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How to explain the re-emergence of chikungunya infection in Reunion Island in 2010?
Acta Tropica 123 (2012) 85–90
Contents lists available at SciVerse ScienceDirect
Acta Tropica journal homepage: www.elsevier.com/locate/actatropica
How to explain the re-emergence of chikungunya infection in Reunion Island in 2010?夽 P. Vilain a,∗ , S. Larrieu a , P. Renault a , M. Baville b , L. Filleul a a b
Regional Office of French Institute for Public Health Surveillance of Indian Ocean, 2 bis avenue Georges Brassens, CS 60050, 97408 Saint Denis Cedex 9, Reunion Vector Control Team, Health Agency of Indian Ocean, 2 bis avenue Georges Brassens, CS 60050, 97408 Saint Denis Cedex 9, Reunion
a r t i c l e
i n f o
Article history: Received 3 August 2011 Received in revised form 12 March 2012 Accepted 24 March 2012 Available online 13 April 2012 Keywords: Chikungunya Re-emergence Reunion Island
a b s t r a c t In March 2010, a new outbreak of chikungunya infection was detected in the west of Reunion Island. An investigation was launched to describe the incident cases occurrence and to raise hypotheses on factors that could explain the occurrence of this outbreak. All probable or confirmed cases detected by the surveillance system in the western area between March 1st and July 2nd, 2010 were included in the investigation. A standardized questionnaire was performed by phone, including sociodemographic, environmental and behaviour data. A total of 74 cases were described (i.e. response rate of 72%). They were mainly women (sex ratio M/F = 0.7), all ages were represented. Most of them (76%) resided in a house; 31% had recently moved, including 22% from metropolitan France. They reported to have been more exposed to mosquitoes and to infected patients than during the major epidemic of 2005–2006. In addition, 41% reported to have reduced their protection against mosquitoes. The results suggest that several concomitant factors contributed to this outbreak: the reintroduction of the chikungunya virus in the island, the population characteristics and environmental factors. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Chikungunya virus (CHIKV) is an alphavirus belonging to the Togaviridae family (Porterfield, 1980). It is transmitted to human beings by mosquitoes of the Aedes genus (Powers and Logue, 2007). It was first isolated in 1952 during an outbreak that occurred in the Southern Province of Tanganyika (Ross, 1956). The clinical course is characterized by a sudden onset of fever often accompanied by arthralgia, myalgia, headache and rash (Borgherini et al., 2007; Queyriaux et al., 2008). Although the evolution is favourable in most cases, persistent arthralgia, which can be incapacitating, is frequently observed (Borgherini et al., 2008; Sissoko et al., 2009). Currently, there is neither etiological treatment nor vaccine and the treatment is only symptomatic. During 2004–2007, CHIKV has been responsible for several outbreaks in the southwestern Indian Ocean region. The first epidemic occurred in East Africa (Sergon et al., 2008); then it
夽 Meeting(s) where the information has previously been presented: European Scientific Conference on Applied Infectious Disease Epidemiology (ESCAIDE), Lisbon, Portugal, 11–13 November 2010. ∗ Corresponding author. Tel.: +262 02 62 93 94 24; fax: +262 02 62 93 94 57. E-mail addresses: [email protected] (P. Vilain), [email protected] (S. Larrieu), [email protected] (P. Renault), [email protected] (M. Baville), [email protected] (L. Filleul). 0001-706X/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.actatropica.2012.03.009
progressively spread to the islands of the Indian Ocean: Comoros (Sergon et al., 2007), Mayotte (Sissoko et al., 2008), Madagascar (Ratsitorahina et al., 2008), Reunion Island (Renault et al., 2007), Mauritius (Beesoon et al., 2008) and Seychelles. On Reunion Island, the major outbreak of CHIKV infection began in March 2005 and ended in December 2006. During this epidemic, 266,000 people were infected, corresponding to an attack rate of 36% over the entire population (Renault et al., 2007). A seroprevalence study conducted at the end of the outbreak confirmed this result by showing that 38% of the population had antibodies for CHIKV (Gerardin et al., 2008b). Following this epidemic, an entomological and epidemiological surveillance has been established (Balleydier et al., 2008); since 2006, no virus circulation has been detected, except in August 2009 when a cluster of five chikungunya fever (CHIKF) cases occurred on the west coast of the island (D’Ortenzio et al., 2009). In March 2010, the surveillance system identified several cases clinically compatible with a recent infection of CHIKV in the neighbourhood of Plateau Caillou located in the municipality of Saint-Paul (west of the island). These cases were confirmed by RTPCR and after investigation, it appeared that these patients had no recent travel history. They were defined as autochthonous cases (D’Ortenzio et al., 2011). The occurrence of this outbreak raised several questions: why did this new outbreak occur five years after the major epidemic? What were the characteristics of infected people
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P. Vilain et al. / Acta Tropica 123 (2012) 85–90
Fig. 1. Surveillance system of chikungunya infection, Reunion Island, 2010.
in terms of exposition? What other factors could explain this outbreak? The Regional Office of French Institute for Public Health Surveillance of Indian Ocean (Cire-OI) immediately conducted an investigation to describe the incident cases of CHIKF on the west coast of Reunion Island during the 2010 outbreak and raise hypotheses on factors that could explain the occurrence of this outbreak. The goals were to better understand the event in order to respond to health authorities that needed to adjust their control measures. 2. Materials and methods Reunion Island is a French overseas district located in the southwest Indian Ocean, east of Madagascar. Its population in 2010 was estimated at 802,000 inhabitants. There are two distinct seasons: a cool and dry winter from May to October, and a warmer, rainy summer from November to April. The habitat is usually composed of houses with gardens, with very few high buildings. 2.1. Organization of the surveillance system Since 2006, the Cire-OI has organized a surveillance network of CHIKV infection in Reunion Island (Fig. 1). This surveillance is based on the laboratories of medical and biological analysis (LABM) which report to the Cire-OI all limit or positive IgM chikungunya serologies, positive RT-PCR and CHIKV isolation. After a first evaluation with the physician who prescribed the biological test, the reporting is sent to the vector control team (LAV) for investigation. The vector control team carries out an entomological prospecting around the habitat of the case and searches in the neighbourhood for people with the same symptoms in order to identify a possible cluster. If the investigation leads to the detection of new cases, all physicians of the area are encouraged to prescribe a laboratory confirmation to any patient presenting “dengue-like” syndrome. The results are then sent to the Cire-OI that classifies cases according to several definitions. The definitions used for
surveillance were validated by a group of experts including clinicians, biologists, epidemiologists, entomologists, sociologists and veterinarians who compose the committee of infectious and emerging disease of Reunion Island (Balleydier et al., 2008): – a “dengue-like syndrome” is defined by a sudden onset of fever >38◦ 5 C accompanied by one or several non-specific symptoms: muscle and joint pain, hemorrhagic manifestations, frontal headaches, asthenia, digestive symptoms, retro-orbital pain, maculopapular rash, and in the absence of any other infection; – a confirmed case is defined by the presence of the following serological or virological criteria: detection of the viral genome by RT-PCR, seroconversion, or increase by four of Immunoglobulin G (IgG) between two serums drawn at a two weeks minimum interval; – a probable case is defined as a person with a dengue-like syndrome and positive or limit chikungunya immunoglobulin M (IgM); – an autochthonous case is defined as a person who did not travel in any endemic or epidemic area seven days before the onset of symptoms. 2.2. Case definition The case definition used for the study was the following: any probable or confirmed autochthonous case detected between March 1st and July 2nd 2010 in the western area and born before July 2006. 2.3. Data collection All the cases identified by the surveillance system and meeting the case definition were interviewed by telephone. A standardized questionnaire was used to collect data aiming at describing two factors that could have influenced the occurrence of this outbreak: characteristics of the population (sex, age, housing and use of prophylactic measures), and environment of the patients
P. Vilain et al. / Acta Tropica 123 (2012) 85–90
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Fig. 2. Epidemic curve of confirmed and probable chikungunya cases, Reunion Island, 2010.
(self-assessment of exposure to mosquitoes, self-assessment of contact with people infected by CHIKV). For each item, patients were interviewed about two periods (2005–2006 and 2010) in order to highlight changes in their characteristics and/or habits that could explain why they were infected in 2010 whereas they were not in 2005–2006. 2.4. Ethical clearance Prior to the study, the French Institute for Public Health Surveillance (InVS) received a permanent agreement by the Commission nationale de l’informatique et des libertés (CNIL) allowing it to collect personal data during the occurrence of an epidemic in order to implement control measures. The CNIL authorized the InVS to collect personal data in the case of urgent investigations that have to be conducted without delay and that represent a public health issue. The goal is to highlight the source and vehicle of epidemics in order to control and prevent them. As this study was performed during the outbreak in order to target people for preventive measures, it was covered by this permanent agreement. 3. Results Between March and November 2010, the surveillance system identified 158 chikungunya cases among which 112 were confirmed cases and 46 were probable cases. The outbreak started in the neighbourhood of Plateau Caillou, then expanded to the city of Saint-Paul. Other isolated cases occurred in several towns of the island (Figs. 2 and 3). Out of the 103 cases meeting case definition, 74 agreed to participate to the study (i.e. a response rate of 72%). 3.1. Population characteristics The sex-ratio M/F was 0.7. This predominance of female cases mostly concerned the age groups of 20–39 years (33% vs 19%) and 60 years and over (14% vs 7%). The male cases were mainly concentrated in the age group of 19 years or less (39% vs 16%). The median age was 38.5 years (min: 6; max: 79).
Three quarters of the cases lived in houses and one quarter in apartments. Among those living in apartments, 67% were in the ground-floor. Thirty-one percent of cases reported they had moved to a new place after the major epidemic of 2005–2006. Among them, 22% were new migrants to the island coming from metropolitan France (Table 1).
3.2. Proximity to people infected by chikungunya virus and exposure to mosquitoes Most cases said they had seen “few or no” people who had CHIKF in 2006 (at home: 87%; in their neighbourhood: 66%; in their workplace or school: 87%). Among them, half (47%) were more exposed in 2010 since they reported contacts with cases, mainly in the neighbourhood (58%) but also at home (32%), in the other places (friends, family: 23%) or at work (3%). Likewise, most of the subjects reported “few or no” mosquitoes in their workplace (74%) and at home (69%) during the major
Table 1 Socio-demographical characteristics of chikungunya cases, Reunion Island, 2010. Population characteristic
n
%
Sex Male Female
31 43
41.9 58.1
Age group 19 years and less 20–39 years 40–59 years 60 years and over
19 20 27 8
25.7 27.0 36.5 10.8
Type of housing in 2010 Individual house Apartment Ground Floor Other floors
56 18 12 6
75.7 24.3 66.7 33.3
Move after 2006 No Yes New migrant No new migrant
51 23 5 18
68.9 31.1 21.7 78.2
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Fig. 3. Geographical distribution of confirmed and probable chikungunya cases, Reunion Island, 2010.
epidemic; and half of them (49%) noticed an increase in the number of mosquitoes in their environment in 2010. Between March and June 2010, entomological prospecting around the habitat of the cases by control vector team indicated a Breteau index (i.e. the number of positive Aedes albopictus containers per 100 houses inspected) of 49.3 and a house index (i.e. the percentage of houses infested with Ae. albopictus larvae or pupae) of 19.6%.
To understand the dynamic of the chikungunya virus infection re-emergence, it was important to study this episode in its entirety, i.e. to consider simultaneously the infectious agent, the environment, the host and the interaction between three fundamentals elements (Desenclos, 2007). From the results of this investigation and bibliographical analysis, we will try to explain the three factors above.
3.3. Prophylactic measures Fifty-four cases (78%) reported they had used individual protections against mosquito bites (long clothing, repellents, electric diffusers, screens, etc.) or implemented preventive measures against breeding places during the epidemic of 2005–2006. Among them, 41% reported to have decreased their protections in 2010: half of them considered they had a low risk of CHIKV infection after the 2005–2006 epidemic; the other reasons were “few or no” mosquitoes in the environment (n = 4), currently low-risk people (no pregnant, no immunocompromised, etc.) (n = 3), and allergy to repellents (n = 4). During the entomological investigations around chikungunya cases by the control vector team, a survey of breeding places was conducted in private gardens: 37% of positive breeding sites were flower pot saucer, 34% small containers (less than 10 l capacity), 7% tires, and 4% were vases. Only 11% of positive breeding sites were natural. 4. Discussion Five years after the major epidemic of CHIKV infection that affected Reunion Island in 2005–2006, a new cluster was detected in the west of the island.
4.1. Virus introduction During this outbreak, phylogenetic analysis based on the sequence comparison of partial envelope gene or complete genome showed that nucleotide and amino acid sequences of the 2010 CHIKV isolate from Reunion Island were similar at 99.6% to the 2009 sporadic cases on Reunion Island, as well as to the Malagasy strains circulating since 2006 (D’Ortenzio et al., 2011). All isolated sequences bore the A226V substitution within the E1 protein. Altogether, these results have been supporting the hypothesis of a continuous circulation of A226V strains in the southwestern Indian Ocean since 2006 and the possible reintroduction of CHIKV on Reunion Island, most probably from Madagascar. Indeed, in February 2010, an outbreak of CHIKV occurred at the East of Madagascar just before the detection of the first cases in Reunion Island (International Society for Infectious Diseases, 2010). Human travels are likely responsible for the rapid spread of the virus between islands (Morse, 1995) since imported and autochthonous cases on Reunion Island occurred after a holiday period for residents of Reunion Island who often travelled to Madagascar. The probability of an unnoticeable virus circulation on the island cannot be excluded but seems to be unlikely.
P. Vilain et al. / Acta Tropica 123 (2012) 85–90
4.2. Population characteristics Trends in terms of age group and sex are similar to those observed during the epidemic of 2005–2006, with a predominance of females over 20 years old that could be due to greater home and gardening activities or differences in clothing leading to a greater exposure of the skin (Gerardin et al., 2008a). Among the people infected in this outbreak, 31% reported they had moved to a new place after the epidemic of 2005–2006. The fact that most of these cases reported “few or no” chikungunya patients in their environment during the 2005–2006 epidemic suggests that they lived in neighbourhoods where the attack rate was low. Indeed, the seroprevalence survey in 2007 did not allow to estimate the prevalence rate by municipality (Gerardin et al., 2008b). The occurrence of this outbreak suggests that the immunity had heterogeneous distribution on this island and that the immunity population in the Saint Paul area was lower. Among them, 22% had never been previously exposed to chikungunya since they had recently moved on to the island. The introduction of immunologically naive population has contributed to create propitious conditions to the development of the cluster. In addition, changes in individual behaviours might have increased population exposure. In fact, among cases having reported the use of protective measures against mosquito bites or put into place preventive measures against mosquito breeding sites during the epidemic 2005–2006, nearly half reported having reduced these protections in 2010. The entomological prospecting showed that the great majority of breeding sites could have been easy to remove by the population (Dehecq et al., 2011). 4.3. Environmental factors Last, environmental factors might have played a role in the occurrence of the outbreak. In our study, three quarters of the cases lived in individual houses and 67% of those who lived in apartments resided at the ground floors, which are well-known factors of infection linked to arboviruses (Gerardin et al., 2008a). In Reunion Island, the vector of chikungunya is Ae. albopictus (Delatte et al., 2008b). The distribution area of Ae. albopictus on the island shows that it is mainly spread over the urban areas, that is to say essentially on the coastline. The typology of breeding places reveals the capacity of Ae. albopictus to colonize several types of water points whether they are natural or anthropogenic. In urban environments, mosquito larvae live mostly in flower pot saucer and small containers, and in peri-urban and rural areas, in bamboo holes and rocks (Delatte et al., 2008a). This omnipresence in urban areas increases the contact with human beings and therefore the risk of CHIKV transmission by this anthropophilic and exophagic vector (Delatte et al., 2010). Vector density has also probably played an important role in extending this cluster since half of the cases have noticed a significant presence of the vector in their environment. In fact, during this outbreak, the house index and Breteau index collected around chikungunya cases were much higher than the level of epidemic risk defined by WHO (for dengue virus and Ae. aegypti) (Dehecq et al., 2011). During the major epidemic 2005–2006, an entomological survey in nine urban areas showed a Breteau index of 68.4 and a house index of 19.2% (Delatte et al., 2008a). These results are similar to those observed in 2010. The main limit of this investigation is that the results are descriptive and based on the patients reports. However, the occurrence of this outbreak caused a crisis situation, in which public health authorities needed to know immediately the characteristics of the CHIKF cases in order to understand its occurrence. Complementary research is to be done; in particular, the seroprevalence rate
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by municipality would be of interest, and sociological studies are important to better understand people’s behaviour. This study sheds a new light on the factors that could explain the re-emergence of CHIKV in Reunion Island five years after the world’s greatest epidemic. The factors that can play a role during the different steps of a re-emerging disease process are numerous and deeply linked and mixed to each other; it is therefore important to have a multifactorial approach. 5. Conclusion The persistent circulation of arboviruses such as CHIKV together with the presence of the vector throughout the year involves a permanent epidemic threat to Reunion Island. Movements of non-immune population and behavioural changes constitute vulnerable cluster to CHIKV infection. These results may contribute to target the population for which a reiterating sensitization campaign is needed. Acknowledgements Agents of Vector Control Team, laboratories and physicians of Reunion Island and the Reference National Center of arbovirus, Sandra Giron, Jean-Sébastien Dehecq, Thomas Margueron, Marianne Mérolle. References Balleydier, E., D’Ortenzio, E., Renault, P., 2008. Épidémiologie du chikungunya à la Réunion. Bilan d’une année de surveillance, 19 avril 2007–18 avril 2008. Institut de Veille Sanitaire, Saint-Maurice. Beesoon, S., Funkhouser, E., Kotea, N., Spielman, A., Robich, R.M., 2008. Chikungunya fever, Mauritius, 2006. Emerging Infectious Diseases 14, 337–338. Borgherini, G., Poubeau, P., Jossaume, A., Gouix, A., Cotte, L., Michault, A., ArvinBerod, C., Paganin, F., 2008. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion Island. Clinical Infectious Diseases 47, 469–475. Borgherini, G., Poubeau, P., Staikowsky, F., Lory, M., Le Moullec, N., Becquart, J.P., Wengling, C., Michault, A., Paganin, F., 2007. Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients. Clinical Infectious Diseases 44, 1401–1407. D’Ortenzio, E., Grandadam, M., Balleydier, E., Dehecq, J.S., Jaffar-Bandjee, M.C., Michault, A., Andriamandimby, S.F., Reynes, J.M., Filleul, L., 2009. Sporadic cases of chikungunya, Reunion Island, August 2009. Euro Surveillance 14, 19324. D’Ortenzio, E., Grandadam, M., Balleydier, E., Jaffar-Bandjee, M.C., Michault, A., Brottet, E., Baville, M., Filleul, L., 2011. A226V strains of chikungunya virus, Reunion Island, 2010. Emerging Infectious Diseases 17, 309–311. Dehecq, J.S., Baville, M., Margueron, T., Mussard, R., Filleul, L., 2011. The reemergence of the chikungunya virus in Reunion Island on 2010: evolution of the mosquito control practices. Bulletin de la Societe de Pathologie Exotique 104, 153–160. Delatte, H., Dehecq, J.S., Thiria, J., Domerg, C., Paupy, C., Fontenille, D., 2008a. Geographic distribution and developmental sites of Aedes albopictus (Diptera: Culicidae) during a chikungunya epidemic event. Vector Borne Zoonotic Diseases 8, 25–34. Delatte, H., Desvars, A., Bouetard, A., Bord, S., Gimonneau, G., Vourc’h, G., Fontenille, D., 2010. Blood-feeding behavior of Aedes albopictus, a vector of chikungunya on La Reunion. Vector Borne Zoonotic Diseases 10, 249–258. Delatte, H., Paupy, C., Dehecq, J.S., Thiria, J., Failloux, A.B., Fontenille, D., 2008b. Aedes albopictus, vector of chikungunya and dengue viruses in Reunion Island: biology and control. Parasite 15, 3–13. Desenclos, J., 2007. Maladies infectieuses émergentes. In: Bourdillon, F., Brücker, G., Tabuteau, D. (Eds.), Traité de santé publique. , 2nd ed. Médecine – Sciences Flammarion, Paris, pp. 437–442. Gerardin, P., Guernier, V., Perrau, J., Fianu, A., Le Roux, K., Grivard, P., Michault, A., de Lamballerie, X., Flahault, A., Favier, F., 2008a. Determinants of chikungunya virus infection in the Reunion Island: Results of the SEROCHIK seroprevalence survey in the population, August–October 2006. Bulletin Epidémiologique Hebdomadaire 38-39, 361–366. Gerardin, P., Guernier, V., Perrau, J., Fianu, A., Le Roux, K., Grivard, P., Michault, A., de Xavier, L., Flahault, A., Francois, F., 2008b. Estimating chikungunya prevalence in La Reunion Island outbreak by serosurveys: two methods for two critical times of the epidemic. BMC Infectious Diseases 8, 99. International Society for Infectious Diseases Chikungunya: Madagascar (Fianarantsoa), Myanmar Institut Pasteur from Madagascar: Madagascar, 286-2011. Available from http://www.promedmail.org/pls/apex/f?p=2400:1202: 4493792339191053::NO::F2400 P1202 CHECK DISPLAY.
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Morse, S.S., 1995. Factors in the emergence of infectious diseases. Emerging Infectious Diseases 1, 7–15. Porterfield, J., 1980. Antigenic characteristics and classification of the Togaviridae. In: Schlesinger, R. (Ed.), The Togaviruses. Academic Press, New York, pp. 13–46. Powers, A.M., Logue, C.H., 2007. Changing patterns of chikungunya virus: reemergence of a zoonotic arbovirus. Journal of General Virology 88, 2363–2377. Queyriaux, B., Simon, F., Grandadam, M., Michel, R., Tolou, H., Boutin, J.P., 2008. Clinical burden of chikungunya virus infection. Lancet Infectious Diseases 8, 2–3. Ratsitorahina, M., Harisoa, J., Ratovonjato, J., Biacabe, S., Reynes, J.M., Zeller, H., Raoelina, Y., Talarmin, A., Richard, V., Louis, S.J., 2008. Outbreak of dengue and chikungunya fevers, Toamasina, Madagascar, 2006. Emerging Infectious Diseases 14, 1135–1137. Renault, P., Solet, J.L., Sissoko, D., Balleydier, E., Larrieu, S., Filleul, L., Lassalle, C., Thiria, J., Rachou, E., de Valk, H., Ilef, D., Ledrans, M., Quatresous, I., Quenel, P., Pierre, V., 2007. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. American Journal of Tropical Medicine and Hygiene 77, 727–731. Ross, R.W., 1956. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. Journal of Hygiene 54, 177–191.
Sergon, K., Njuguna, C., Kalani, R., Ofula, V., Onyango, C., Konongoi, L.S., Bedno, S., Burke, H., Dumilla, A.M., Konde, J., Njenga, M.K., Sang, R., Breiman, R.F., 2008. Seroprevalence of chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. American Journal of Tropical Medicine and Hygiene 78, 333–337. Sergon, K., Yahaya, A.A., Brown, J., Bedja, S.A., Mlindasse, M., Agata, N., Allaranger, Y., Ball, M.D., Powers, A.M., Ofula, V., Onyango, C., Konongoi, L.S., Sang, R., Njenga, M.K., Breiman, R.F., 2007. Seroprevalence of chikungunya virus infection on Grande Comore Island, union of the Comoros 2005. American Journal of Tropical Medicine and Hygiene 76, 1189–1193. Sissoko, D., Malvy, D., Ezzedine, K., Renault, P., Moscetti, F., Ledrans, M., Pierre, V., 2009. Post-epidemic chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Neglected Tropical Diseases 3, e389. Sissoko, D., Moendandze, A., Malvy, D., Giry, C., Ezzedine, K., Solet, J.L., Pierre, V., 2008. Seroprevalence and risk factors of chikungunya virus infection in Mayotte, Indian Ocean, 2005–2006: a population-based survey. PLoS One 3, e3066.
Contents lists available at SciVerse ScienceDirect
Acta Tropica journal homepage: www.elsevier.com/locate/actatropica
How to explain the re-emergence of chikungunya infection in Reunion Island in 2010?夽 P. Vilain a,∗ , S. Larrieu a , P. Renault a , M. Baville b , L. Filleul a a b
Regional Office of French Institute for Public Health Surveillance of Indian Ocean, 2 bis avenue Georges Brassens, CS 60050, 97408 Saint Denis Cedex 9, Reunion Vector Control Team, Health Agency of Indian Ocean, 2 bis avenue Georges Brassens, CS 60050, 97408 Saint Denis Cedex 9, Reunion
a r t i c l e
i n f o
Article history: Received 3 August 2011 Received in revised form 12 March 2012 Accepted 24 March 2012 Available online 13 April 2012 Keywords: Chikungunya Re-emergence Reunion Island
a b s t r a c t In March 2010, a new outbreak of chikungunya infection was detected in the west of Reunion Island. An investigation was launched to describe the incident cases occurrence and to raise hypotheses on factors that could explain the occurrence of this outbreak. All probable or confirmed cases detected by the surveillance system in the western area between March 1st and July 2nd, 2010 were included in the investigation. A standardized questionnaire was performed by phone, including sociodemographic, environmental and behaviour data. A total of 74 cases were described (i.e. response rate of 72%). They were mainly women (sex ratio M/F = 0.7), all ages were represented. Most of them (76%) resided in a house; 31% had recently moved, including 22% from metropolitan France. They reported to have been more exposed to mosquitoes and to infected patients than during the major epidemic of 2005–2006. In addition, 41% reported to have reduced their protection against mosquitoes. The results suggest that several concomitant factors contributed to this outbreak: the reintroduction of the chikungunya virus in the island, the population characteristics and environmental factors. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Chikungunya virus (CHIKV) is an alphavirus belonging to the Togaviridae family (Porterfield, 1980). It is transmitted to human beings by mosquitoes of the Aedes genus (Powers and Logue, 2007). It was first isolated in 1952 during an outbreak that occurred in the Southern Province of Tanganyika (Ross, 1956). The clinical course is characterized by a sudden onset of fever often accompanied by arthralgia, myalgia, headache and rash (Borgherini et al., 2007; Queyriaux et al., 2008). Although the evolution is favourable in most cases, persistent arthralgia, which can be incapacitating, is frequently observed (Borgherini et al., 2008; Sissoko et al., 2009). Currently, there is neither etiological treatment nor vaccine and the treatment is only symptomatic. During 2004–2007, CHIKV has been responsible for several outbreaks in the southwestern Indian Ocean region. The first epidemic occurred in East Africa (Sergon et al., 2008); then it
夽 Meeting(s) where the information has previously been presented: European Scientific Conference on Applied Infectious Disease Epidemiology (ESCAIDE), Lisbon, Portugal, 11–13 November 2010. ∗ Corresponding author. Tel.: +262 02 62 93 94 24; fax: +262 02 62 93 94 57. E-mail addresses: [email protected] (P. Vilain), [email protected] (S. Larrieu), [email protected] (P. Renault), [email protected] (M. Baville), [email protected] (L. Filleul). 0001-706X/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.actatropica.2012.03.009
progressively spread to the islands of the Indian Ocean: Comoros (Sergon et al., 2007), Mayotte (Sissoko et al., 2008), Madagascar (Ratsitorahina et al., 2008), Reunion Island (Renault et al., 2007), Mauritius (Beesoon et al., 2008) and Seychelles. On Reunion Island, the major outbreak of CHIKV infection began in March 2005 and ended in December 2006. During this epidemic, 266,000 people were infected, corresponding to an attack rate of 36% over the entire population (Renault et al., 2007). A seroprevalence study conducted at the end of the outbreak confirmed this result by showing that 38% of the population had antibodies for CHIKV (Gerardin et al., 2008b). Following this epidemic, an entomological and epidemiological surveillance has been established (Balleydier et al., 2008); since 2006, no virus circulation has been detected, except in August 2009 when a cluster of five chikungunya fever (CHIKF) cases occurred on the west coast of the island (D’Ortenzio et al., 2009). In March 2010, the surveillance system identified several cases clinically compatible with a recent infection of CHIKV in the neighbourhood of Plateau Caillou located in the municipality of Saint-Paul (west of the island). These cases were confirmed by RTPCR and after investigation, it appeared that these patients had no recent travel history. They were defined as autochthonous cases (D’Ortenzio et al., 2011). The occurrence of this outbreak raised several questions: why did this new outbreak occur five years after the major epidemic? What were the characteristics of infected people
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Fig. 1. Surveillance system of chikungunya infection, Reunion Island, 2010.
in terms of exposition? What other factors could explain this outbreak? The Regional Office of French Institute for Public Health Surveillance of Indian Ocean (Cire-OI) immediately conducted an investigation to describe the incident cases of CHIKF on the west coast of Reunion Island during the 2010 outbreak and raise hypotheses on factors that could explain the occurrence of this outbreak. The goals were to better understand the event in order to respond to health authorities that needed to adjust their control measures. 2. Materials and methods Reunion Island is a French overseas district located in the southwest Indian Ocean, east of Madagascar. Its population in 2010 was estimated at 802,000 inhabitants. There are two distinct seasons: a cool and dry winter from May to October, and a warmer, rainy summer from November to April. The habitat is usually composed of houses with gardens, with very few high buildings. 2.1. Organization of the surveillance system Since 2006, the Cire-OI has organized a surveillance network of CHIKV infection in Reunion Island (Fig. 1). This surveillance is based on the laboratories of medical and biological analysis (LABM) which report to the Cire-OI all limit or positive IgM chikungunya serologies, positive RT-PCR and CHIKV isolation. After a first evaluation with the physician who prescribed the biological test, the reporting is sent to the vector control team (LAV) for investigation. The vector control team carries out an entomological prospecting around the habitat of the case and searches in the neighbourhood for people with the same symptoms in order to identify a possible cluster. If the investigation leads to the detection of new cases, all physicians of the area are encouraged to prescribe a laboratory confirmation to any patient presenting “dengue-like” syndrome. The results are then sent to the Cire-OI that classifies cases according to several definitions. The definitions used for
surveillance were validated by a group of experts including clinicians, biologists, epidemiologists, entomologists, sociologists and veterinarians who compose the committee of infectious and emerging disease of Reunion Island (Balleydier et al., 2008): – a “dengue-like syndrome” is defined by a sudden onset of fever >38◦ 5 C accompanied by one or several non-specific symptoms: muscle and joint pain, hemorrhagic manifestations, frontal headaches, asthenia, digestive symptoms, retro-orbital pain, maculopapular rash, and in the absence of any other infection; – a confirmed case is defined by the presence of the following serological or virological criteria: detection of the viral genome by RT-PCR, seroconversion, or increase by four of Immunoglobulin G (IgG) between two serums drawn at a two weeks minimum interval; – a probable case is defined as a person with a dengue-like syndrome and positive or limit chikungunya immunoglobulin M (IgM); – an autochthonous case is defined as a person who did not travel in any endemic or epidemic area seven days before the onset of symptoms. 2.2. Case definition The case definition used for the study was the following: any probable or confirmed autochthonous case detected between March 1st and July 2nd 2010 in the western area and born before July 2006. 2.3. Data collection All the cases identified by the surveillance system and meeting the case definition were interviewed by telephone. A standardized questionnaire was used to collect data aiming at describing two factors that could have influenced the occurrence of this outbreak: characteristics of the population (sex, age, housing and use of prophylactic measures), and environment of the patients
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Fig. 2. Epidemic curve of confirmed and probable chikungunya cases, Reunion Island, 2010.
(self-assessment of exposure to mosquitoes, self-assessment of contact with people infected by CHIKV). For each item, patients were interviewed about two periods (2005–2006 and 2010) in order to highlight changes in their characteristics and/or habits that could explain why they were infected in 2010 whereas they were not in 2005–2006. 2.4. Ethical clearance Prior to the study, the French Institute for Public Health Surveillance (InVS) received a permanent agreement by the Commission nationale de l’informatique et des libertés (CNIL) allowing it to collect personal data during the occurrence of an epidemic in order to implement control measures. The CNIL authorized the InVS to collect personal data in the case of urgent investigations that have to be conducted without delay and that represent a public health issue. The goal is to highlight the source and vehicle of epidemics in order to control and prevent them. As this study was performed during the outbreak in order to target people for preventive measures, it was covered by this permanent agreement. 3. Results Between March and November 2010, the surveillance system identified 158 chikungunya cases among which 112 were confirmed cases and 46 were probable cases. The outbreak started in the neighbourhood of Plateau Caillou, then expanded to the city of Saint-Paul. Other isolated cases occurred in several towns of the island (Figs. 2 and 3). Out of the 103 cases meeting case definition, 74 agreed to participate to the study (i.e. a response rate of 72%). 3.1. Population characteristics The sex-ratio M/F was 0.7. This predominance of female cases mostly concerned the age groups of 20–39 years (33% vs 19%) and 60 years and over (14% vs 7%). The male cases were mainly concentrated in the age group of 19 years or less (39% vs 16%). The median age was 38.5 years (min: 6; max: 79).
Three quarters of the cases lived in houses and one quarter in apartments. Among those living in apartments, 67% were in the ground-floor. Thirty-one percent of cases reported they had moved to a new place after the major epidemic of 2005–2006. Among them, 22% were new migrants to the island coming from metropolitan France (Table 1).
3.2. Proximity to people infected by chikungunya virus and exposure to mosquitoes Most cases said they had seen “few or no” people who had CHIKF in 2006 (at home: 87%; in their neighbourhood: 66%; in their workplace or school: 87%). Among them, half (47%) were more exposed in 2010 since they reported contacts with cases, mainly in the neighbourhood (58%) but also at home (32%), in the other places (friends, family: 23%) or at work (3%). Likewise, most of the subjects reported “few or no” mosquitoes in their workplace (74%) and at home (69%) during the major
Table 1 Socio-demographical characteristics of chikungunya cases, Reunion Island, 2010. Population characteristic
n
%
Sex Male Female
31 43
41.9 58.1
Age group 19 years and less 20–39 years 40–59 years 60 years and over
19 20 27 8
25.7 27.0 36.5 10.8
Type of housing in 2010 Individual house Apartment Ground Floor Other floors
56 18 12 6
75.7 24.3 66.7 33.3
Move after 2006 No Yes New migrant No new migrant
51 23 5 18
68.9 31.1 21.7 78.2
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Fig. 3. Geographical distribution of confirmed and probable chikungunya cases, Reunion Island, 2010.
epidemic; and half of them (49%) noticed an increase in the number of mosquitoes in their environment in 2010. Between March and June 2010, entomological prospecting around the habitat of the cases by control vector team indicated a Breteau index (i.e. the number of positive Aedes albopictus containers per 100 houses inspected) of 49.3 and a house index (i.e. the percentage of houses infested with Ae. albopictus larvae or pupae) of 19.6%.
To understand the dynamic of the chikungunya virus infection re-emergence, it was important to study this episode in its entirety, i.e. to consider simultaneously the infectious agent, the environment, the host and the interaction between three fundamentals elements (Desenclos, 2007). From the results of this investigation and bibliographical analysis, we will try to explain the three factors above.
3.3. Prophylactic measures Fifty-four cases (78%) reported they had used individual protections against mosquito bites (long clothing, repellents, electric diffusers, screens, etc.) or implemented preventive measures against breeding places during the epidemic of 2005–2006. Among them, 41% reported to have decreased their protections in 2010: half of them considered they had a low risk of CHIKV infection after the 2005–2006 epidemic; the other reasons were “few or no” mosquitoes in the environment (n = 4), currently low-risk people (no pregnant, no immunocompromised, etc.) (n = 3), and allergy to repellents (n = 4). During the entomological investigations around chikungunya cases by the control vector team, a survey of breeding places was conducted in private gardens: 37% of positive breeding sites were flower pot saucer, 34% small containers (less than 10 l capacity), 7% tires, and 4% were vases. Only 11% of positive breeding sites were natural. 4. Discussion Five years after the major epidemic of CHIKV infection that affected Reunion Island in 2005–2006, a new cluster was detected in the west of the island.
4.1. Virus introduction During this outbreak, phylogenetic analysis based on the sequence comparison of partial envelope gene or complete genome showed that nucleotide and amino acid sequences of the 2010 CHIKV isolate from Reunion Island were similar at 99.6% to the 2009 sporadic cases on Reunion Island, as well as to the Malagasy strains circulating since 2006 (D’Ortenzio et al., 2011). All isolated sequences bore the A226V substitution within the E1 protein. Altogether, these results have been supporting the hypothesis of a continuous circulation of A226V strains in the southwestern Indian Ocean since 2006 and the possible reintroduction of CHIKV on Reunion Island, most probably from Madagascar. Indeed, in February 2010, an outbreak of CHIKV occurred at the East of Madagascar just before the detection of the first cases in Reunion Island (International Society for Infectious Diseases, 2010). Human travels are likely responsible for the rapid spread of the virus between islands (Morse, 1995) since imported and autochthonous cases on Reunion Island occurred after a holiday period for residents of Reunion Island who often travelled to Madagascar. The probability of an unnoticeable virus circulation on the island cannot be excluded but seems to be unlikely.
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4.2. Population characteristics Trends in terms of age group and sex are similar to those observed during the epidemic of 2005–2006, with a predominance of females over 20 years old that could be due to greater home and gardening activities or differences in clothing leading to a greater exposure of the skin (Gerardin et al., 2008a). Among the people infected in this outbreak, 31% reported they had moved to a new place after the epidemic of 2005–2006. The fact that most of these cases reported “few or no” chikungunya patients in their environment during the 2005–2006 epidemic suggests that they lived in neighbourhoods where the attack rate was low. Indeed, the seroprevalence survey in 2007 did not allow to estimate the prevalence rate by municipality (Gerardin et al., 2008b). The occurrence of this outbreak suggests that the immunity had heterogeneous distribution on this island and that the immunity population in the Saint Paul area was lower. Among them, 22% had never been previously exposed to chikungunya since they had recently moved on to the island. The introduction of immunologically naive population has contributed to create propitious conditions to the development of the cluster. In addition, changes in individual behaviours might have increased population exposure. In fact, among cases having reported the use of protective measures against mosquito bites or put into place preventive measures against mosquito breeding sites during the epidemic 2005–2006, nearly half reported having reduced these protections in 2010. The entomological prospecting showed that the great majority of breeding sites could have been easy to remove by the population (Dehecq et al., 2011). 4.3. Environmental factors Last, environmental factors might have played a role in the occurrence of the outbreak. In our study, three quarters of the cases lived in individual houses and 67% of those who lived in apartments resided at the ground floors, which are well-known factors of infection linked to arboviruses (Gerardin et al., 2008a). In Reunion Island, the vector of chikungunya is Ae. albopictus (Delatte et al., 2008b). The distribution area of Ae. albopictus on the island shows that it is mainly spread over the urban areas, that is to say essentially on the coastline. The typology of breeding places reveals the capacity of Ae. albopictus to colonize several types of water points whether they are natural or anthropogenic. In urban environments, mosquito larvae live mostly in flower pot saucer and small containers, and in peri-urban and rural areas, in bamboo holes and rocks (Delatte et al., 2008a). This omnipresence in urban areas increases the contact with human beings and therefore the risk of CHIKV transmission by this anthropophilic and exophagic vector (Delatte et al., 2010). Vector density has also probably played an important role in extending this cluster since half of the cases have noticed a significant presence of the vector in their environment. In fact, during this outbreak, the house index and Breteau index collected around chikungunya cases were much higher than the level of epidemic risk defined by WHO (for dengue virus and Ae. aegypti) (Dehecq et al., 2011). During the major epidemic 2005–2006, an entomological survey in nine urban areas showed a Breteau index of 68.4 and a house index of 19.2% (Delatte et al., 2008a). These results are similar to those observed in 2010. The main limit of this investigation is that the results are descriptive and based on the patients reports. However, the occurrence of this outbreak caused a crisis situation, in which public health authorities needed to know immediately the characteristics of the CHIKF cases in order to understand its occurrence. Complementary research is to be done; in particular, the seroprevalence rate
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by municipality would be of interest, and sociological studies are important to better understand people’s behaviour. This study sheds a new light on the factors that could explain the re-emergence of CHIKV in Reunion Island five years after the world’s greatest epidemic. The factors that can play a role during the different steps of a re-emerging disease process are numerous and deeply linked and mixed to each other; it is therefore important to have a multifactorial approach. 5. Conclusion The persistent circulation of arboviruses such as CHIKV together with the presence of the vector throughout the year involves a permanent epidemic threat to Reunion Island. Movements of non-immune population and behavioural changes constitute vulnerable cluster to CHIKV infection. These results may contribute to target the population for which a reiterating sensitization campaign is needed. Acknowledgements Agents of Vector Control Team, laboratories and physicians of Reunion Island and the Reference National Center of arbovirus, Sandra Giron, Jean-Sébastien Dehecq, Thomas Margueron, Marianne Mérolle. References Balleydier, E., D’Ortenzio, E., Renault, P., 2008. Épidémiologie du chikungunya à la Réunion. Bilan d’une année de surveillance, 19 avril 2007–18 avril 2008. Institut de Veille Sanitaire, Saint-Maurice. Beesoon, S., Funkhouser, E., Kotea, N., Spielman, A., Robich, R.M., 2008. Chikungunya fever, Mauritius, 2006. Emerging Infectious Diseases 14, 337–338. Borgherini, G., Poubeau, P., Jossaume, A., Gouix, A., Cotte, L., Michault, A., ArvinBerod, C., Paganin, F., 2008. Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on Reunion Island. Clinical Infectious Diseases 47, 469–475. Borgherini, G., Poubeau, P., Staikowsky, F., Lory, M., Le Moullec, N., Becquart, J.P., Wengling, C., Michault, A., Paganin, F., 2007. Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients. Clinical Infectious Diseases 44, 1401–1407. D’Ortenzio, E., Grandadam, M., Balleydier, E., Dehecq, J.S., Jaffar-Bandjee, M.C., Michault, A., Andriamandimby, S.F., Reynes, J.M., Filleul, L., 2009. Sporadic cases of chikungunya, Reunion Island, August 2009. Euro Surveillance 14, 19324. D’Ortenzio, E., Grandadam, M., Balleydier, E., Jaffar-Bandjee, M.C., Michault, A., Brottet, E., Baville, M., Filleul, L., 2011. A226V strains of chikungunya virus, Reunion Island, 2010. Emerging Infectious Diseases 17, 309–311. Dehecq, J.S., Baville, M., Margueron, T., Mussard, R., Filleul, L., 2011. The reemergence of the chikungunya virus in Reunion Island on 2010: evolution of the mosquito control practices. Bulletin de la Societe de Pathologie Exotique 104, 153–160. Delatte, H., Dehecq, J.S., Thiria, J., Domerg, C., Paupy, C., Fontenille, D., 2008a. Geographic distribution and developmental sites of Aedes albopictus (Diptera: Culicidae) during a chikungunya epidemic event. Vector Borne Zoonotic Diseases 8, 25–34. Delatte, H., Desvars, A., Bouetard, A., Bord, S., Gimonneau, G., Vourc’h, G., Fontenille, D., 2010. Blood-feeding behavior of Aedes albopictus, a vector of chikungunya on La Reunion. Vector Borne Zoonotic Diseases 10, 249–258. Delatte, H., Paupy, C., Dehecq, J.S., Thiria, J., Failloux, A.B., Fontenille, D., 2008b. Aedes albopictus, vector of chikungunya and dengue viruses in Reunion Island: biology and control. Parasite 15, 3–13. Desenclos, J., 2007. Maladies infectieuses émergentes. In: Bourdillon, F., Brücker, G., Tabuteau, D. (Eds.), Traité de santé publique. , 2nd ed. Médecine – Sciences Flammarion, Paris, pp. 437–442. Gerardin, P., Guernier, V., Perrau, J., Fianu, A., Le Roux, K., Grivard, P., Michault, A., de Lamballerie, X., Flahault, A., Favier, F., 2008a. Determinants of chikungunya virus infection in the Reunion Island: Results of the SEROCHIK seroprevalence survey in the population, August–October 2006. Bulletin Epidémiologique Hebdomadaire 38-39, 361–366. Gerardin, P., Guernier, V., Perrau, J., Fianu, A., Le Roux, K., Grivard, P., Michault, A., de Xavier, L., Flahault, A., Francois, F., 2008b. Estimating chikungunya prevalence in La Reunion Island outbreak by serosurveys: two methods for two critical times of the epidemic. BMC Infectious Diseases 8, 99. International Society for Infectious Diseases Chikungunya: Madagascar (Fianarantsoa), Myanmar Institut Pasteur from Madagascar: Madagascar, 286-2011. Available from http://www.promedmail.org/pls/apex/f?p=2400:1202: 4493792339191053::NO::F2400 P1202 CHECK DISPLAY.
90
P. Vilain et al. / Acta Tropica 123 (2012) 85–90
Morse, S.S., 1995. Factors in the emergence of infectious diseases. Emerging Infectious Diseases 1, 7–15. Porterfield, J., 1980. Antigenic characteristics and classification of the Togaviridae. In: Schlesinger, R. (Ed.), The Togaviruses. Academic Press, New York, pp. 13–46. Powers, A.M., Logue, C.H., 2007. Changing patterns of chikungunya virus: reemergence of a zoonotic arbovirus. Journal of General Virology 88, 2363–2377. Queyriaux, B., Simon, F., Grandadam, M., Michel, R., Tolou, H., Boutin, J.P., 2008. Clinical burden of chikungunya virus infection. Lancet Infectious Diseases 8, 2–3. Ratsitorahina, M., Harisoa, J., Ratovonjato, J., Biacabe, S., Reynes, J.M., Zeller, H., Raoelina, Y., Talarmin, A., Richard, V., Louis, S.J., 2008. Outbreak of dengue and chikungunya fevers, Toamasina, Madagascar, 2006. Emerging Infectious Diseases 14, 1135–1137. Renault, P., Solet, J.L., Sissoko, D., Balleydier, E., Larrieu, S., Filleul, L., Lassalle, C., Thiria, J., Rachou, E., de Valk, H., Ilef, D., Ledrans, M., Quatresous, I., Quenel, P., Pierre, V., 2007. A major epidemic of chikungunya virus infection on Reunion Island, France, 2005–2006. American Journal of Tropical Medicine and Hygiene 77, 727–731. Ross, R.W., 1956. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. Journal of Hygiene 54, 177–191.
Sergon, K., Njuguna, C., Kalani, R., Ofula, V., Onyango, C., Konongoi, L.S., Bedno, S., Burke, H., Dumilla, A.M., Konde, J., Njenga, M.K., Sang, R., Breiman, R.F., 2008. Seroprevalence of chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004. American Journal of Tropical Medicine and Hygiene 78, 333–337. Sergon, K., Yahaya, A.A., Brown, J., Bedja, S.A., Mlindasse, M., Agata, N., Allaranger, Y., Ball, M.D., Powers, A.M., Ofula, V., Onyango, C., Konongoi, L.S., Sang, R., Njenga, M.K., Breiman, R.F., 2007. Seroprevalence of chikungunya virus infection on Grande Comore Island, union of the Comoros 2005. American Journal of Tropical Medicine and Hygiene 76, 1189–1193. Sissoko, D., Malvy, D., Ezzedine, K., Renault, P., Moscetti, F., Ledrans, M., Pierre, V., 2009. Post-epidemic chikungunya disease on Reunion Island: course of rheumatic manifestations and associated factors over a 15-month period. PLoS Neglected Tropical Diseases 3, e389. Sissoko, D., Moendandze, A., Malvy, D., Giry, C., Ezzedine, K., Solet, J.L., Pierre, V., 2008. Seroprevalence and risk factors of chikungunya virus infection in Mayotte, Indian Ocean, 2005–2006: a population-based survey. PLoS One 3, e3066.