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Revising rates of asymptomatic Zika virus infection based on sentinel surveillance data from French Overseas Territories
International Journal of Infectious Diseases 65 (2017) 116–118
Contents lists available at ScienceDirect
International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid
Short Communication
Revising rates of asymptomatic Zika virus infection based on sentinel surveillance data from French Overseas Territories Lorenzo Subissia,b,* , Elise Daudens-Vayssec, Sylvie Cassadouc, Martine Ledransc, Priscillia Bompardd,e , Joël Gustavef , Maité Aubryg , Van-Mai Cao-Lormeaug, Henri-Pierre Malletd a
Santé Publique France, EPRUS, Saint-Maurice, France European Centre for Disease Control/World Health Organization, Papeete, French Polynesia c Santé Publique France, Regional Unit, Cire, Antilles Guyane, Saint-Maurice, France d Direction of Health, Papeete, French Polynesia e Sorbonne Universités, UPMC Université Paris 06, INSERM, Institut Pierre-Louis d’Épidémiologie et de Santé Publique, IPLESP UMRS 1136, Paris, France f Regional Health Agency, Guadeloupe, Vector Control Unit, France g Institut Louis Malardé, Papeete, French Polynesia b
A R T I C L E I N F O
Article history: Received 14 July 2017 Received in revised form 28 September 2017 Accepted 16 October 2017 Corresponding Editor: Eskild Petersen, Aarhus, Denmark Keywords: Zika virus Sentinel surveillance Asymptomatic infections Pacific islands Caribbean region Vector-borne infections
A B S T R A C T
French Polynesia and the French Territories of the Americas (FTAs) have experienced outbreaks of Zika virus (ZIKV) infection. These territories used similar sentinel syndromic surveillance to follow the epidemics. However, the surveillance system only takes into account consulting patients diagnosed with ZIKV disease, while non-consulting cases, as well as asymptomatic cases, are not taken into account. In the French territories under study, the ratio of consulting to non-consulting patients was found to likely be as low as 1/3 to 1/4, and rough estimates of the ZIKV asymptomatic infections indicated a lower rate than previously reported (i.e., not more than half). © 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/4.0/).
Introduction The first documented outbreak of Zika virus (ZIKV), a mosquitoborne flavivirus associated with neurological complications (CaoLormeau et al., 2016; de Araújo et al., 2016), was reported in 2007. This outbreak involved 70% of the population (5300 individuals) of Yap islands, in the Federated States of Micronesia (Duffy et al., 2009). In 2013–2014, French Polynesia experienced a larger Zika outbreak with an estimated 11.5% of the population (over 30 000 people) having consulted a doctor for suspected ZIKV infection (Musso and Gubler, 2016). In 2015–2016, ZIKV spread throughout the Americas and the Caribbean region (World Health Organization, 2017). Based on data from the Yap outbreak, it was assumed that asymptomatic ZIKV infections account for 80% of the overall
* Corresponding author at: Viral Diseases Department, Scientific Institute of Public Health, Brussels (Belgium). E-mail address: [email protected] (L. Subissi).
infections (Duffy et al., 2009). However, recently published serological data from French Polynesia and Martinique have estimated it to be less than half of the overall infections (Aubry et al., 2017; Gallian et al., 2017). In this study, a rough estimate of the level of asymptomatic infections was performed using the sentinel syndromic surveillance data available from three comparable French Overseas Territories that experienced Zika outbreaks: French Polynesia, Martinique, and Guadeloupe. The study French Polynesia, Martinique, and Guadeloupe have comparable syndromic surveillance systems, which include a network of 35–55 general practitioners (GPs) or consultation sites reporting the number of patients that fit the case definition for a given syndrome on a weekly basis. During the Zika outbreaks, these sentinel networks were considered as representative of all private and public GP consultations in the three territories, as they provided 16–25% of the overall medical consultations in the community, with a regular geographic distribution (Table 1).
https://doi.org/10.1016/j.ijid.2017.10.009 1201-9712/© 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
L. Subissi et al. / International Journal of Infectious Diseases 65 (2017) 116–118
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Table 1 Sentinel surveillance data to estimate ZIKV asymptomatic infection rates. French Polynesia Number of inhabitants
270 000 (Tahiti: 180 000) 4200 Surface (km ) (Tahiti: 1000) 2013-41 Date of emergence (first confirmed case) Dates of the outbreak Oct 2013–Apr 2014 28 Length of the outbreak (weeks) Peak week (from first confirmed case) 9 Number of GPS or sites participating in the sentinel network 45 during the outbreak 30% SN representativeness (ratio of SN sites reported to total consultation sites) 32 000 Total estimated number of symptomatic consulting cases Consultation rate in the population 11.5% Estimated ratio of consulting/non-consulting among 1:3 to 1:4 symptomatic cases Estimated attack rate of symptomatic cases in the population 34–46% ZIKV overall attack rate from seroprevalence data 49% (general population) (Aubry et al., 2017) 86% (Kucharski et al., 2016) Highest estimate of ZIKV overall attack rate Estimated rate of asymptomatic cases 3–51.5% 2
Martinique
Guadeloupe (except North Islands)
390 000
400 000
1100
1600
2015-50 Jan 2016–Oct 2016 35 18 55
2016-02 Apr 2016–Sept 2016 22 15 35
25%
16%
38 350 9.8%
30 560 7.6%
29–39% 42% (blood donors, in early June) (Gallian et al., 2017) ND 3–57%
23–30% ND ND ND
ZIKV, Zika virus; GPS, global positioning system; SN, sentinel network; ND, not determined.
Cases were reported according to local clinically suspected case definitions (Daudens-Vaysse et al., 2016; Mallet et al., 2016). These case definitions, using a combination of a minimum of three symptoms, met those proposed by the European Centre for Disease Prevention and Control and the Pan-American Health Organization, and have proven to be fairly specific and sensitive (Chow et al., 2017). Consultations in emergency structures (hospitals and mobile emergency services) were accounted for in the global surveillance network in French Polynesia, in Martinique, and in Guadeloupe. The total number of clinically suspected cases for the whole country was estimated by summation of these sources and extrapolation. This surveillance system was implemented to monitor the space–time evolution of the epidemic, but in the case of ZIKV, it failed to estimate the total number of infected people. As ZIKV infection mostly causes a mild illness, a significant proportion of infected people may not consult a GP. Furthermore, many cases are asymptomatic. During the Zika outbreaks, the total estimated proportion of individuals who sought medical care with symptoms compatible with ZIKV infection in the three French Territories ranged from 7.6% to 11.5% of the overall population (Table 1). Based on the ZIKV serosurvey conducted in French Polynesia (Aubry et al., 2017), a blood donor study in Martinique (Gallian et al., 2017), and data from a cross-sectional survey conducted in Guadeloupe (Table 2), the estimated ratio of consulting to non-consulting symptomatic suspected cases was found to be in the range of 1:3 to 1:4. Information from the survey in Guadeloupe, which used quota sampling, was gathered through telephone-based interviews of a sample of 501 individuals aged >15 years. The questionnaire was Table 2 Estimate of consultation rates from a cross-sectional study based on telephone interviews with individuals aged >15 years (n = 501) recruited by quota sampling at the end of the Zika outbreak—Guadeloupe, October 2016.a Percentage ZIKV reported symptoms Yes (consulted a GP) No Consultation rate of symptomatic cases
31 (9) 69 29
ZIKV, Zika virus; GP, general practitioner. a Data courtesy of IPSOS Antilles. For details (in French): http://www.ireps.gp/ data/IMG/Rapport_Impact_Comm_Zika_ARS_Mai_2016.pdf.
mainly focused on knowledge of the disease and reported infectious episodes, including specific symptoms (IPSOS Antilles, 2016). The resulting attack rates of symptomatic ZIKV infection ranged from 23% to 46% (Table 1). Using available estimates of ZIKV overall attack rates from (1) seroprevalence studies (Aubry et al., 2017; Gallian et al., 2017), and (2) a modeling study in French Polynesia (Kucharski et al., 2016), it was found that surveillance data indicated asymptomatic infection rates not exceeding half of the overall infections. Discussion The estimated ZIKV asymptomatic infection rates reported here are lower than that found during the 2007 Yap outbreak. This inconsistency with the data from Yap may be due to the limited sample representativeness of the Yap study (Duffy et al., 2009). Alternatively, unknown risk factors, such as environmental or individual conditions, may have affected the ZIKV asymptomatic rate. Taking into consideration the underlying assumptions and limitations, the estimated asymptomatic case rates from sentinel surveillance data reported here, which are compatible with those from seroprevalence studies (Aubry et al., 2017; Gallian et al., 2017), are important in order to improve surveillance systems: they give a more realistic idea of the true number of susceptible individuals throughout the outbreak, because they consider individuals who have experienced asymptomatic infection as immunized. Together with the estimate of the outbreak-specific consultation rate, the new ZIKV asymptomatic infection rate allows a rough prediction of the overall intensity of ZIKV circulation. This is particularly important on islands, where attack rates often reach high percentages (Aubry et al., 2017). Zika outbreak surveillance should be improved by implementing simple cost-effective surveys during outbreaks to assess the outbreak-specific consultation rate and the asymptomatic infection rate, in order to obtain a less error-prone estimate of viral circulation. The first could be estimated using telephone-based interviews and the second by analyzing blood donor samples. Ideally, to be confident that estimates are not biased, a populationbased survey using probability sampling rather than quota sampling should be performed. However, such surveys are often
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L. Subissi et al. / International Journal of Infectious Diseases 65 (2017) 116–118
difficult to implement during outbreaks as they are costly and time-consuming. Standardized protocols should be available to allow the rapid implementation of these surveys in any country or territory where ZIKV is likely to (re-)emerge. In conclusion, the ZIKV asymptomatic infection rate should be taken into account to estimate the level of ZIKV circulation in a country or territory. Determining viral circulation is, in turn, essential to guide public health action. Past reference studies may have overestimated the true ZIKV asymptomatic infection rate, which in the present study settings, corresponds to, at most, half of the infected people. Conflict of interest None declared. Acknowledgements We thank IPSOS Antilles for sharing data. References Aubry Maite, Teissier Anita, Huart Michael, Merceron Sébastien, Vanhomwegen Jessica, Roche Claudine, et al. Zika virus seroprevalence, French Polynesia, 20142015. Emerg Infect Dis 2017;23(4), doi:http://dx.doi.org/10.3201/ eid2304.161549. Cao-Lormeau Van-Mai, Blake Alexandre, Mons Sandrine, Lastère Stéphane, Roche Claudine, Vanhomwegen Jessica, et al. Guillain-Barrè Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet Lond Engl 2016;387(10027):1531–9, doi:http://dx.doi.org/10.1016/ S0140-6736(16)00562-6.
Chow Angela, Ho Hanley, Win Mar-Kyaw, Leo Yee-Sin. Assessing sensitivity and specificity of surveillance case definitions for Zika virus disease. Emerg Infect Dis 2017;23(4):677–9, doi:http://dx.doi.org/10.3201/eid2304.161716. Daudens-Vaysse Elise, Ledrans Martine, Gay Noellie, Ardillon Vanessa, Cassadou Sylvie, Najioullah Fatiha, et al. Zika emergence in the French Territories of America and description of first confirmed cases of Zika virus infection on Martinique, November 2015 to February 2016. Euro Surveill 2016;21(28), doi: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.28.30285. de Araújo Thalia Velho Barreto, Rodrigues Laura Cunha, de Alencar Ximenes Ricardo Arraes, de Barros Miranda-Filho Demócrito, Montarroyos Ulisses Ramos, de Melo Ana Paula Lopes, et al. Association between Zika virus infection and microcephaly in Brazil, January to May, 2016: preliminary report of a casecontrol study. Lancet Infect Dis 2016;16(12):1356–63, doi:http://dx.doi.org/ 10.1016/S1473-3099(16)30318-8. Duffy Mark R, Chen Tai-Ho, Hancock W Thane, Powers Ann M, Kool Jacob L, Lanciotti Robert S, et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 2009;360(24):2536–43, doi:http://dx.doi.org/10.1056/NEJMoa0805715. Gallian Pierre, Cabié André, Richard Pascale, Paturel Laure, Charrel Rémi N, Pastorino Boris, et al. Zika virus in asymptomatic blood donors, Martinique: 2016. Blood [172_TD$DIFF]2017;129(2):263–6, doi:http://dx.doi.org/10.1182/ blood-2016-09-737981. IPSOS Antilles. Study on the impact of prevention communication and information about Zika. 2016. http://www.ireps.gp/data/IMG/Rapport_Impact_Comm_Zika_ARS_Mai_2016.pdf. Kucharski Adam J, Funk Sebastian, Eggo Rosalind M, Mallet Henri-Pierre, Edmunds W John, Nilles Eric J. Transmission dynamics of Zika virus in Island populations: a modelling analysis of the 2013-14 French Polynesia Outbreak. PLoS Negl Trop Dis 2016;10(5), doi:http://dx.doi.org/10.1371/journal.pntd.0004726. Mallet HP, Vial AL, Musso D. Bilan de l’épidémie à virus Zika survenue en Polynésie française entre octobre 2013 et mars 2014. De la description de l’épidémie aux connaissances acquises après l’évènement. Bull Epidémiol Hebd 2016;367– 73:20–1. Musso Didier, Gubler Duane J. Zika virus. Clin Microbiol Rev 2016;29(3):487–524, doi:http://dx.doi.org/10.1128/CMR.00072-15. World Health Organization. Zika situation report. 2017.
Contents lists available at ScienceDirect
International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid
Short Communication
Revising rates of asymptomatic Zika virus infection based on sentinel surveillance data from French Overseas Territories Lorenzo Subissia,b,* , Elise Daudens-Vayssec, Sylvie Cassadouc, Martine Ledransc, Priscillia Bompardd,e , Joël Gustavef , Maité Aubryg , Van-Mai Cao-Lormeaug, Henri-Pierre Malletd a
Santé Publique France, EPRUS, Saint-Maurice, France European Centre for Disease Control/World Health Organization, Papeete, French Polynesia c Santé Publique France, Regional Unit, Cire, Antilles Guyane, Saint-Maurice, France d Direction of Health, Papeete, French Polynesia e Sorbonne Universités, UPMC Université Paris 06, INSERM, Institut Pierre-Louis d’Épidémiologie et de Santé Publique, IPLESP UMRS 1136, Paris, France f Regional Health Agency, Guadeloupe, Vector Control Unit, France g Institut Louis Malardé, Papeete, French Polynesia b
A R T I C L E I N F O
Article history: Received 14 July 2017 Received in revised form 28 September 2017 Accepted 16 October 2017 Corresponding Editor: Eskild Petersen, Aarhus, Denmark Keywords: Zika virus Sentinel surveillance Asymptomatic infections Pacific islands Caribbean region Vector-borne infections
A B S T R A C T
French Polynesia and the French Territories of the Americas (FTAs) have experienced outbreaks of Zika virus (ZIKV) infection. These territories used similar sentinel syndromic surveillance to follow the epidemics. However, the surveillance system only takes into account consulting patients diagnosed with ZIKV disease, while non-consulting cases, as well as asymptomatic cases, are not taken into account. In the French territories under study, the ratio of consulting to non-consulting patients was found to likely be as low as 1/3 to 1/4, and rough estimates of the ZIKV asymptomatic infections indicated a lower rate than previously reported (i.e., not more than half). © 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/4.0/).
Introduction The first documented outbreak of Zika virus (ZIKV), a mosquitoborne flavivirus associated with neurological complications (CaoLormeau et al., 2016; de Araújo et al., 2016), was reported in 2007. This outbreak involved 70% of the population (5300 individuals) of Yap islands, in the Federated States of Micronesia (Duffy et al., 2009). In 2013–2014, French Polynesia experienced a larger Zika outbreak with an estimated 11.5% of the population (over 30 000 people) having consulted a doctor for suspected ZIKV infection (Musso and Gubler, 2016). In 2015–2016, ZIKV spread throughout the Americas and the Caribbean region (World Health Organization, 2017). Based on data from the Yap outbreak, it was assumed that asymptomatic ZIKV infections account for 80% of the overall
* Corresponding author at: Viral Diseases Department, Scientific Institute of Public Health, Brussels (Belgium). E-mail address: [email protected] (L. Subissi).
infections (Duffy et al., 2009). However, recently published serological data from French Polynesia and Martinique have estimated it to be less than half of the overall infections (Aubry et al., 2017; Gallian et al., 2017). In this study, a rough estimate of the level of asymptomatic infections was performed using the sentinel syndromic surveillance data available from three comparable French Overseas Territories that experienced Zika outbreaks: French Polynesia, Martinique, and Guadeloupe. The study French Polynesia, Martinique, and Guadeloupe have comparable syndromic surveillance systems, which include a network of 35–55 general practitioners (GPs) or consultation sites reporting the number of patients that fit the case definition for a given syndrome on a weekly basis. During the Zika outbreaks, these sentinel networks were considered as representative of all private and public GP consultations in the three territories, as they provided 16–25% of the overall medical consultations in the community, with a regular geographic distribution (Table 1).
https://doi.org/10.1016/j.ijid.2017.10.009 1201-9712/© 2017 The Author(s). Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
L. Subissi et al. / International Journal of Infectious Diseases 65 (2017) 116–118
117
Table 1 Sentinel surveillance data to estimate ZIKV asymptomatic infection rates. French Polynesia Number of inhabitants
270 000 (Tahiti: 180 000) 4200 Surface (km ) (Tahiti: 1000) 2013-41 Date of emergence (first confirmed case) Dates of the outbreak Oct 2013–Apr 2014 28 Length of the outbreak (weeks) Peak week (from first confirmed case) 9 Number of GPS or sites participating in the sentinel network 45 during the outbreak 30% SN representativeness (ratio of SN sites reported to total consultation sites) 32 000 Total estimated number of symptomatic consulting cases Consultation rate in the population 11.5% Estimated ratio of consulting/non-consulting among 1:3 to 1:4 symptomatic cases Estimated attack rate of symptomatic cases in the population 34–46% ZIKV overall attack rate from seroprevalence data 49% (general population) (Aubry et al., 2017) 86% (Kucharski et al., 2016) Highest estimate of ZIKV overall attack rate Estimated rate of asymptomatic cases 3–51.5% 2
Martinique
Guadeloupe (except North Islands)
390 000
400 000
1100
1600
2015-50 Jan 2016–Oct 2016 35 18 55
2016-02 Apr 2016–Sept 2016 22 15 35
25%
16%
38 350 9.8%
30 560 7.6%
29–39% 42% (blood donors, in early June) (Gallian et al., 2017) ND 3–57%
23–30% ND ND ND
ZIKV, Zika virus; GPS, global positioning system; SN, sentinel network; ND, not determined.
Cases were reported according to local clinically suspected case definitions (Daudens-Vaysse et al., 2016; Mallet et al., 2016). These case definitions, using a combination of a minimum of three symptoms, met those proposed by the European Centre for Disease Prevention and Control and the Pan-American Health Organization, and have proven to be fairly specific and sensitive (Chow et al., 2017). Consultations in emergency structures (hospitals and mobile emergency services) were accounted for in the global surveillance network in French Polynesia, in Martinique, and in Guadeloupe. The total number of clinically suspected cases for the whole country was estimated by summation of these sources and extrapolation. This surveillance system was implemented to monitor the space–time evolution of the epidemic, but in the case of ZIKV, it failed to estimate the total number of infected people. As ZIKV infection mostly causes a mild illness, a significant proportion of infected people may not consult a GP. Furthermore, many cases are asymptomatic. During the Zika outbreaks, the total estimated proportion of individuals who sought medical care with symptoms compatible with ZIKV infection in the three French Territories ranged from 7.6% to 11.5% of the overall population (Table 1). Based on the ZIKV serosurvey conducted in French Polynesia (Aubry et al., 2017), a blood donor study in Martinique (Gallian et al., 2017), and data from a cross-sectional survey conducted in Guadeloupe (Table 2), the estimated ratio of consulting to non-consulting symptomatic suspected cases was found to be in the range of 1:3 to 1:4. Information from the survey in Guadeloupe, which used quota sampling, was gathered through telephone-based interviews of a sample of 501 individuals aged >15 years. The questionnaire was Table 2 Estimate of consultation rates from a cross-sectional study based on telephone interviews with individuals aged >15 years (n = 501) recruited by quota sampling at the end of the Zika outbreak—Guadeloupe, October 2016.a Percentage ZIKV reported symptoms Yes (consulted a GP) No Consultation rate of symptomatic cases
31 (9) 69 29
ZIKV, Zika virus; GP, general practitioner. a Data courtesy of IPSOS Antilles. For details (in French): http://www.ireps.gp/ data/IMG/Rapport_Impact_Comm_Zika_ARS_Mai_2016.pdf.
mainly focused on knowledge of the disease and reported infectious episodes, including specific symptoms (IPSOS Antilles, 2016). The resulting attack rates of symptomatic ZIKV infection ranged from 23% to 46% (Table 1). Using available estimates of ZIKV overall attack rates from (1) seroprevalence studies (Aubry et al., 2017; Gallian et al., 2017), and (2) a modeling study in French Polynesia (Kucharski et al., 2016), it was found that surveillance data indicated asymptomatic infection rates not exceeding half of the overall infections. Discussion The estimated ZIKV asymptomatic infection rates reported here are lower than that found during the 2007 Yap outbreak. This inconsistency with the data from Yap may be due to the limited sample representativeness of the Yap study (Duffy et al., 2009). Alternatively, unknown risk factors, such as environmental or individual conditions, may have affected the ZIKV asymptomatic rate. Taking into consideration the underlying assumptions and limitations, the estimated asymptomatic case rates from sentinel surveillance data reported here, which are compatible with those from seroprevalence studies (Aubry et al., 2017; Gallian et al., 2017), are important in order to improve surveillance systems: they give a more realistic idea of the true number of susceptible individuals throughout the outbreak, because they consider individuals who have experienced asymptomatic infection as immunized. Together with the estimate of the outbreak-specific consultation rate, the new ZIKV asymptomatic infection rate allows a rough prediction of the overall intensity of ZIKV circulation. This is particularly important on islands, where attack rates often reach high percentages (Aubry et al., 2017). Zika outbreak surveillance should be improved by implementing simple cost-effective surveys during outbreaks to assess the outbreak-specific consultation rate and the asymptomatic infection rate, in order to obtain a less error-prone estimate of viral circulation. The first could be estimated using telephone-based interviews and the second by analyzing blood donor samples. Ideally, to be confident that estimates are not biased, a populationbased survey using probability sampling rather than quota sampling should be performed. However, such surveys are often
118
L. Subissi et al. / International Journal of Infectious Diseases 65 (2017) 116–118
difficult to implement during outbreaks as they are costly and time-consuming. Standardized protocols should be available to allow the rapid implementation of these surveys in any country or territory where ZIKV is likely to (re-)emerge. In conclusion, the ZIKV asymptomatic infection rate should be taken into account to estimate the level of ZIKV circulation in a country or territory. Determining viral circulation is, in turn, essential to guide public health action. Past reference studies may have overestimated the true ZIKV asymptomatic infection rate, which in the present study settings, corresponds to, at most, half of the infected people. Conflict of interest None declared. Acknowledgements We thank IPSOS Antilles for sharing data. References Aubry Maite, Teissier Anita, Huart Michael, Merceron Sébastien, Vanhomwegen Jessica, Roche Claudine, et al. Zika virus seroprevalence, French Polynesia, 20142015. Emerg Infect Dis 2017;23(4), doi:http://dx.doi.org/10.3201/ eid2304.161549. Cao-Lormeau Van-Mai, Blake Alexandre, Mons Sandrine, Lastère Stéphane, Roche Claudine, Vanhomwegen Jessica, et al. Guillain-Barrè Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet Lond Engl 2016;387(10027):1531–9, doi:http://dx.doi.org/10.1016/ S0140-6736(16)00562-6.
Chow Angela, Ho Hanley, Win Mar-Kyaw, Leo Yee-Sin. Assessing sensitivity and specificity of surveillance case definitions for Zika virus disease. Emerg Infect Dis 2017;23(4):677–9, doi:http://dx.doi.org/10.3201/eid2304.161716. Daudens-Vaysse Elise, Ledrans Martine, Gay Noellie, Ardillon Vanessa, Cassadou Sylvie, Najioullah Fatiha, et al. Zika emergence in the French Territories of America and description of first confirmed cases of Zika virus infection on Martinique, November 2015 to February 2016. Euro Surveill 2016;21(28), doi: http://dx.doi.org/10.2807/1560-7917.ES.2016.21.28.30285. de Araújo Thalia Velho Barreto, Rodrigues Laura Cunha, de Alencar Ximenes Ricardo Arraes, de Barros Miranda-Filho Demócrito, Montarroyos Ulisses Ramos, de Melo Ana Paula Lopes, et al. Association between Zika virus infection and microcephaly in Brazil, January to May, 2016: preliminary report of a casecontrol study. Lancet Infect Dis 2016;16(12):1356–63, doi:http://dx.doi.org/ 10.1016/S1473-3099(16)30318-8. Duffy Mark R, Chen Tai-Ho, Hancock W Thane, Powers Ann M, Kool Jacob L, Lanciotti Robert S, et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N Engl J Med 2009;360(24):2536–43, doi:http://dx.doi.org/10.1056/NEJMoa0805715. Gallian Pierre, Cabié André, Richard Pascale, Paturel Laure, Charrel Rémi N, Pastorino Boris, et al. Zika virus in asymptomatic blood donors, Martinique: 2016. Blood [172_TD$DIFF]2017;129(2):263–6, doi:http://dx.doi.org/10.1182/ blood-2016-09-737981. IPSOS Antilles. Study on the impact of prevention communication and information about Zika. 2016. http://www.ireps.gp/data/IMG/Rapport_Impact_Comm_Zika_ARS_Mai_2016.pdf. Kucharski Adam J, Funk Sebastian, Eggo Rosalind M, Mallet Henri-Pierre, Edmunds W John, Nilles Eric J. Transmission dynamics of Zika virus in Island populations: a modelling analysis of the 2013-14 French Polynesia Outbreak. PLoS Negl Trop Dis 2016;10(5), doi:http://dx.doi.org/10.1371/journal.pntd.0004726. Mallet HP, Vial AL, Musso D. Bilan de l’épidémie à virus Zika survenue en Polynésie française entre octobre 2013 et mars 2014. De la description de l’épidémie aux connaissances acquises après l’évènement. Bull Epidémiol Hebd 2016;367– 73:20–1. Musso Didier, Gubler Duane J. Zika virus. Clin Microbiol Rev 2016;29(3):487–524, doi:http://dx.doi.org/10.1128/CMR.00072-15. World Health Organization. Zika situation report. 2017.