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Sentinel physician’s network in Reunion Island: A tool for infectious diseases surveillance夽 Le réseau de médecins sentinelles à la Réunion : un outil pour la surveillance des maladies infectieuses E. Brottet a,∗, M.C. Jaffar-Bandjee b, E. Rachou c, D. Polycarpe d, B. Ristor e, S. Larrieu a, L. Filleul a a

Cellule de l’institut de veille sanitaire en région océan Indien, 2 bis, avenue Georges-Brassens, CS61002, 97743 Saint-Denis cedex 9, Île de la Réunion b Laboratoire de virologie, CHU site Nord, 97405 Saint-Denis, Île de la Réunion c Observatoire régional de la santé de la Réunion (ORS), 12, rue Colbert, 97400 Saint-Denis, Île de la Réunion d Agence de santé de l’océan Indien, bis, avenue Georges-Brassens, CS61002, 97743 Saint-Denis cedex 9, Île de la Réunion e Caisse générale de sécurité sociale de la Réunion, 4, boulevard Doret, 97704 Saint-Denis cedex 9, Île de la Réunion Received 18 September 2014; received in revised form 13 October 2014; accepted 26 November 2014 Available online 6 January 2015

Abstract The surveillance of infectious diseases in Reunion Island is based on a sentinel network of family physicians (FPs) coordinated by the Indian Ocean regional institute for public health surveillance (French acronym OI Cire). The objectives are to identify and monitor outbreaks of influenza, gastroenteritis, and chicken pox, and to characterize circulating influenza viruses. The network can monitor other potentially epidemic diseases. Method. – The Réunion sentinel network ensures a continuous and permanent surveillance. Physicians send their weekly activity data to the Cire that collects, processes, and interprets it; they also collect samples for biological surveillance of influenza. Statistical thresholds, based on historical data and the estimated numbers of incident cases, are calculated to follow the trend, detect outbreaks, and quantify their impact. Results. – The network currently includes 56 FPs and pediatricians, accounting for 6.5% of FPs on the island. The network has clarified the seasonality of influenza during the austral winter and identified the seasonality of acute diarrhea with an epidemic peak when school starts in August. The sentinel FPs’s reports allowed monitoring the epidemic trend and estimating the number of cases during the 2005 and 2006 chikungunya outbreaks and 2009 influenza A (H1N1) outbreaks. Conclusion. – The network has proven its contribution, responsiveness, and reliability for epidemiological surveillance during outbreak. It is an essential tool for infectious diseases surveillance in Reunion Island. © 2014 Elsevier Masson SAS. All rights reserved. Keywords: Sentinel surveillance; Family physicians; Influenza; Gastroenteritis; Réunion Island

Résumé À la Réunion, la surveillance des maladies infectieuses repose notamment sur un réseau de médecins sentinelles volontaires coordonné par la Cire Océan Indien. Les objectifs sont d’identifier et de suivre l’évolution des épidémies de grippe, de gastro-entérites et de varicelle et de caractériser les virus grippaux circulant. Le réseau peut être mobilisé pour surveiller d’autres maladies à potentiel épidémique. Méthode. – Le réseau de médecins sentinelles de la Réunion est un système de surveillance permanent. Les médecins transmettent leurs données d’activité hebdomadaire à la Cire qui les saisit, les analyse et les interprète, et ils effectuent des prélèvements pour la surveillance biologique de la grippe. Des seuils statistiques basés sur les données historiques et l’estimation du nombre de cas incidents de pathologie sont calculés afin de suivre la tendance, de détecter des épidémies et d’en quantifier l’impact.

夽 This study was presented at the 1st International Forum for Public Health Surveillance and Response in Island Territories, on June 11, 2013, and at the French Indian Ocean Family Practice Congress on April 26, 2013. ∗ Corresponding author. E-mail address: [email protected] (E. Brottet).

http://dx.doi.org/10.1016/j.medmal.2014.11.004 0399-077X/© 2014 Elsevier Masson SAS. All rights reserved.

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Résultats. – En 2014, le réseau compte 56 médecins généralistes et pédiatres libéraux représentant 6,5 % des médecins. Le réseau a permis de préciser la saisonnalité de la grippe en hiver austral et d’identifier une saisonnalité des diarrhées aiguës avec un pic épidémique à la rentrée scolaire d’août. Durant les épidémies de chikungunya de 2005–2006 et de grippe A (H1N1) en 2009, le suivi de la tendance épidémique et l’estimation du nombre de cas ont reposé sur les déclarations des médecins sentinelles. Conclusion. – Le réseau a démontré son intérêt, sa réactivité et sa fiabilité dans la surveillance épidémiologique lors d’épidémie. C’est un élément essentiel dans la surveillance des maladies infectieuses à la Réunion. © 2014 Elsevier Masson SAS. Tous droits réservés. Mots clés : Surveillance sentinelle ; Grippe ; Gastro-entérite ; Réunion

1. Introduction Reunion Island is a French Overseas Department (French acronym Dom) located in the heart of the Indian Ocean, between Madagascar and Mauritius, with a population of 850,000 inhabitants. The climate is tropical and especially favorable to infectious agents and their vectors [1]. It is active in tourism and trade with its neighboring countries (Madagascar, Mauritius, Comoros, Seychelles, and many East African and South East Asian countries) with a permanent risk of importing infectious diseases. A local surveillance network was implemented in 1996 under the aegis of Reunion Island Regional Health and Social Affairs Services (French acronym DRASS) and General Council to obtain data on the circulation of influenza virus and dengue fever in Reunion Island. The network was initially supported by a group of Médecins du Monde physicians. The network objectives were to document dengue circulation, to identify and monitor influenza outbreaks, and to identify and characterize influenza viruses circulating in Reunion Island [2]. Reunion Island is located in a tropical area in the southern hemisphere, and a specific viral circulation may be observed compared to mainland France in terms of seasonality and type of circulating virus. The surveillance networks in the southern hemisphere are located in countries such as Australia or South Africa, far away from Reunion Island. A network of sentinel physicians (SPN) located in Reunion Island created its own system to improve the response in data exchange and availability of physicians, based on the operative mode of sentinel physician networks in France [3–5]. The network has undergone several changes in terms of operation and monitored diseases since its implementation. It was reorganized jointly in July 1998, by the Drass and Reunion Island Regional Health Observatory (French acronym ORS) in charge of the network. The Indian Ocean Regional Institute for Public Health Surveillance (French acronym Cire) took over the coordination and management of the network in January 2010, according to the new regulations for healthcare surveillance at local and national levels. Surveillance of acute diarrhea was added to that of dengue fever and influenza in 2000, after consulting the network physicians. Conversely, following the implementation of mandatory reporting in 2006, dengue fever was no longer monitored by the SPN. Finally, varicella was added to monitored diseases in 2012 to describe seasonality and acquire epidemiological on varicella at Reunion Island.

Reunion Island, thus, has its own SPN, independent from the one in continental mainland France. It has allowed physicians to monitor infectious diseases on the highly exposed island territory for 18 years. Our purpose was to describe the network, its contribution to the surveillance of infectious diseases on Reunion Island, and its implication in outbreaks. 2. Material and method 2.1. Network management OI Cire is responsible for the management and scientific coordination of the SPN (Fig. 1). It regularly recruits new physicians to maintain a network covering the whole territory, at meetings and conferences, or by telephone solicitation. These physicians all volunteered to participate in the network. Every week, Cire epidemiologists collect, process, and interpret the data, and solicit physicians if necessary. Cire also answers questions from sentinel physicians. Periodic feedback is achieved through thematic epidemiological updates.

Fig. 1. Organization of the sentinel FP surveillance system on Reunion Island. Organisation du système de surveillance des médecins sentinelles de la Réunion.

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Cire also organizes regular meetings of network participants to promote mutual exchanges.

results of all tests are sent to the OI Cire at the end of each test series.

2.2. Collected data

2.5. Data processing

Every week, several epidemiological indicators, identified according to physicians’ reports, are collected (by Internet, fax, or phone):

Every week, the percentage of consultations for each condition is calculated, and the total number of consultations on the island is estimated, taking into account the rate of consultations carried out by participating physicians compared to the total number of consultations carried out on the island (data provided by the Social Security (SSTC) from healthcare prescriptions). The weekly data is thus described in terms of overall activity and syndrome, and compared to that of the previous week, and to that of the same period in previous years. The time trends in the number of detected influenza viruses and positivity rate are also analyzed weekly. The number of patients having consulted a physician for each condition on the whole island is estimated according to the activity of sentinel physicians compared to all the medical activity on the island according to healthcare insurance data for that week.

• number of office consultations; • number of home visits; • number of consultations for influenza-like illness: sudden onset fever greater than or equal to 38 ◦ C and cough, possibly associated with dyspnea, and/or myalgia, and/or headaches; • number of consultations for acute diarrhea: more than 3 liquid stools per day in the previous 15 days, leading to consultation; • number of consultations for varicella: sudden onset of a typical rash (erythematous and vesicular for 3 to 4 days, itchy, with a scab stage) with mild fever (37.5 ◦ C–38.0 ◦ C).

2.6. Feedback 2.3. Data collection method A centralized VoozanooTM type (http://www.epiconcept.fr/ fr/produit/voozanoo) Internet database was created in late 2010, to improve and simplify data collection by sentinel physicians. Each physician can use the application with a login and password to enter weekly data and visualize surveillance curves. OI Cire is the database administrator and therefore has access to all data collected every week and can also add or remove monitored diseases in the application. Some participating physicians (25%) do not use this tool and send their data by fax (most of the time). In case of a sanitary alert, sentinel physicians may be asked to provide the number of consultations, for a given period, for another disease than those routinely monitored. 2.4. Biological monitoring of influenza All participating physicians are encouraged to perform 1 to 2 weekly nasopharyngeal swabs randomly in patients presenting with influenza-like illness for less than 3 days. A form sent with the swab is completed by the physician, with patient data (sex, age), the date of onset of symptoms, date of sampling, information on influenza vaccination, and documented travelling in the previous 7 days. OI Cire is responsible for providing the sampling equipment to physicians and a biological transport company to bring samples safely to the laboratory. Biological tests are performed by the Teaching Hospital Virology Laboratory (CHU North) along with the South region National Reference Center for influenzae virus. The tests are performed with RT-PCR to identify the influenza A virus (H1N1) pdm09, A non- H1N1, and B. The laboratory transmits individual results to the physician, and the anonymous aggregated

The results of surveillance are published in the OI Cire Epidemiological Updates published weekly in case of a flare of one of the monitored diseases. These updates are sent by email to registered mailing list partners, as well as to all sentinels. These updates can also be sent with recommendations for the management of patients, developed in collaboration with the OI-ARS surveillance alert and health management team (French acronym CVAGS), to sentinel physicians but also to other healthcare professionals, and to the global population. Besides this feedback, sentinel physicians receive epidemiological news or other scientific information (vaccination campaigns, indications for laboratory tests, etc.). 2.7. Conducting studies This network of FPs may also be asked to participate in epidemiological studies conducted by the OI Cire. 2.8. Regulatory aspects This surveillance network received regulatory approvals, including the CNIL approval in July 2012, for the evaluation and surveillance of influenza and gastroenteritis epidemics on Reunion Island. 3. Results 3.1. Descriptive results The SPN included 54 FPs and 2 private practice pediatricians as of January 1, 2014, 24 male and 30 female physicians. These physicians were distributed over 21 of the 24 cities on the island (Fig. 2).

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Fig. 2. Geographical distribution of sentinel GP’s in Reunion Island in 2014 (54 GP’s and 2 pediatricians). Répartition géographique des médecins sentinelles de la Réunion en janvier 2014 (54 médecins généralistes et 2 pédiatres libéraux).

There were 828 FPs and 35 private practice pediatricians on Reunion Island as of January 1, 2014, giving a 6.5%-rate of sentinel physicians. Consultations carried out from January to August 2014, and reported by sentinel physicians, accounted for 4.7% of all consultations carried out in family medicine and private pediatric practice reimbursed by the healthcare insurance. The participation rate1 significantly increased after implementation of the system. Systematic weekly reminders to physicians who had not sent their data were implemented in October 2007; this resulted in a significant increase of the average annual participation rate from 41% in 2006 to 90% in 2013. The weekly participation rate ranged from 73% to 100% in 2013. 3.2. Impact of the network in terms of epidemiological knowledge Currently, the 3 seasonal conditions monitored by the network are epidemic-prone diseases (Fig. 3). Fifteen years of influenza surveillance have allowed demonstrating seasonality in the beginning or at the end of the austral winter at Reunion Island (May to October), corresponding to the period of influenza circulation in the Southern Hemisphere. However, an increase was sometimes observed in March, probably consecutive to epidemics in the Northern Hemisphere and related to the frequent exchanges with continental mainland France [6–8].

The surveillance of circulating viruses has confirmed this trend, with the detection of influenza virus throughout the year, and an increase in the number of viruses during the austral winter. The results of this surveillance are used to rapidly inform physicians on the current epidemiology. They were also used to change the vaccination campaign period that was not adapted to the epidemiological context of Reunion Island in the Southern Hemisphere. The High Council for Public Health issued recommendations for the flu vaccination strategy in Reunion Island in June 2010 [9]. The influenza vaccination campaign has since then begun in April, before the beginning of austral winter favorable to circulation of influenza viruses. The surveillance of acute diarrhea also allowed identifying a seasonal epidemic of gastroenteritis with a peak in late Augustearly September, shortly after the beginning of the school year. The hospital biological laboratory surveillance, along with clinical surveillance of sentinel physicians, also allowed identifying an outbreak of Norovirus gastroenteritis for the first time on Reunion Island, in 2007. Then in 2012, a massive Rotavirus epidemic occurred on Reunion Island between August and November; it was reported and managed by the SPN and Oscour® network monitoring consultations in the emergency department [10]. Varicella was monitored for 2 years to assess the sanitary impact of this disease on the island. It could be replaced by another indicator shortly. 3.3. Impact of the network on exceptional outbreaks

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Number of reporting physicians (having sent a file or reported zero cases) over the number of active physicians (physicians enrolled minus absents during the week).

The number of patients having consulted for an FP at Reunion Island for influenza-like illness, as well the number of confirmed A (H1N1) pdm09 cases, during the influenza A (H1N1) pdm09

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Fig. 3. Weekly percentage of consultations for ILI, acute diarrhea, and varicella, reported by the FP sentinel network on Reunion Island in 2013. Pourcentage hebdomadaire des consultations pour syndrome grippal, diarrhées aiguës et varicelle, rapporté par le réseau de médecins sentinelles de la Réunion en 2013.

pandemic, were estimated by extrapolating weekly SPN data to SSTC data (Fig. 4). This estimation of cases allowed following the trend and the impact of the influenza pandemic in the global population on all Reunion Island. It is also routinely used in the monitoring of seasonal diseases. The SPN, since its implementation, has

demonstrated its ability to follow the course of major epidemics and to assess their impact. SPs achieved this, as soon as the outbreak is identified, by rapidly collecting additional indicators. A dengue epidemic episode was observed and followed in 2004. On this occasion, the SPN was able to prove its important role in the epidemiological surveillance of the disease [11].

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Fig. 4. Estimations of ILI and influenza A(H1H1)pdm09 consultations from June to September 2009 in Reunion Island. Estimations quantitatives des grippes cliniques et des grippes A(H1N1)pdm09 de juin à septembre 2009 à la Réunion.

The network physicians were instructed to report suspected cases of chikungunya seen in consultation after identifying the first cases of chikungunya on Reunion Island in 2005. This surveillance was maintained and reinforced in 2006 by recruiting 20 more GPs specifically monitoring the disease. Throughout the outbreak, the epidemiological evolution was monitored on SGPN data from which the estimated number of weekly cases was determined [12–14]. The network was one of the major tools used for the surveillance of the 2009 influenza pandemic, soon after the international alert concerning a new influenza virus [15]. Unlike for the chikungunya outbreak that involved an emerging virus, the SGPN had already monitored influenza for 14 years and was therefore ready to monitor the epidemic on the island. The first indigenous cases of influenza A (H1N1) pdm09 in Reunion Island was thus identified on a sample collected by a sentinel physician on July 22, 2009. The weekly activity data for ILI reported by sentinel physicians and the results of virological tests allowed estimating the number of incident cases of influenza A (H1N1) pdm09 having occurred on the island every week (Fig. 4) [16]. 3.4. Dealing with specific epidemiological studies A study was recently conducted to screen retrospectively for respiratory infectious agents in nasopharyngeal samples collected by the SPN on Reunion Island from 2011 to 2012. 4. Discussion Reunion Island SPN is an essential tool for the surveillance of infectious diseases on the local level, providing data for the global population, targeting patients consulting for less severe conditions than those reported by the emergency department or data from death certificates. Its contribution to epidemiology has been repeatedly demonstrated, including for the permanent surveillance of influenza leading to modify the vaccination campaign, or during outbreaks such as the chikungunya

epidemic that occurred on Reunion Island from 2005 to 2006 [8,12,13]. The successive recruitment campaigns have resulted in obtaining almost 7% of SPs. This is much higher than the mainland France influenza surveillance networks, which groups 2% of physicians [3,4,17]. Furthermore, the average weekly participation of SP on Reunion Island was 90% in 2013, compared to that of mainland France ranging between 73% and 78% for the GROG network, and 27% for the Sentinelles network [18,19]. The low rate of participation for influenza surveillance in 2006 may be explained by the greater involvement of physicians for the ongoing chikungunya epidemic, at the expense of influenza and gastroenteritis surveillance. In fact, the rate of participation during the chikungunya epidemic peak reached 98%. This network covers most towns on island, giving a global image of the epidemiological evolution on the island. This is why the total number of consultations can be extrapolated from network data. However, the representativeness of sentinel physicians compared to all physicians on the island may be questioned. In 2008, the author of a medical thesis focused on SPs on Reunion Island and their involvement during the chikungunya epidemic [20]. The overall objective was to describe Reunion Island sentinel physicians and understand their expectations. The author reported that the reasons why physicians participate in a surveillance network are the need to communicate, altruism, and acquiring intellectual benefits by enriching their knowledge. Sentinel physicians differ from other physicians by their involvement in other private practice associations and more often practice as associates. These characteristics probably do not significantly influence the patients and therefore do not affect the reliability of network data extrapolation. The SPN has long proven it was an indispensable tool for epidemiological surveillance on Reunion Island. However, even if it seems very reliable to monitor seasonal conditions or pandemics, it has limitations because it does not necessarily allow identifying an unexpected or very localized sanitary event. Thus, it must

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be completed by data from other specific surveillance systems (notifiable diseases, monitoring of arboviruses, leptospirosis, and leprosy, etc.) and non-specific systems (SurSaUD® surveillance of emergencies and death [21]). The data provided by all these systems complement each other and allow the OI Cire to have a very good real time evaluation of the sanitary status on the island, to detect unusual events, and to assess the impact of special events. The local management of the network by OI Cire is a major asset for its operation. Indeed, it is crucial that the data are collected, processed, and interpreted locally, given the distance from mainland France and the social and cultural characteristics of the island. The presence of OI Cire with a good knowledge of the local context and of the epidemiological evolution on the island probably contributes significantly to achieve a high rate of SP participation. Furthermore, the ability to organize meetings between SP strengthens the feeling of network fellowship by sharing experience, and allows keeping participants. Finally, the weekly exchange during OI Cire data collection has helped develop close ties between SPs and epidemiologists. This allows the OI Cire to have the opinion of community physicians who are on the frontline of care provision; and to receive reports beyond the monitored conditions that make the Indian Ocean Regional Health Agency implement additional investigations and control measures. 5. Conclusion Reunion Island has a flexible, adaptable, and responsive SPN, relying on motivated healthcare professionals who provide indispensable data for regional health surveillance every week. The local management of this network is a major asset for its operation and provides reliable surveillance data of infectious diseases on the island. 6. Contributors All authors contributed in processing of results and drafting of the article. EB wrote the article, coordinated the study, and processed data provided by the sentinel physician network. SL and LF helped write the article. LF coordinated the surveillance system. MCJF performed virological analyses. ER coordinated the surveillance system until 2009 and provided historical data for publication. DP participated in the processing of results. BR helped with data processing. Disclosure of interest The authors declare that they have no conflicts of interest concerning this article. Funding: The Reunion island sentinel physician network is a permanent healthcare monitoring system, funded by the Indian Ocean Regional Healthcare Agency (French acronym ARS-OI) and the French Institute for Public Health Surveillance (French acronym InVS).

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Acknowledgments We thank all sentinel physicians having participated in the epidemiological surveillance during these 18 years. We also thank the members of the network for their involvement in the surveillance of infectious diseases, including the Saint-Denis University Hospital virology laboratory. Finally, we thank the Regional Observatory of Health (French acronym ORS) for managing the network during 11 years and for the transmission of historical data.

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Sentinel physician's network in Reunion Island: a tool for infectious diseases surveillance.

The surveillance of infectious diseases in Reunion Island is based on a sentinel network of family physicians (FPs) coordinated by the Indian Ocean re...
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