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Yellow fever risk assessment in the Central African Republic

Alberto Novaes Ramos Junior

a,

* and Jorg Heukelbach

b,c

a

Department of Community Health, School of Medicine, Federal University of Ceara´, Brazil;bDepartment of Community Health, School of

Medicine, Federal University of Ceara´, Brazil;cAnton Breinl Centre for Public Health and Tropical Medicine, School of Public Health, Tropical

Medicine and Rehabilitation Sciences, James Cook University, Townsville, Australia

*Corresponding author: Present address: Rua Professor Costa Mendes, 1608, 58andar, Rodolfo Teo´filo, 60430–140, Fortaleza, Ceara´, Brazil. Tel:+55 85 3366 8045; E-mail: novaes@ufc.br

Received 2 December 2014; revised 1 February 2015; accepted 4 February 2015

Yellow fever still causes high burden in several areas of sub-Saharan Africa and Latin America. There are few well-designed epidemiological studies and limited data about yellow fever in Africa. Staples et al., in a recently pub-lished paper inTransactions of the Royal Society of Tropical Medicine & Hygiene, performed a nationwide study in the Central African Republic (CAR) assessing infection risk and the operational impact of preventive measures. The rapid assessment of human, non-human and mosquito data call attention to the potential risk of future yellow fever outbreaks in the CAR and elsewhere. The study reinforces the need for intensified applied and operational research to address problems and human capacity needs in the realm of neglected tropical diseases in the post-2015 agenda.

Keywords:Central African Republic, Epidemiology, Yellow fever

Yellow fever is a vector-borne flavivirus infection affecting both humans and non-human primates in sub-Saharan Africa and Latin America.1–3In 2013, 230 cases of yellow fever and 85 yellow

fever related deaths were reported from four countries in Africa (Cameroon, Ethiopia, Sudan and Democratic Republic of Congo) and from two countries in South America (Peru and Colombia).1

A recent study estimated that in outbreak situations there may be 9 (95% CI 1 to 70) infections for each severe case identified that are either asymptomatic or cause mild disease.4

In 2013, there was an estimated 130 000 cases in Africa (95% CI 51 000 to 380 000) with fever and jaundice or haemorrhage, including 78 000 (95% CI 19 000 to 180 000) deaths.3Control

actions focus on reduction of disease risk and mortality, and depend on sustained operational efforts, including prevention through personal protective measures and vaccination.1,2,4

Despite the availability of a highly effective vaccine, low vaccin-ation coverage remains a challenge in endemic areas.1,2For

example, in Brazil, outbreaks of yellow fever have been reported in non-vaccinated populations, which led to the revision of national protocols for defining yellow fever risk areas.5,6

In sub-Saharan Africa, control actions based on large-scale vac-cination during the 1940s to 1960s reduced significantly the case emergence of yellow fever for several decades. However, after a period of low vaccination coverage, yellow fever has resurged on the continent.3Since 2008, an increase in yellow fever virus (YFV) circulation has been reported in Africa (Central African Republic [CAR] and Cameroon) and the Americas (Argentina, Brazil, Colombia, Venezuela, and Trinidad and Tobago).3,7

Prevention and control of yellow fever requires detailed eco-epidemiological studies on the different transmission cycles. A group of experts developed a multidisciplinary risk assessment tool, including serological surveys in human and non-human pri-mates, and assessment of vector density and infectivity.7In this context, Staples et al. (2014) conducted in the CAR the first nationwide epidemiological evaluation of yellow fever since the 1970s.8 After registration of an unprecedented number of laboratory-confirmed cases of yellow fever in CAR in 2008/2009 in multiple outbreaks, WHO experts developed a comprehensive study of YFV activity (using this risk assessment tool) to estimate the potential disease risk and vaccine needs in the country.8

The authors used a multistage cluster sampling design for humans, non-human primates and mosquitoes in five distinct ecologic zones within CAR.8In all sampled areas, evidence of yel-low fever infections in humans was found and the presence of known vectors and non-human primate hosts was confirmed.8

In total, 13.3% (125/938) of randomly sampled residents had nat-urally acquired antibodies against YFV, varying by geographical area.8The authors found that human yellow fever infections had increased during the 3 years prior to the assessment. Interestingly, the areas with a higher prevalence of yellow fever antibodies in 2009 corresponded to locations with cases in 2008 and 2009, suggesting epidemiological effect of transmission rather than operational effects caused by improvements of sur-veillance actions.8

Almeida et al. (2014) presented a systematic analysis of sur-veillance data to evaluate vaccine coverage, timeliness of

#The Author 2015. Published by Oxford University Press on behalf of Royal Society of Tropical Medicine and Hygiene. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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doi:10.1093/trstmh/trv011 Advance Access publication 1 March 2015

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registration, investigation and confirmation of epizootic events in relation to occurrence of human cases of yellow fever in Brazil.9 The implementation of epizootic surveillance in risk areas may also be useful in CAR for directing the efforts of vaccine distribution.

The intensity of contacts and the interaction between primates and vectors depend on the degree of human intervention in the environment, especially increasing the extension of critical areas where mosquitoes are easily biting at the ground level. Staples et al. reinforce the complex relationships between biotopes, arbo-virus vectors and vertebrate hosts, defining epidemiological pat-terns and transmission dynamics in endemic areas.2,9They clarified potential risk scenarios in CAR, including the presence of competent vectors, elevated indices ofAedes aegypti, presence of primates as animal resevoirs, presence of naturally acquired antibodies in humans and primates, and increase of YFV sero-prevalence in the 3 years before the assessment. Of 1300 survey participants, only 484 (37.2%) were seroprotected.8

Ngoagouni et al. (2012) identified previously a wide diversity of vector species for YFV in the CAR. Their study indicated that the establishment of surveillance and vector control programmes should take into account the ecological specificity of each spe-cies.10A. aegyptiis re-emerging into regions from which it has

pre-viously been eliminated.2

A recent study estimated that mass vaccination campaigns have reduced the number of cases and deaths by 27% across the African region, with up to 82% reduction in countries targeted by these campaigns.3

The integrated analysis of human, non-human and mosquito data in this assessment indicate the risk of future yellow fever out-breaks in some areas of the CAR, despite no circulating virus detected in mosquitoes during the dry season and few partici-pants having YFV IgM antibodies as an indicator for recent infec-tion.8This risk assessment methodology presented in this paper

translates a complex, multidimensional reality into a simple framework to facilitate decision-making for yellow fever control. As more assessments and data are available, attempts will be made to establish criteria to compare the level of risk for YFV transmission in the areas studied.7 This modelling approach

should be expanded to other endemic areas in Africa and inte-grated into control efforts of other vector-borne diseases in order to concentrate available resources in an effective and effi-cient manner.1,2In fact, there are few well-designed

epidemio-logical studies and limited data about yellow fever in Africa to define epidemiological scenarios and the operational impact of preventive measures.2,3This multidisciplinary risk assessment provides information about ecological areas at risk in zones where YFV is circulating. As a result, criteria may now be estab-lished to compare the level of risk for YFV transmission in the areas studied.7

By targeting yellow fever elimination as a public health prob-lem, Staples et al. reinforce the need of intensifying applied and operational research in local contexts to address problems and human capacity needs in the realm of neglected tropical diseases

in the post-2015 agenda.11Continuing epidemiological monitor-ing and advocacy for the priority of control or elimination of neglected tropical diseases should be placed in the context of uni-versal health coverage and access to free essential medicines for the poor as a human right.11

Authors’ contributions:ANRJ conceived the paper. ANRJ and JH wrote, read and approved the final manuscript. ANRJ and JH are guarantors of the paper.

Funding:None.

Competing interests:None declared.

Ethical approval:Not required.

References

1 World Health Organization. Yellow fever in Africa and South America, 2013. Wkly Epidemiol Rec 2014;89:297–306.

2 World Health Organization. Vaccines and vaccination against yellow fever WHO Position Paper – June 2013, 2013. Wkly Epidemiol Rec 2013;88:269–84.

3 Garske T, Van Kerkhove MD, Yactayo S et al. Yellow Fever Expert Committee. Yellow Fever in Africa: estimating the burden of disease and impact of mass vaccination from outbreak and serological data. PLoS Med 2014;11(5):e1001638.

4 Johansson MA, Vasconcelos PF, Staples JE. The whole iceberg: estimating the incidence of yellow fever virus infection from the number of severe cases. Trans R Soc Trop Med Hyg. 2014;108:482–7. 5 Romano AP, Costa ZG, Ramos DG et al. Yellow Fever outbreaks in

unvaccinated populations, Brazil, 2008–2009. PLoS Negl Trop Dis 2014;8(3):e2740.

6 Caˆmara FP, Carvalho LM, Gomes AL. Demographic profile of sylvatic yellow fever in Brazil from 1973 to 2008. Trans R Soc Trop Med Hyg 2013;107:324–7.

7 World Health Organization. Risk assessment on yellow fever virus circulation in endemic countries - Working document from an informal consultation of experts. A Protocol for risk assessment at the field level. WHO/HSE/PED/CED/2014.2, 2014. 52p.

8 Staples JE, Diallo M, Janusz KB et al. Yellow fever risk assessment in the Central African Republic. Trans R Soc Trop Med Hyg 2014;108:608–15. 9 Almeida MA, Cardoso JC, Santos E et al. Surveillance for yellow fever virus in non-human primates in southern Brazil, 2001–2011: a tool for prioritizing human populations for vaccination. PLoS Negl Trop Dis 2014;8:e2741.

10 Ngoagouni C, Kamgang B, Manirakiza A et al. Entomological profile of yellow fever epidemics in the Central African Republic, 2006–2010. Parasit Vectors 2012;5:175.

11 Molyneux DH. Neglected tropical diseases: now more than just ’other diseases’ -the post-2015 agenda. Int Health 2014;6:172–80.

A. N. Ramos and J. Heukelbach

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http://trstmh.oxfordjournals.org/

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