 2021 (⁶6. Caribbean tourism performance press conference. Caribbean Tourism Organization; 2023 [cited 2023 Dec 16]. Available from: https://www.onecaribbean.org/events-calendar/caribbean-tourism-performance-outlook-press-conference/
https://www.onecaribbean.org/events-cale... ). The risk of importation of vaccine-preventable diseases increases with travelers coming from endemic areas. While there has been no evidence of circulation of the measles virus since the last endemic case in 1991 in Dutch- and English-speaking Caribbean areas (Table 1), imported measles cases have tested the robustness of the immunization program in the Caribbean for 3 decades. Without a global target for elimination (⁷7. Durrheim DN, Bashour H. Measles eradication. Lancet. 2011;377(9768):808; author reply 809–10. https://doi.org/10.1016/S0140-6736(11)60299-7
https://doi.org/10.1016/S0140-6736(11)60... ), the influx of tourists and gaps in immunity and surveillance exacerbated by the COVID-19 pandemic make the Caribbean vulnerable to the reintroduction of measles and other vaccine-preventable diseases. This paper reviews measles elimination in the Caribbean subregion since 1991, including best practices contributing to sustainability of measles elimination, challenges, and lessons learnt, focusing on key elements of measles, rubella, and CRS elimination and sustainability (what happened in the past) and challenges and strategies to prevent reintroduction (what is expected to happen in the future).

METHODS

Data were gathered by searching the grey literature and PubMed. In the grey literature search, the Iris site of the Pan American Health Organization (PAHO) was used to identify technical reports using the keywords measles, rubella, CRS elimination, and Caribbean. Reports on measles and rubella from oversight committees were reviewed, and interviews were conducted with Caribbean experts. The PubMed search strategy used the Medical Subject Headings (MeSH): (measles) AND (Caribbean region) AND (prevention and control) [All fields] and (rubella) OR rubella syndrome, congenital AND (Caribbean region) AND (prevention and control) [All fields]. The approach to sustaining measles, rubella, and CRS elimination and strategies to prevent re-introduction were analyzed.

The strategies were stratified into macro, meso, and micro health levels. The macro level relates to subregional and national policies, governance, and health financing development (⁸8. Caldwell SE, Mays N. Studying policy implementation using a macro, meso and micro frame analysis: the case of the Collaboration for Leadership in Applied Health Research & Care (CLAHRC) programme nationally and in North West London. Health Res Policy Syst. 2012;10:32. https://doi.org/10.1186/1478-4505-10-32
https://doi.org/10.1186/1478-4505-10-32... ). The meso level relates to health strategies to operationalize and implement policies through the intersectoral and integrated health services networks (⁸8. Caldwell SE, Mays N. Studying policy implementation using a macro, meso and micro frame analysis: the case of the Collaboration for Leadership in Applied Health Research & Care (CLAHRC) programme nationally and in North West London. Health Res Policy Syst. 2012;10:32. https://doi.org/10.1186/1478-4505-10-32
https://doi.org/10.1186/1478-4505-10-32... , ⁹9. Légaré F, Stacey D, Gagnon S, Dunn S, Pluye P, Frosch D, et al. Validating a conceptual model for an inter-professional approach to shared decision making: a mixed methods study. J Eval Clin Pract. 2011;17(4):554–64. https://doi.org/10.1111/j.1365-2753.2010.01515.x
https://doi.org/10.1111/j.1365-2753.2010... ). The micro level describes service delivery interface with communities (⁸8. Caldwell SE, Mays N. Studying policy implementation using a macro, meso and micro frame analysis: the case of the Collaboration for Leadership in Applied Health Research & Care (CLAHRC) programme nationally and in North West London. Health Res Policy Syst. 2012;10:32. https://doi.org/10.1186/1478-4505-10-32
https://doi.org/10.1186/1478-4505-10-32... , ¹⁰10. Plochg T, Klazinga NS. Community-based integrated care: myth or must? Int J Qual Health Care. 2002;14(2):91–101. https://doi.org/10.1093/oxfordjournals.intqhc.a002606
https://doi.org/10.1093/oxfordjournals.i... ).

RESULTS

Table 2 summarizes macro, meso, and micro health strategies to sustain the elimination of measles, rubella, and CRS and prevent their reintroduction.

Macro health strategies

Key strategies for sustaining the elimination of measles, rubella, and CRS include technical leadership, international partnerships, commitment from members of CARICOM, immunization legislation and policies on school-aged vaccination, national financing, and the PAHO revolving fund. Government commitment to invest in Expanded Programme on Immunization (EPI) programs and strengthen immunization legislation are necessary to prevent the reintroduction of vaccine-preventable diseases. Also important are policies to reduce the turnover of EPI managers and train new managers and staff.

Meso health strategies

Effective public health strategies for population immunity, high vaccine coverage, and surveillance were achieved through integrated networks in schools, day-care centers, the hotel cruise ship industry, immigration, and the private sector (e.g., pediatricians), coupled with program incentives. Partnerships with the airlines to ensure timely delivery of laboratory samples, increasing laboratory testing capacity, improving infrastructure for adolescent and adult immunization, and digitalizing EPI registries are needed to strengthen sustainability efforts.

Micro health strategies

Sustainability strategies focus on gaining public trust through social mobilization and communication programs. Community health workers know the children in island states with small populations, so fostering relationships with families and community leaders and motivating involvement in immunization activities is easier. Outreach activities, later opening hours, and weekend clinics are service delivery strategies to reach defaulters. Culturally relevant messaging and digitalized tracking and contact of defaulters can enhance sustainability efforts.

DISCUSSION

Key elements of measles, rubella, and CRS elimination and sustainability

Leadership and support. Caribbean countries eliminated measles, rubella, and CRS with the last indigenous cases reported in 1991, 2000 and 1998, respectively (Table 1). The work to achieve these goals was under the leadership of Dr. Ciro de Quadros, team leader of PAHO’s EPI from 1977 to 2002, the technical team that worked with him, and the leaders of the country programs. Both Dr. de Quadros and Mr. Henry Smith, the first Immunization Officer for the Caribbean (1977–1995), gained experience through smallpox eradication in Africa. Dr. de Quadros and his team worked with the EPI managers and their teams to test elimination strategies for polio in the small island populations and built on this experience to eliminate measles, rubella, and CRS. The technical leadership to support the elimination agenda was strong, clear, and unified. It emphasized country ownership to ensure a sustainable EPI infrastructure to deliver routine vaccination, implement surveillance, and focus on eliminating one disease at a time. PAHO provided technical assistance, surveillance, and laboratory support through the Caribbean Epidemiology Centre (CAREC), and several international agencies and nongovernmental organizations provided valuable support in funding, vaccines, supplies, and cold chain equipment (¹1. Smith H, Irons B. The Expanded Program on Immunization (EPI). In: the CAREC story. The Caribbean Epidemiology Centre: contributions to public health 1975–2012. Washington, D.C: Pan American Health Organization; 2017 [cited 2023 Dec 14]. Available from: https://www.paho.org/spc-crb/dmdocuments/history-of-carec/The%20EPI.pdf
https://www.paho.org/spc-crb/dmdocuments... –³3. Irons B, Smith HC, Carrasco PA, De Quadros C. The immunisation programme in the Caribbean. Caribb Health. 1999;2(3):9–11.).

On the retirement of Henry Smith, Caribbean advisers to the EPI program came to play important roles in supporting and sustaining measles, rubella, and CRS elimination for more than 2 decades.

Commitment of CARICOM member states. To understand the success of disease elimination and its sustainability, one needs to understand the role of CARICOM and its Council for Human and Social Development (COHSOD) which sets regional goals and coordinates subregional efforts. Caribbean governments committed resources for their EPI programs and elimination and sustainability efforts. Governments provide 90–100% of the cost of the immunization program. There was horizontal cooperation among countries and costed annual national plans of action. COHSOD, with technical guidance and support of PAHO and the World Health Organization (WHO), proposed resolutions to eliminate, in turn, polio, measles, rubella, and CRS from the Caribbean through coordinated, simultaneous mass vaccination catch-up and follow-up campaigns (¹¹11. Evans-Gilbert T, Lewis-Bell KN, Figueroa JP. The Caribbean Immunization Technical Advisory Group (CITAG): a unique NITAG. Vaccine. 2019;37(44):6584–7. https://doi.org/10.1016/j.vaccine.2019.09.032
https://doi.org/10.1016/j.vaccine.2019.0... ). Most countries mandated vaccination for school entry through legislation under the education, public health, or free-standing vaccination acts (¹²12. Evans-Gilbert T, Lewis-Bell KN, Irons B, Duclos P, Gonzalez-Escobar G, Ferdinand E, et al. A review of immunization legislation for children in English- and Dutch-speaking Caribbean countries. Rev Panam Salud Publica. 2023;47:e19. https://doi.org/10.26633/RPSP.2023.19
https://doi.org/10.26633/RPSP.2023.19... ). After the last case of polio was recorded in the English-speaking Caribbean in 1982, CARICOM health ministers resolved in 1988 to eliminate measles by 1995 and rubella and CRS by the end of 2000. The PAHO technical adviser, in collaboration with the CARICOM secretariat, gives an annual report on sustaining measles, rubella and CRS elimination to the ministers responsible for health in CARICOM. Further commitment to sustaining elimination gains was evident when health ministers of the Caribbean agreed to strengthen national immunization programs in the Declaration of Nassau in 2023 (¹³13. Pan American Health Organization. Countries of the Caribbean agree to strengthen national immunization programs through Declaration of Nassau. PAHO; 2023 [cited 2023 Dec 16].Available from: https://www.paho.org/en/news/27-4-2023-countries-caribbean-agree-strengthen-national-immunization-programs-through
https://www.paho.org/en/news/27-4-2023-c... ).

PAHO revolving fund for vaccines. The PAHO/WHO revolving fund for vaccines allows countries that require relatively small quantities of vaccines to access high-quality vaccines at significant cost savings of up to 90%, with timely delivery and a 60-day line of credit. This fund was put into operation in 1978 and vaccines required for South and Central America and the Caribbean are ordered through a tender system from WHO prequalified manufacturers (¹1. Smith H, Irons B. The Expanded Program on Immunization (EPI). In: the CAREC story. The Caribbean Epidemiology Centre: contributions to public health 1975–2012. Washington, D.C: Pan American Health Organization; 2017 [cited 2023 Dec 14]. Available from: https://www.paho.org/spc-crb/dmdocuments/history-of-carec/The%20EPI.pdf
https://www.paho.org/spc-crb/dmdocuments... –³3. Irons B, Smith HC, Carrasco PA, De Quadros C. The immunisation programme in the Caribbean. Caribb Health. 1999;2(3):9–11.).

Effective public health strategies for population immunity. Within the Caribbean subregion, vaccination of children is mainly done by the public health sector free of charge through their network of clinics. The private sector administers vaccines to about 10% of each birth cohort.

Population immunity was achieved after large measles outbreaks during 1981–1990, with more than 43 000 cases reported, mainly in Bahamas, Guyana, Jamaica, and Trinidad and Tobago. An average of 4 814 cases were recorded annually, with 18 deaths. The measles elimination strategy devised by PAHO included: (i) a mass vaccination campaign (catch-up) targeting all children aged 9 months to 14 years; (ii) improvement of surveillance for monitoring the progress of measles elimination; (iii) routine measles vaccination coverage of 95% in each birth cohort; and (iv) follow-up vaccination campaigns to avoid an accumulation of susceptible children equivalent to the birth cohort (¹⁴14. de Quadros CA, Hersh BS, Nogueira AC, Carrasco PA, da Silveira CM. Measles eradication: experience in the Americas. Bull World Health Organ. 1998;76 Suppl 2):47–52.).

During the so-called Big Bang in May 1991, 94% of the targeted 1.9 million children aged 9 months to 14 years were vaccinated in that month. Since this mass catch-up campaign, high routine vaccine coverage has been maintained through so-called keep-up and follow-up campaigns and outreach vaccination activities. The natural immunity that occurred in 1981–1990 due to the measles outbreaks, high vaccination coverage, and periodic mass campaigns ensured the sustainability of measles elimination (¹⁵15. Irons B, Dobbins JG; Caribbean Vaccine Managers. The Caribbean experience in maintaining high measles vaccine coverage. J Infect Dis. 2011;204(Suppl 1):S284–8. https://doi.org/10.1093/infdis/jir212
https://doi.org/10.1093/infdis/jir212... ).

Rubella immunization and elimination were economically justified (¹⁶16. Hinman AR, Irons B, Lewis M, Kandola K. Economic analyses of rubella and rubella vaccines: a global review. Bull World Health Organ. 2002;80(4):264–70) and the following strategies were implemented: mass vaccination of children and adults of both sexes aged 1–39 years using a measles-containing vaccine; surveillance of fever and rash and CRS; and vaccination of 95% of each birth cohort using two doses of the measles–rubella or mumps–measles–rubella (MMR) vaccine. A mass vaccination campaign targeting adults was conducted to ensure women in the reproductive age group were immune to rubella, thereby preventing CRS in infants of susceptible women. Natural immunity in previous rubella outbreaks protected most adults older than 40 years. Figure 1 outlines rubella and measles elimination and sustainability in the English-speaking Caribbean countries and Suriname. The graph shows a multifaceted approach at macro, meso, and micro levels, including sustaining measles and rubella vaccine coverage with follow-up and catch-up campaigns, fever and rash surveillance, and political resolution to eliminate measles and rubella and sustain their elimination.

The same strategies used in elimination are also used for sustaining elimination. These include maintaining high coverage in birth cohorts, school-aged populations (including at the tertiary education level), immigrants, and frontline workers in tourism and health, and strong government commitment.

Vaccine coverage. Maintaining high vaccination coverage is essential to sustain elimination status. Vaccination coverage of 95% or more for vaccines administered is the goal for each country. Vaccination is done in the countries through fixed sites and outreach activities, along with identification and vaccination of drop-outs at home. In countries such as Belize, Guyana, and Suriname emphasis was placed on enhanced vaccination activities at border communities with collaborative actions across neighboring countries. In all countries, focus was placed on areas with high population density and communities with tourists. Vaccines are given at no cost at public health facilities and at some private health clinics in most countries. In almost all countries, the private health sector receives vaccines from the Government sector free or at cost, thereby allowing better access to vaccination in the private sector. Private clinics must submit reports of vaccines given to collect a new supply of vaccines.

The elimination strategy introduced a second dose of measles and rubella-containing vaccine in 1996 to ensure that all vaccinated children developed immunity (¹⁶16. Hinman AR, Irons B, Lewis M, Kandola K. Economic analyses of rubella and rubella vaccines: a global review. Bull World Health Organ. 2002;80(4):264–70). The second dose was usually administered between ages 3 and 6 years years. In keeping with the recommendations of PAHO’s Technical Advisory Group on immunization to improve immunity against measles, between 2016 and 2018, Caribbean countries reduced the age to receive the MMR2 vaccine to the second year of life. Eighteen of the 25 CARICOM countries and areas now give this vaccine between 15 and 24 months.

Countries procure vaccines through the PAHO revolving fund for vaccines, which ensures access to affordable, high-quality vaccines. In the spirit of Pan-Americanism, countries are willing to lend vaccines to other countries when needed, knowing that the vaccines can be repaid through the revolving fund.

Coverage of the MMR1 vaccine in the Caribbean declined from 96% in 2015 to 91% in 2017, with improvements made over the next 2 years (Table 3). From 2010 to 2019, MMR2 coverage ranged between 79% and 92%. A precipitous fall occurred in both MMR1 and MMR2 coverage in 2020 and 2021 due to the prioritization of activities related to COVID-19 control and closure of health facilities used as centers for respiratory infections. Countries have subsequently implemented catch-up and community outreach activities to find and vaccinate defaulters to improve coverage levels. However, the coverage data have not been consistently recorded for the respective birth cohorts following these campaigns, leading to an underestimation of MMR coverage.

Immunization legislation. Legislation has played an important role in the elimination strategy in the Caribbean and the Americas. Nearly all countries have policies or legislation requiring children to be vaccinated for school entry; some include day-care and preschool institutions (¹²12. Evans-Gilbert T, Lewis-Bell KN, Irons B, Duclos P, Gonzalez-Escobar G, Ferdinand E, et al. A review of immunization legislation for children in English- and Dutch-speaking Caribbean countries. Rev Panam Salud Publica. 2023;47:e19. https://doi.org/10.26633/RPSP.2023.19
https://doi.org/10.26633/RPSP.2023.19... ). Some countries need to enact legislation. Measles and rubella vaccination is required for students attending most tertiary institutions and for persons immigrating to countries. A strengthened legislative framework is required for almost all countries.

Effective public health strategies to improve surveillance. Finding and vaccinating every child and finding and investigating every suspected case are the key to sustaining elimination. Before measles elimination, case-based surveillance was used for reporting measles cases. As part of the measles elimination strategy, the surveillance system was strengthened to improve sensitivity and ensure routine weekly reporting on suspected cases from a wide cross-section of hospitals and clinics in both the public and private health sectors, including negative reporting. Laboratory diagnosis and community investigations using standard reporting and investigation forms are integral to case detection and control (¹⁷17. Irons B, Morris-Glasgow V, Andrus JK, Castillo-Solórzano C, Dobbins JG; Caribbean Surveillance Group. Lessons learned from integrated surveillance of measles and rubella in the Caribbean. J Infect Dis. 2011;204(Suppl 2):S622–6. https://doi.org/10.1093/infdis/jir437
https://doi.org/10.1093/infdis/jir437... ). Software developed by PAHO was used to report suspected cases by CAREC and PAHO and prepare weekly surveillance bulletins (¹⁸18. Irons B, Carrasco P, Morris-Glasgow V, Castillo-Solórzano C, de Quadros CA. Integrating measles and rubella surveillance: the experience in the Caribbean. J Infect Dis. 2003;187(Suppl 1):S153–7. https://doi.org/10.1086/368031
https://doi.org/10.1086/368031... ). As immunization coverage improved and measles and rubella cases declined, a more sensitive case definition was needed. A suspected measles case was initially defined as fever, rash, and one of either cough, coryza, or conjunctivitis. With the integration of measles and rubella surveillance, a suspected case is now defined as a case of fever and generalized rash. Blood specimens are required to confirm the diagnosis of measles and rubella. At the first contact of the case with the health sector, an investigation form is completed and specimen(s) are taken for diagnostic purposes. This first contact strategy allows for early diagnosis and follow-up.

CRS surveillance was enhanced in 2004 with the investigation and follow-up of neonates and infants whose specimens were submitted for TORCH testing. Some countries routinely screen pregnant women for rubella antibodies and vaccinate those testing negative in the postpartum period.

Weekly review of the investigation forms, identifying the areas requiring strengthening, and working with countries to amend deficits in clinical information and investigations are ongoing activities. The number of surveillance sites in countries in both public and private health sectors continues to expand. Almost all imported measles or rubella cases visit private health facilities for care. Therefore, training and awareness activities are essential for the private health sector. Hotels and cruise ship ports are used as surveillance sites for fever and rash cases, and they also report weekly in some countries.

During 1991–2020, nine imported and one import-related cases of measles were reported in seven countries: Barbados (1991), Trinidad and Tobago (1997), Jamaica (2011), Antigua and Barbuda (2018), and Bahamas, Curacao and Saint Lucia (2019) (Table 1). The last imported measles case was reported by Saint Lucia in a cruise ship crew member infected in Denmark with genotype D8. All imported cases were from Europe. Bermuda reported one imported rubella case in 2008. All these imported cases were tourists, identified primarily within the private sector, where the first contact strategy used for measles elimination in the Caribbean was implemented. In this strategy, specimens are taken for diagnosis at first contact with the health sector, an investigation report is completed, and the persons are isolated. The inclusion of the private health sector and health-care workers in the tourism sector are key strategies used by all countries. Public–private partnership played and continues to play a pivotal role in the sustainability of measles, rubella and CRS elimination.

Social mobilization. Social mobilization occurs annually during vaccination week in April as a strategy for sustaining elimination. This week includes catch-up and public outreach activities, which facilitate sensitization in schools, communities, and workplaces. These activities during vaccination week use social media, health fairs, and community and school awareness through skits and songs. These activities need to be sustained and their impact evaluated.

Program incentives – awards. Two awards are presented to countries at the annual EPI managers’ meeting as incentives for improving surveillance and vaccination coverage (¹1. Smith H, Irons B. The Expanded Program on Immunization (EPI). In: the CAREC story. The Caribbean Epidemiology Centre: contributions to public health 1975–2012. Washington, D.C: Pan American Health Organization; 2017 [cited 2023 Dec 14]. Available from: https://www.paho.org/spc-crb/dmdocuments/history-of-carec/The%20EPI.pdf
https://www.paho.org/spc-crb/dmdocuments... ). Countries are encouraged to have annual evaluation meetings and institute similar awards nationally. These can stimulate competition and help to strengthen surveillance and vaccination coverage.

Oversight committees. The Caribbean Commission for Monitoring and Re-verification of Measles and Rubella Elimination, established in 2018, has provided oversight to ensure the sustainability of measles elimination. The Caribbean Immunization Technical Advisory Group established by CARICOM in 2018 (¹¹11. Evans-Gilbert T, Lewis-Bell KN, Figueroa JP. The Caribbean Immunization Technical Advisory Group (CITAG): a unique NITAG. Vaccine. 2019;37(44):6584–7. https://doi.org/10.1016/j.vaccine.2019.09.032
https://doi.org/10.1016/j.vaccine.2019.0... ) provides technical guidance and oversight of the immunization programs. This group has proposed model immunization legislation (¹²12. Evans-Gilbert T, Lewis-Bell KN, Irons B, Duclos P, Gonzalez-Escobar G, Ferdinand E, et al. A review of immunization legislation for children in English- and Dutch-speaking Caribbean countries. Rev Panam Salud Publica. 2023;47:e19. https://doi.org/10.26633/RPSP.2023.19
https://doi.org/10.26633/RPSP.2023.19... ), which CARICOM has agreed to support. At these oversight committee meetings and the annual meetings of Caribbean EPI managers, priority discussions include disease elimination and strategies to sustain the gains. Challenges in these programs are discussed and recommendations to strengthen EPI programs, close immunity gaps, and improve surveillance indicators are made to the policy-makers in countries.

CARICOM leadership in sustaining the elimination of measles, rubella, and CRS. The history of eliminating measles, rubella, and CRS in the Caribbean is integral to the sustainability of the program. Resolutions and decisions are taken by the most senior health officials, the ministers responsible for health in the respective countries. Decisions are usually accompanied by the required funding. Health teams demonstrate buy-in and advocate with their policy-makers before resolutions are made. The strategy of having CARICOM set elimination goals presents a collective, collaborative, coordinated, and unified approach to decision-making and implementation of activities.

Challenges and strategies to prevent reintroduction

Building vaccine confidence. Decades after elimination, most of the population, including many health providers, are unaware of the morbidity and mortality caused by measles and rubella, and social acceptance of childhood vaccination has decreased. This situation, along with misinformation to discredit the benefits of vaccination, has increased vaccine hesitancy in some people. Social mobilization and advocacy are now crucial to keep the prevention of these diseases to the fore among the population and health-care workers.

Strong social and communication programs are needed to create public trust and promote the value of vaccines to complement evidence-based public health strategies. Community engagement can offer insights into low uptake and can investigate gaps between intention and action to vaccinate to enable better design of interventions. Using social and commercial marketing principles, evidence-based best practices, engagement with communication professionals and community stakeholders, and culturally relevant messaging, innovative strategies can be developed to better inform and mobilize communities (¹⁹19. Nowak GJ, Gellin BG, MacDonald NE, Butler R; SAGE Working Group on Vaccine Hesitancy. Addressing vaccine hesitancy: the potential value of commercial and social marketing principles and practices. Vaccine. 2015;33(34):4204–11. https://doi.org/10.1016/j.vaccine.2015.04.039
https://doi.org/10.1016/j.vaccine.2015.0... ). The aim is for Caribbean people to perceive immunization services positively, as a social norm and a right, and necessary to protect their health. The involvement of all sectors of society will help improve vaccine uptake (²⁰20. Findley SE, Sanchez M, Mejia M, Ferreira R, Pena O, Matos S, et al. Effective strategies for integrating immunization promotion into community programs. Health Promot Pract. 2009;10(2 Suppl):128S–37S. https://doi.org/10.1177/1524839909331544
https://doi.org/10.1177/1524839909331544... ).

Addressing rapid turnover of EPI managers and staff. A committed cadre of vaccination staff and community outreach workers responsible for a defined number of children fosters sustainability. Rapid turnover of EPI managers and staff threatens this process. Recommended strategies to handle the migration of the health workforce have been described and need to be applied (²¹21. International Organization for Migration. The migration of health care workers: creative solutions to manage health workforce migration. In: Seminar on Health and Migration, 9–11 June 2004 [cited 2023 Dec 16]. Available from: https://www.iom.int/jahia/webdav/site/myjahiasite/shared/shared/mainsite/microsites/IDM/workshops/Health_and_Migration_09110604/se3_conf_globaloverview.pdf
https://www.iom.int/jahia/webdav/site/my... ).

Laboratory services. The Caribbean has faced a challenge to meet the surveillance indicator of 80% of samples received in the reference laboratory within 5 days and only met this target in 2016 and 2019 (Table 4). The CARPHA laboratory in Trinidad and Tobago conducts the measles and rubella testing for English-speaking countries and areas as well as for Haiti and Honduras. As countries have to pay to send samples by air to CARPHA, samples are batched and sent weekly. Bermuda uses a reference laboratory in the United States, and Dutch-speaking countries send samples to the Kingdom of the Netherlands or French Saint Martin. In islands with small populations, there are not enough cases to ensure laboratory competency in each island, and larger islands such as Jamaica need to ensure capacity for measles and rubella testing. Shipping agreements paid through CARICOM as part of trade and transport agreements should be put in place to facilitate the transport of samples (²²22. Caribbean Community. Revised Treaty of Chagauramas establishing the Caribbean Community including the CARICOM single market economy. Georgetown; CARICOM Secretariat; 2001 [cited 2023 Dec 16].Available from: https://www.jacustoms.gov.jm/sites/default/files/docs/TradeAgreements/revised_treaty-text.pdf
https://www.jacustoms.gov.jm/sites/defau... ).

Legislation to ring-fence the EPI budget. Despite the political commitment in Caribbean countries to support EPI programs, challenges exist in ensuring timely payments for vaccines and supplies. Continued advocacy is needed to ensure that program funds are protected. Legislation to ring-fence the budget for vaccine programs is also needed.

Lessons from COVID-19 for sustainability. The decline in EPI programs and other essential health services during the COVID-19 pandemic highlighted the importance of maintaining these services during disasters. Exploring evidence-based strategies to strengthen health systems during subsequent natural disasters will help limit future disruption to EPI programs (²³23. World Health Organization. WHO guidance on research methods for health emergency and disaster risk management. Geneva: WHO; 2021 [cited 2023 Dec 29]. Available from : https://iris.who.int/handle/10665/345591
https://iris.who.int/handle/10665/345591... ). Most Caribbean countries need to establish an infrastructure for adolescent and adult vaccination that includes the private health sector, where about 50% of the adult population access primary health care. During the COVID-19 pandemic, the public sector nurses who do childhood vaccinations were called on to vaccinate adults and EPI vaccination coverage fell.

Digitalizing EPI and surveillance systems. The digitalization of national immunization registers, surveillance of vaccine-preventable diseases, and adverse events supposedly attributable to vaccines or immunization will significantly improve the efficiency and productivity of health staff and facilitate the inclusion of new vaccines in the EPI program, enhancing the scope of diseases for which it can offer protection.

Conclusions

Measles, rubella, and CRS elimination was established in the Caribbean through strong leadership, cooperation, coordinated public health measures, and vaccine confidence. Growing misinformation and vaccine hesitancy have created a need for immunization programs to develop strategies to create vaccine confidence and bridge immunity gaps exacerbated by the COVID-19 pandemic. Countries must invest more in EPI programs, including adolescent and adult vaccination infrastructure, multisectoral involvement (e.g., hotels and cruises for surveillance), and digitalization of EPI and surveillance systems for timely decision-making. Legislation that contributes to eliminating several vaccine-preventable diseases in the Caribbean needs to be strengthened. Stronger immunization programs will ensure the sustainability of measles elimination and set the stage for future elimination targets.

Disclaimer.

The authors hold sole responsibility for the views expressed in the manuscript, which may not necessarily reflect the opinions or policies of the Revista Panamericana de Salud Pública/Pan American Journal of Public Health, the Pan American Health Organization and the World Health Organization or the US Centers for Disease Control and Prevention or the Department of Health and Human Services.

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