Post on 09-Aug-2020
Wildlife epidemiological surveillance ‐
Results of analyses performed from 2006 to 2008 within the framework of the SAGIR network
Anouk Decors, Olivier Mastain Translation by Catherine Carter
National hunting and wildlife agency (ONCFS) Department of studies and research
Edition July 2010
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Suggested citation :
Decors A., Mastain O., 2010, Wildlife epidemiological surveillance, results of analyses performed from 2006 to 2008 within the framework of the SAGIR network, ONCFS/FNC/FDC network. National hunting and wildlife agency (ONCFS) (ed.), Paris, 48p. http://www.oncfs.gouv.fr/Reseau‐SAGIR‐ru105
3Epidémiosurveillance de la faune sauvage – Bilan des analyses effectuées de 2006 à 2008 dans le cadre du réseau SAGIR. Juillet 2010. Pour toute utilisation de ces données, en particulier à des fins scientifiques, merci de prendre contact avec le réseau sagir@oncfs.gouv.fr
TABLE OF CONTENTS
INTRODUCTION .......................................................................................................................................................7
I METHODS ..........................................................................................................................................................8 I.A EPIDEMIOLOGICAL CHARACTERISTICS OF THE SAGIR NETWORK .............................................................................8 I.B DEFINITION OF THE CASE..........................................................................................................................................8 I.C INTERPRETATION OF RESULTS..................................................................................................................................8
II SPATIO‐TEMPORAL DISTRIBUTION OF CASES FROM 2006 TO 2008......................................................................9 II.A ANNUAL DISTRIBUTION OF CASES............................................................................................................................9 II.B MONTHLY DISTRIBUTION OF CASES .......................................................................................................................10 II.C DISTRIBUTION OF CASES PER MUNICIPALITY .........................................................................................................12
III SAMPLE DESCRIPTION ...................................................................................................................................... 14 III.A SPECIES ...................................................................................................................................................................14 III.B DEAD ANIMALS VS. SICK ANIMALS .........................................................................................................................16
IV MAIN INFECTIOUS AND PARASITIC DISEASES DIAGNOSED BETWEEN 2006 AND 2008 ...................................... 16 IV.A NEW PATHOGENS AND DISEASES IDENTIFIED BETWEEN 2006 AND 2008 .............................................................16 IV.B DISEASES WITH AN IMPACT ON WILDLIFE SPECIES’ POPULATIONS OBSERVED BETWEEN 2006 AND 2008 ..........17
IV.B.1 Species whose hunting is authorized, key events .....................................................................................................17 IV.B.1.1 Wood pigeon................................................................................................................................................................. 17 IV.B.1.2 Stock dove ..................................................................................................................................................................... 17 IV.B.1.3 Collared dove ................................................................................................................................................................ 18 IV.B.1.4 European rabbit ............................................................................................................................................................ 18 IV.B.1.5 Roe deer ........................................................................................................................................................................ 18 IV.B.1.6 Chamois ........................................................................................................................................................................ 18 IV.B.1.7 Red fox .......................................................................................................................................................................... 18 IV.B.1.8 European brown hare.................................................................................................................................................... 18 IV.B.1.8.1 Dominant pathological features............................................................................................................................. 18 IV.B.1.8.2 Zoom on European brown hare syndrome (EBHS) ................................................................................................. 20
IV.B.1.8.2.1 EBHS macroscopic findings................................................................................................................ 20 IV.B.1.8.2.2 Distribution of cases per departement from 2005 to 2008 ............................................................... 22
IV.B.2 Protected species, key events...................................................................................................................................23 IV.B.2.1 Alpine ibex..................................................................................................................................................................... 23 IV.B.2.2 Brent goose ................................................................................................................................................................... 24 IV.B.2.3 Red squirrel ................................................................................................................................................................... 24 IV.B.2.4 Gulls .............................................................................................................................................................................. 24 IV.B.2.5 Black‐headed gull .......................................................................................................................................................... 24 IV.B.2.6 Siskin ............................................................................................................................................................................. 24 IV.B.2.7 Greenfinch..................................................................................................................................................................... 25
IV.C ZOONOTIC PATHOGENS IDENTIFIED BETWEEN 2006 AND 2008 ...........................................................................25 IV.C.1 Tularemia ..................................................................................................................................................................25 IV.C.2 Swine erysipelas........................................................................................................................................................25 IV.C.3 Leptospirosis .............................................................................................................................................................25 IV.C.4 Pseudotuberculosis...................................................................................................................................................25
IV.D PATHOGENS SHARED WITH DOMESTIC ANIMALS IDENTIFIED BETWEEN 2006 AND 2008 ....................................26
V INTOXICATIONS IDENTIFIED BY SAGIR FROM 2006 TO 2008.............................................................................. 26 V.A IDENTIFIED CAUSATIVE AGENTS OF INTOXICATIONS .............................................................................................26
V.A.1 Intoxications by anticoagulants from 2006 to 2008.................................................................................................29 V.A.2 Intoxications by cholinesterase inhibitors from 2006 to 2008.................................................................................30 V.A.3 Intoxications by organochlorines from 2006 to 2008 ...............................................................................................31 V.A.4 Intoxications by chloralose from 2006 to 2008.........................................................................................................31 V.A.5 Intoxications by toxicant associations from 2006 to 2008........................................................................................33
V.B DISTRIBUTION PER DEPARTEMENT OF INTOXICATION CASES FROM 2006 TO 2008..............................................34 V.C INTENTIONAL INTOXICATION .................................................................................................................................34
VI EXAMPLES OF COMPLEMENTARY SAGIR EPIDEMIOLOGICAL MONITORING PROGRAMMES ............................... 35 VI.A MONITORING OF INFLUENZA VIRUSES IN THE WILD AVIFAUNA............................................................................35 VI.B MONITORING OF THE WEST‐NILE VIRUS IN THE WILD AVIFAUNA .........................................................................36 VI.C SAGIR, AN ESSENTIAL LINK FOR THE MONITORING OF CLASSICAL SWINE FEVER ..................................................37 VI.D MONITORING OF TUBERCULOSIS IN WILD ANIMALS IN FRANCE ...........................................................................38 VI.E AVIAN SCHISTOSOMA : BIODIVERSITY, HOST – PARASITE RELATIONSHIPS, IMPLICATIONS IN CERCARIAL
DERMATITIS ............................................................................................................................................................39
CONCLUSIONS ....................................................................................................................................................... 41
VII REFERENCES ..................................................................................................................................................... 43
4Epidémiosurveillance de la faune sauvage – Bilan des analyses effectuées de 2006 à 2008 dans le cadre du réseau SAGIR. Juillet 2010. Pour toute utilisation de ces données, en particulier à des fins scientifiques, merci de prendre contact avec le réseau sagir@oncfs.gouv.fr
TABLES AND FIGURES Figure 1 : Number of cases recorded from 2005 to 2008 by the SAGIR network....................................................................................9 Figure 2 : Monthly distribution of cases in 2006, 2007, 2008................................................................................................................11 Figure 3 : Monthly distribution of roe deer cases in 2006, 2007, 2008. ................................................................................................12 Figure 4 : Monthly distribution of European brown hare cases in 2006, 2007, 2008...........................................................................12 Figure 5 : Distribution of cases per municipality in metropolitan France and in Martinique in 2006, 2007 and 2008..........................13 Figure 6 : Ranking of species in the SAGIR sample sinced 1986 according to the number of cases .....................................................14 Figure 7 : Species richness of the SAGIR sample in 2005, 2006, 2007 and 2008 ...................................................................................15 Figure 8 : Monthly distribution of cases in 2006 for the common buzzard, starling, grey heron, blackbird, house sparrow, siskin,
collared dove and greenfinch. ..............................................................................................................................................15 Figure 9 : Dominant pathological features in the European brown hare – Relative evolution between 2005 and 2008.....................19 Figure 10 : Cumulated presence and distribution per departement of pasteurellosis in the European brown hare from 2005 to 2008.
..............................................................................................................................................................................................19 Figure 11 : Frequency of lesions associated with EBHS in the European brown hare between 2006 and 2008 ...................................20 Figure 12 : Frequency of affected organs in EBHS cases in the European brown hare between 2006 and 2008..................................21 Figure 13 : Representation of the principal lesion/organ associations in EBHS cases in the European brown hare from 2006 to 2008.
..............................................................................................................................................................................................21 Figure 14 : Classification of lesion associations most frequently described in EBHS cases in the European brown hare between 2006
and 2008...............................................................................................................................................................................22 Figure 15 : Cumulated presence and distripution per departement of EBHS in the European brown hare from 2005 to 2008. .........23 Figure 16 : Cumulated presence and distribution per departement of tularemia in the European brown hare from 2005 to 2008. .25 Figure 17 : Cumulated presence and distribution per departement of pseudotuberculosis in the European brown hare from 2005 to
2008......................................................................................................................................................................................26 Figure 18 : Departements concerned by anticoagulant intoxications from 2006 to 2008....................................................................30 Figure 19 : Proportion of chloralose intoxications among confirmed intoxication cases in wild birds..................................................32 Figure 20 : Weekly distribution of chloralose intoxication cases in wild birds in France and highly pathogenic avian influenza cases
in Europe in 2006 .................................................................................................................................................................33 Figure 21 : Number of intoxication cases per departement from 2006 to 2008 identified by SAGIR....................................................34 Table I : The 7 most represented species in the database in 2005, 2006, 2007 and 2008. ...................................................................16 Table II : List of the new pathogens and diseases identified by SAGIR between 2006 and 2008. ........................................................17 Table III : Toxicants quantified per species and per year from 2006 to 2008........................................................................................27 Table IV : Number of anticoagulant intoxication cases per species from 2006 to 2008........................................................................29 Table V : Number of cholinesterase inhibitor intoxication cases per species from 2006 to 2008. ......................................................30 Table VI : Number of organochlorine intoxication cases per species from 2006 to 2008. ....................................................................31 Table VII : Number of individuals per species, intoxicated by chloralose in 2006. ................................................................................31 Table VIII : Toxicant associations and species concerned.....................................................................................................................33 Table IX : Number of individuals per species intoxicated intentionally from 2006 to 2008. .................................................................35 Table IX : Observed prevalences of avian schistosoma in 16 bird species according to the visceral or nasal localization of parasites 39
LIST OF ABBREVIATIONS
ADILVA : French association of directors and managers of public veterinary laboratories
ANSES : French agency for food, environmental and occupational health safety
CSF: Classical swine fever
DDD : dichlorodiphenyldichloroethane
DR : Interregional delegation of the ONCFS
EBHS : European brown hare syndrom
FDC : Departemental hunting federation
FNC : National hunting federation
FRC : Regional hunting federation
H5N1 HP : Highly pathogenic avian influenza H5N1
ITD : Technical departemental representative
LDAV : Departemental veterinary laboratory
MAC : Abnormal roe deer mortality
ONCFS : National hunting and wildlife agency
PCB : Polychlorobiphenyles
SAGIR : The term SAGIR was created by Claude Mallet, first national manager of the network. SAGIR is not an acronym, but rather sounds like a motto, SAGIR, surveiller pour agir !
SD : Departemental service of the ONCFS
WN : West‐Nile
5Epidémiosurveillance de la faune sauvage – Bilan des analyses effectuées de 2006 à 2008 dans le cadre du réseau SAGIR. Juillet 2010. Pour toute utilisation de ces données, en particulier à des fins scientifiques, merci de prendre contact avec le réseau sagir@oncfs.gouv.fr
FOREWORD
I am pleased to present you the results of analyses performed within the framework of the SAGIR network during the years 2006, 2007 and 2008.
In 2006, and to a lesser extent in 2007, the network was mobilized in the participation to the management of health crises related to the highly pathogenic avian influenza H5N1. All the network’s organisation levels were involved. The observers, the technical departemental representatives (ITD), the technicians and veterinarians of the departemental veterinary laboratories, managed the inflow of notifications and analyses. But this resourcefulness has also shown its limitations at the data centralization and processing level. This explains the delay in the exploitation of results and in the production of this special report covering three years of monitoring.
These results rely on an exceptional network, both in its human dimensions with its regular collaborations and in its technical and scientific achievements at an unequalled geographical scale. They provide invaluable information to hunters, hunting managers, biologists, epidemiologists, public policy makers and the general public.
This is the occasion to express my deep gratitude to all the people, Presidents, administrators, staff and ITD of the departemental, regional and national hunting federations, hunters and naturalists, agents and ITD of the ONCFS, staff of the departemental veterinary laboratories, the other laboratory partners of SAGIR and the rabies and wildlife laboratory of ANSES in Nancy, Presidents and local councillors, officials of the Ministry of the Environment, who daily participate to the surveillance of wildlife diseases in a direct and practical way or by investing their own means, for a sustainable hunting and the protection of wild birds and mammals.
I hope this report will inform and interest you. You will find a satisfaction questionnaire at the end of this report, which I invite you to fill in with comments and suggestions so as to make the next report of analyses performed in 2009 a document satisfying all ambitions.
Lastly, I invite you to disseminate this report around you. It is available in French and in English, on the Internet pages of the SAGIR network www.oncfs.gouv.fr/Reseau‐SAGIR‐ru105. Administrator and scientific manager of the SAGIR
network
Olivier MASTAIN
6Epidémiosurveillance de la faune sauvage – Bilan des analyses effectuées de 2006 à 2008 dans le cadre du réseau SAGIR. Juillet 2010. Pour toute utilisation de ces données, en particulier à des fins scientifiques, merci de prendre contact avec le réseau sagir@oncfs.gouv.fr
ACKNOWLEDGEMENTS
The authors would like to thank Philippe Aubry (ONCFS), Philippe Berny (veterinary VetAgro Sup Campus of Lyon), Catherine Carter (ONCFS), Charlotte Dunoyer (FNC), Hubert Ferté (University of Reims Champagne‐Ardenne), Dominique Gauthier (ADILVA), Sophie Grammont (ONCFS), Jean‐Sébastien Guitton (ONCFS), Jean Hars (ONCFS), Philippe Landry (ONCFS), Marie Moinet (ANSES), Viviane Moquay‐Tkaczuk (ADILVA), Sophie Rossi (ONCFS) and Alain VIRY (LDAV du Jura) for their careful reading and their contribution to this report.
The SAGIR network is grateful to all the observers, in particular the hunters and technicians of the ONCFS who relentlessly submit their observations, for the knowledge, hunting management and environmental protection.
The SAGIR network sincerely thanks all the actors of the network for their contribution :
The hunters and naturalists, the veterinary practitioners at their side ;
The national, regional and departemental hunting federations, FNC, FRC Alsace, FRC Auvergne, FRC Bourgogne, FRC Centre, FRC Corse, FRC Haute‐Normandie, FRC Languedoc‐Roussillon, FRC Lorraine, FRC Nord Pas‐de‐Calais, FRC Picardie, FRC Provence Alpes Côte d’Azur, FRC Rhône‐Alpes, FRC Poitou‐Charentes, FRC Pays‐de‐la‐Loire, FRC Midi‐Pyrénées, FRC Limousin, FRC Ile‐de‐France, FRC Franche‐Comté, FRC Champagne‐Ardenne, FRC Bretagne, FRC Basse‐Normandie, FRC Aquitaine, FDC 01,FDC 02, FDC 03, FDC 04, FDC 05, FDC 06, FDC 07, FDC 08, FDC 09, FDC 10, FDC 11, FDC 12, FDC 13, FDC 14, FDC 15, FDC 16, FDC 17, FDC 18, FDC 19, FDC 2A, FDC 2B, FDC 21, FDC 22, FDC 23, FDC 24, FDC 25, FDC 26, FDC 27, FDC 28, FDC 29, FDC 30, FDC 31, FDC 32, FDC 33, FDC 34, FDC 35, FDC 36, FDC 37, FDC 38, FDC 39, FDC 40, FDC 41, FDC 42, FDC 43, FDC 44, FDC 45, FDC 46, FDC 47, FDC 48, FDC 49, FDC 50, FDC 51, FDC 52, FDC 53, FDC 54, FDC 55, FDC 56, FDC 57, FDC 58, FDC 59, FDC 60, FDC 61, FDC 62, FDC 63, FDC 64,FDC 65, FDC 66, FDC 67, FDC 68, FDC 69, FDC 70, FDC 71, FDC 72, FDC 73, FDC 74, FDC 75, FDC 76, FDC 77, FDC 78, FDC 79, FDC 80, FDC 81, FDC 82, FDC 83, FDC 84, FDC 85, FDC 86, FDC 87, FDC 88, FDC 89, FDC 90, FDC 972 and in particular the technical departemental representatives ;
The interregional delegations and departemental services of the National hunting and wildlife agency (ONCFS), DR Alpes Méditerranée – Corse, DR Bretagne Pays de la Loire, DR Nord‐Ouest, DR Nord‐Est, DR Poitou‐Charente Limousin, DR Bourgogne Franche‐Comte, DR Sud‐Ouest, DR Auvergne Languedoc‐Roussillon, DR Centre Ile‐de‐France, SD 01, SD 02, SD 03, SD 04, SD 05, SD 06, SD 07, SD 08, SD 09, SD 10, SD 11, SD 12, SD 13, SD 14, SD 15, SD 16, SD 17, SD 18, SD 19, SD 2A, SD 2B, SD 21, SD 22, SD 23, SD 24, SD 25, SD 26, SD 27, SD 28, SD 29, SD 30, SD 31, SD 32, SD 33, SD 34, SD 35, SD 36, SD 37, SD 38, SD 39 ,SD 40, SD 41, SD 42, SD 43, SD 44, SD 45, SD 46, SD 47, SD 48, SD 49, SD 50, SD 51, SD 52, SD 53, SD 54, SD 55, SD 56, SD 57, SD 58, SD 59, SD 60, SD 61, SD 62, SD 63, SD 64, SD 65, SD 66, SD 67, SD 68, SD 69, SD 70, SD 71, SD 72, SD 73, SD 74, SD 75, SD 76, SD 77, SD 78, SD 79, SD 80, SD 81, SD 82, SD 83, SD 84, SD 85, SD 86, SD 87, SD 88, SD 89, SD 90, SD972 and in particular the technical departemental representatives ;
The departemental veterinary laboratories and the “Conseils généraux”, LDA 01, LVD 02, LVD 03, LVD 04, LVD 05, LVD 06, LDA 08, LVD 09, LDA 10, LVD 11, Aveyron Labo, LDA 13, Laboratoire départemental Franck Duncombe, LASAT, LDA 18, LDA 19, Laboratoire départemental d'analyses vétérinaires, agricoles et des eaux d'Ajaccio, LDA 2B, LDA 21, Laboratoire de développement et d'analyse de Ploufragan, LDA 23, LDA 24, LVD 25, LDA 26, LDA 27, IDHESA Bretagne – Océane, LDA 30, LVD 31, LVD 32, LABSA 33, LVD 34, Institut en santé Agro ‐ environnement 35, LDA 36, LDA 37, LVD 38, LDA 39, LDA 40, LVD 42, LDA 43, Institut départemental d'analyses et conseil de Nantes, LVD 46, LVD 47, LDA 48, LVD 49, LDA 50, LDA 52, LVD 53, LVD 54, LVD 55, LDA 56, Laboratoire central d'analyses de Metz, LDA 58, LDA 59, LDA 60, LDA 61, LDA 62, LDA 63, Laboratoire des Pyrénées, Centre d'analyses Méditerranée – Pyrénées, LVD 67, LVD 68, LVD 69, LVD 70, LVD 71, LVD 72, LDA 73, LVD 74, LVD 76, LVD 77, LDA 78, LVD 79, LVD 80, Laboratoire départemental d'hygiène d'Albi, LVD 82, LDA 83, LDA 84, LDA 85, Laboratoire d'analyse et de sécurité alimentaire de Poitiers, LVD 87, LVD 88, Institut départemental de l'environnement et d'analyses d'Auxerre, LDAV972 ;
The toxicology laboratory of the veterinary VetAgro Sup Campus of Lyon ;
The Biomathematics and epidemiology unit of the veterinary VetAgro Sup Campus of Lyon ;
The Vectorial transmission and epidemiosurveillance of parasitic diseases laboratory of the University of Reims Champagne‐Ardenne ;
The national reference laboratories of ANSES and the Pasteur Institute ;
Vet Diagnostics ;
The rabies and wildlife laboratory of ANSES in Nancy which centralizes the network’s data since 1993, participes to the network’s running and contributes to the scientific valorisation of results.
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INTRODUCTION
SAGIR is a network for the epidemiological surveillance of wild birds and terrestrial mammals, in particular species whose hunting is authorized in France. This surveillance, based on a constant partnership between the Hunting federations and the National hunting and wildlife agency (ONCFS) has been carried out since 1955 (de Lavaur, 1978), it was consolidated in 1972 and has taken on its its present dimension in 1986 under the name SAGIR. It has four main objectives : i) characterization in time and space of wild bird and mammal diseases with priority stake ? for the health of populations , ii) early detection of the appearance of new wildlife diseases, iii) monitoring of acute non‐intentional effects of the use of phytopharmaceutical products in agriculture on wild birds and mammals, iv) knowledge of wildlife pathogens that are transmissible to humans, with a view to the latter’s protection, in particular that of hunters. This general long‐term monitoring also contributes to the knowledge of pathogens that are shared by wildlife and domestic animals. This data is fundamental for hunting managers and for risk managers and assessors.
To carry out this epidemiological surveillance, the SAGIR network uses the detection of wild bird and mammal mortality and the determination of its aetiology.
This report presents the results of the SAGIR network recorded from 2006 to 2008, representing 11 634 wild bird and mammal specimens. These animals were discovered dead or sick in the field, collected by the network observers and then analyzed by the departemental veterinary laboratories. The analysis systematically consists of an autopsy and, when necessary, further examinations are performed to specify and confirm the post mortem diagnosis. The data sources of this report are macroscopic findings, the results of the histology, bacteriology, virology, parasitology, toxicology and other veterinary areas of specialization.
After outlining the methods, we detail the results per species, per year and per “département”. The main diagnosed infectious and parasitic diseases are presented in a specific chapter and the following chapter presents intoxication cases. Although the results generated by the network can generally only be analysed in a descriptive way, they can extend scientific questioning through new analytical hypotheses. In this case, another research team takes over or works in partnership with the network. Indeed, for a sound understanding of a health phenomenon, general surveillance data are insufficient, and must be completed with further results steming from a strengthened and targeted surveillance, bringing together different specialists in ecology, veterinary diagnostic, pathology, epidemiology, to have an integrated vision of the phenomenon. Six examples are highlighted in this report to illustrate the complementarity between the SAGIR and other epidemiosurveillance systems.
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I METHODS
I.A Epidemiological characteristics of the SAGIR network The SAGIR network is a generalist1 epidemiological surveillance2 network with a nationwide geographical coverage. The data’s mode of production is passive3 but can, on the occasion of a special operation, be active4. The network uses opportunistic or convenience sampling (Dohoo et al., 2003), in other words, the most accessible dead or sick animals. For all these reasons, the collected sample is not a representative sample of the population. It is a qualitative monitoring, it enables the detection of the presence of a species’ pathogen at a place and time t, but it does not for the time being allow the quantification of a health phenomenon and hence calculation of prevalence5. The SAGIR network is a participative network, which means that its smooth running relies predominantly on the contribution of field actors in the network, on their motivation and the information available to them on health episodes affecting wildlife. I.B Definition of the case A SAGIR case corresponds to an animal observed dead or sick, incapable of returning to the natural environment or a hunter‐killed animal showing signs of disease at the opening of the carcass. Healthy animals, showing no signs of disease and shot or trapped for the screening of a specific disease are not considered as a SAGIR case and are not exploited within the framework of this report. An exploitable SAGIR case is a SAGIR case with an autopsy report and a SAGIR form, whose information has been centralized in the SAGIR database. A non exploitable SAGIR case is thus a case for which :
- the SAGIR form is missing;
- the case history is vague6 or incomplete7 ;
- the autopsy has not been performed ;
- or the autopsy report has not been submitted for the data centralization.
Advanced state of decomposition of the dead bodies is not a criterion for exclusion of the exploitable SAGIR case since their autopsy has, in many cases, revealed the presence of a pathogen of relevance for the species’ conservation or human health.
For the present report, in 2006, 2007 and 2008, respectively 3,5 % , 2,6 % and 2,1 % of SAGIR cases could not be considered as exploitable.
Throughout this report, the term « case » is used for exploitable SAGIR cases. I.C Interpretation of results For the interpretation of the SAGIR network data, it is essential to bear in mind the constraints imposed by the sampling and the various filters applied to the different stages of the SAGIR protocol. They are not detailed in the present report and mainly come within the following :
1 Non specialized. The network is interested in several diseases and in several animal species. 2 This more general term is used to refer to all epidemiosurveillance et and epidemiovigilance networks. An epidemiosurveillance network is devoted to the surveillance of diseases that are present in a territory, as opposed to an epidemiovigilance network, which enables the detection of the appearance of a new or exotic disease (Dufour and Hendrikx, 2007). 3 One describes as passive any surveillance activity relying on the spontaneous notification of cases or suspected cases of the disease monitored by the actors as data sources. It is thus impossible to know in advance the number, nature and localization of the data collected by the network. This type of organization is adapted to situations where the purpose is to give an early warning in case of the appearance or re‐appearance of a disease (Dufour et Hendrikx, 2007). 4 The production is active when it is organized specifically, with for example a sampling design, sampling and analyses performed for the sole purpose of epidemiosurveillance (Toma et al., 2001). 5 Measurement of the frequency of a disease existing at a time t (P = total number of cases at a time t / total population at this time). 6 For example, with only the observed species, the municipality and the date of discovery mentioned. 7 For example, with only the specimen’s genus, without mention of the species.
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- mortality detection probability. The dead bodies are not actively searched for, they are discovered in a fortuitous manner. The observed apparent mortality does not represent the true mortality and largely underestimates it;
- the reporting of spontaneous information based on the motivation of observers and SAGIR ITD ; - a non‐homogeneous sampling process from one departement to another. Indeed, the selection of individuals whose analysis results will be entered into the database is subjected to a series of non standardized filters, which are as many sources of selective forces (and hence of bias) coming into play in the building of the sample, from the reporting of the dead body to the collection, transport and analysis to the centralization.
For all these reasons, caution is required in the data exploitation, notably with regard to the quantification of a health phenomenon or the data representativeness for a wildlife species. The SAGIR network is adapted to the detection of the presence of a disease, so we shall restrict this report to the disease outbreaks8. On the other hand, it is difficult to conclude on the absence of a disease in the absence of data. The absence of data in a municipality does not necessarily imply that there is no wildlife mortality or disease in this municipality. It can result from the true absence of the pathogen or from a lack of observation (hostile environment, presence of important vegetation cover, absence of ITD in the departement, …), or lack of reporting or analysis (absence of LDAV in the departement, dead body in a too advanced state of decomposition, …). Similarly, SAGIR data allow the comparison in time and place of a pathogen’s presence with all the necessary caution. On the other hand, to compare the amplitude of a health phenomenon in time and space, a prior analysis of the increase in case numbers and an assessment of the portion due to a higher observation pressure and that attributable to the true progression of the disease are required, which is impossible with the general SAGIR protocol.
II SPATIO‐TEMPORAL DISTRIBUTION OF CASES FROM 2006 TO 2008
II.A Annual distribution of cases After a substantial increase in the number of cases in 2006, the collection in 2007 and 2008 decreased to its usual level, with a number of cases close to that recorded in 2005 (Figure 1).
Figure 1 : Number of cases recorded from 2005* to 2008 by the SAGIR network. * from Terrier et al., 2006
In relation with the international context of the highly pathogenic avian influenza virus (H5N1 HP) circulation, the monitoring of wild bird mortality and the screening of higly pathogenic viruses (H5 or H7) were strengthened from September 2005 onwards, relying on the SAGIR network in rural areas. The
8 Epidemiological unit of pathological cases, clinically expressed or not, occurring in the same place during a limited period of time (Toma et al., 2001).
Source : SAGIR data.. ONCFS/FNC/FDC netw
ork
Number of cases
2005 2006 2007 2008
1000
2000
3000
4000
5000
6000
n = 3475
n = 6271
n = 3043
n = 2320
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general system aimed at collecting dead birds in a good state of preservation in a context of abnormal mortality, i.e., at least five birds found dead at the same site within a radius of 500 meters, within 7 days. Following the discovery of three dead common pochards Aythya ferina in the Dombes (Ain) and the detection of the highly pathogenic avian influenza virus (H5N1 HP) on 13 February 2006, the general system was strengthened, including any dead swan observed in France and any dead anatid observed in an at‐risk wetland area, notably in this region where the wild bird mortality surveillance pressure was very high. From February to August 2006, 734 dead birds were collected in the Ain, including 470 on the Dombes ponds, showing evidence of the avian influenza epizootic in this territory (Baroux et al., 2007 ; Hars et al., 2007a ; Hars et al., 2008). Apart from this mortality episode in the Ain, the increase in SAGIR cases in 2006 compared to 2005, related to the increase in the number of birds collected by the network (Figure 1), was not associated with a mortality caused by avian influenza. On the other hand, this increase was the consequence of the strengthening of the surveillance following the vigilance appeal in the avian influenza context. This increased surveillance led to an increase in the number of notifications by observers9 and in SAGIR cases. Meanwhile, the notifications by new observers among the public were taken into account in this particular context, thereby increasing the « avian influenza » effect on the SAGIR network. The intervention of these new observers likely explains the increasing proportion of non exploitable SAGIR cases in 2006 (cf. Chapter I.1.), which reminds one that the intervention of trained people guarantees the effectiveness of the territory surveillance. This episode in 2006 is a new illustration of SAGIR’s capacity to strengthen its surveillance to face a particular health event, thanks to the mobilization of the network’s observers under the coordination of departemental technical representatives 10 (ITD) and the national team. In 2007, 949 dead birds11 were collected and analysed in France within the framework of the monitoring of avian influenza virus circulation among wild birds, which is much less than in 200612. In 2008, slightly over 350 dead birds were subjected to a search for the highly pathogenic influenza virus. This significant decrease in the number of dead birds analysed in 2007 and 2008 is the expression of lower levels of awareness of the new observers outside of a health crisis period. It is above all indicative of a lack of clarity for the network of the role officially entrusted to it. II.B Monthly distribution of cases SAGIR cases are recorded continuously throughout the year (Figure 2). The substantial increase in cases recorded in February and March 2006 reflects the public reaction to the announcement of the first avian influenza case in the Ain in February 2006 (cf. Chapter II.1.). This effect becomes less marked in April and even less marked as from May 2006.
9 Observers of the SAGIR network are mainly hunters, technicians of hunting federations and agents of the ONCFS. 10 ITD are in charge of the running of the SAGIR network in their departement. There are two of them in each departement, one from the
departemental hunting federation and the other from the ONCFS departemental service. 11 For the record, only 7 anatid specimens, 5 mute swans Cygnus olor and 2 mallards Anas plathyrhynchos, were found to be infected in Moselle in
2007 and no test on specimens collected in 2008 was found positive. 12 One should note that not all of these cases appear in the 2007 and 2008 bars in Figure 1 since all the results of the avian influenza monitoring on
wild birds found dead or sick were not entered into the SAGIR database in 2007, as well as in 2008.
11
2006
2007
2008
Figure 2 : Monthly distribution of cases in 2006, 2007, 2008. Apart from anatids, among the species well represented in the SAGIR sample, the number of roe deer Capreolus capreolus collected in February and March 2006, as well as in November and December 2006, is higher than the number collected in the same months for the years 2007 and 2008 (Figure 3). A higher number of injuries was recorded in roe deer in February and March 2006, whereas digestive system diseases (enterotoxaemia, parasitism, diarrhoea) dominated in November and December 2006. In July, August and September 2007, the three peaks were notably due to an increase in cases of polyparasitized roe deer, as well as an increase in the number of injuries in July 2007. Since 1997, many departements have reported unusual levels of dead roe deer discoveries, associated or not with a population decrease. A large number of investigations were conducted within the framework of the SAGIR network, notably in search of a specific pathogen associated with this phenomenon called MAC for mortalité anormale du chevreuil, i.e., abnormal roe deer mortality. No specific pathogen has been identified. On the other hand, autopsy reports often reported a massive parasitic infestation, associated with a marked thinness. At the individual scale, these results did not provide satisfactory answers for managers. Nevertheless, their national aggregation enabled biologists to elaborate hypotheses on this mortality phenomenon. The roe deer’s high sensitivity to its environment contributes to explain the observed or perceived mortality (Delorme et al., 2008). Nevertheless, as far as possible, the surveillance of roe deer mortality causes is essential for the early detection of diseases. The MAC issue is a good illustration of the collaborative approach between different fields (ecology, population dynamics, pathology, epidemiology,
histology, parasitology, …), essential to the understanding of some mortality events that pathology alone cannot always explain.
Source : SA
GIR data.. ONCFS/FNC/FDC netw
ork
Number of cases
December
0
100
200
300
500
400
600
January Feb. March April May June July Aug. September Oct. November
n = 1429
n = 1743
12
2006
2007
2008
2006
2007
2008
Figure 3 : Monthly distribution of roe deer cases in 2006, 2007, 2008.
Figure 4 : Monthly distribution of European brown hare cases in 2006, 2007, 2008.
With more than 1000 cases per year, the European brown hare Lepus europaeus is the most represented species in the SAGIR sample. In 2006, 2007 and 2008, their numbers increased in autumn (Figure 4). This observation is an abiding feature in the SAGIR network, and is probably related to the higher surveillance pressure during the hunting period for this species and to some pathologies frequently observed during this season (see infra). On the other hand it is difficult to interpret the other monthly and interannual differences in the number of cases. It is worth noting however that cases of pasteurellosis, coccidiosis and European brown hare syndrom (EBHS) were observed rather in November 2006 and in September and October 2007. This is indicative of a later appearance of the disease in 2006 or of a time‐lag in observation. The large number of cases in Octobre 2007 is explained by the more frequent identification of tularemia as the aetiology of death. Lastly, the higher number of cases in March 2007 is explained by an upsurge in cases of pseudotuberculosis, coccidiosis, EBHS, and a not insignificant proportion of unspecified causes of death. II.C Distribution of cases per municipality The distribution of cases per municipality (Figure 5) illustrates the nationwide coverage of the network and the dynamism of observers and SAGIR ITD, as well as of the LDAV. No data is available in a few departements. In some departements, the absence of LDAV or of an animal health activity in the departemental laboratory is a handicap for the optimal running of the SAGIR network. The web site http://carmen.carmencarto.fr/index.php?map=espece_sagir.map&service_idx=38W presents the distribution per municipality and per year of species that are well represented in SAGIR, such as the mallard Anas plathyrhyncos, roe deer, European brown hare and European rabbit Oryctolagus cuniculus.
Source : SAGIR data.. ONCFS/FNC/FDC netw
ork
Number of cases
0
Janv
50
100
150
250
200
0
50
100
150
250
200Fev
Mar
Apr
May
june
July
Aug
Sept
Oct
Nov
Dec
Jan
Fev
March
Apr
May
June
July
Aug
Sept
oct
Nov
Dec
13
Figure 5 : Distribution of cases per municipality in metropolitan France and in Martinique in 2006, 2007 and 2008.
2006*
2007
2008
Number of cases /
Number of cases /
Number of cases / municipality
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
* H5N1 HP cases are not all represented .
.
..
.
.
14
III SAMPLE DESCRIPTION
III.A Species Since 1986, SAGIR cases concern 205 species of wild birds and mammals (Appendix 1). Seven species represent 80 % of SAGIR cases with, in decreasing order of their numbers :
1. European brown hare
2. Roe deer ;
3. European rabbit;
4. Wild boar Sus scrofa ;
5. Red fox Vulpes vulpes ;
6. Mallard ;
7. Wood pigeon Columba palumbus.
Although a few species are flagship species in the SAGIR network, the species richness of the SAGIR sample is exceptional and, to our knowledge, unique in France and in Europe (Figure 6). Whereas departemental hunting federations are heedful of the monitoring of mortality in all the species whose hunting is authorized in France, the SAGIR network is also interested in other species of wild birds and mammals in France, in particular with regard to raptor intoxications for example (see infra). The common buzzard Buteo buteo thus ranks in tenth position in the list of the most represented species in SAGIR since 1986.
0
2000
4000
6000
8000
10000
12000
14000
16000
18000
20000
Lepus europaeus
Capreolus capreolus
Oryctolagus cuniculus
Sus scrofa
Vulpes vulpes
Anas platyrhuncos
Columba palumbus
Rupicapra rupicapra
Cygnus olor
Buteo buteo
Columba sp.
Perdix perdix
Cervus elaphus
Sturnus vulgaris
Streptopelia decaocto
Perdix sp.
Phasianus colchicus
Alectoris rufa
Meles m
eles
Capra ibex
Streptopelia sp.
Fulica
atra
Passer domesticus
Larus sp.
Felix lynx
Scolopax rusticola
Ardea
cinerea
Carduelis chloris
Martes foina
Turdus merula
Columba livia
Milvus milvus
Larus michahellis
Rupicapra pyrenaica
Larus ridibundus
Ovis gmelini musimon
Carduelis spinus
others
Number of cases
0
10
20
30
40
50
60
70
80
90
100
%
Figure 6 : Ranking of species in the SAGIR sample sinced 1986 according to the number of cases (Pareto diagram).
This wild bird species diversity increased in 2006 as a result of the avian influenza episode (Figure 7).
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
15
0
20
40
60
80
100
120
140
160
Figure 7 : Species richness of the SAGIR sample in 2005*, 2006, 2007 and 2008. * from Terrier et al., 2006
Within the framework of a strengthened surveillance, the SAGIR network has shown its capacity to detect in the field the mortality of specimens belonging to species other than those usually monitored by the network, notably of small size, deemed to be more difficult to observe (Figure 8). This episode is an illustration of SAGIR’s capacity to rapidly adapt to health stakes of the moment with unequalled results.
0
50
100
150
200
250
300
moineau domestique
merle noir
héron cendré
tarin des aulnes
buse variable
verdier d'Europe
étourneau sansonnet
tourterelle turque
Figure 8 : Monthly distribution of cases in 2006 for the common buzzard*, starling, grey heron, blackbird, house sparrow, siskin, collared dove and greenfinch. * For the scientific names of these species, refer to Appendix 1.
Looking at the seven first species mainly collected from 2005 to 2008 (Table I), the effect of the avian influenza episode on the species’ structure of the sample is clear : the classically observed structure of the database changes drastically in 2006 and in 2007, and the ranking is again respected in 2008.
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
2007 2008 20062005
Number of species
Jan. Fev. March April May June July Aug. Sept. Oct. Nov. Dec.
Number of cases
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Passer domesticus
Turdus merula
Ardea cinerea
Carduelis spinus
Buteo buteo
Carduelis chloris
Sturnus vulgaris
Streptopelia decaocto
16
Table I : The 7 most represented species in the database in 2005*, 2006, 2007 and 2008. * from Terrier et al., 2006
Rank 2005 2006 2007 2008
1 Europe brown hare mallard European brown hare Europe brown hare
2 Roe deer European brown hare Roe deer Roe deer
3 Red fox Roe deer mallard Wild boar
4 European rabbit pigeon sp. European rabbit European rabbit
5 Mallard Mute swan Wild boar Red fox
6 Wild boar starling Red fox Wood pigeon
7 Wood pigeon Common buzzard Mute swan Mallard
III.B Dead animals vs. sick animals From 2006 to 2008, SAGIR cases relating to animals found alive and sick represent 20 % of the total number of cases. For 50 % of these cases, the observer and/or the LDAV have described symptoms in the SAGIR form. This information is invaluable for the orientation of the post mortem diagnosis and the determination of further possible associated examinations. It was not possible in this report to compare the number of animals found alive during this period with that found in previous years.
IV MAIN INFECTIOUS AND PARASITIC DISEASES DIAGNOSED BETWEEN 2006 AND 2008
IV.A New pathogens and diseases identified between 2006 and 2008 A new pathogen or a new disease refers to a pathogen or a disease revealed for the first time in SAGIR’s history since the data centralization, either because no case had been observed until then, or because the case concerned a new wild bird or mammal species. Between 2006 and 2008, 10 new diseases or pathogens have been observed by the network (Table II).
17
Table II : List of the new pathogens and diseases identified by SAGIR between 2006 and 2008.
DISEASE SPECIES* (number of specimens, departement, date, observation)
Botulism (D) Clostridium botulinum, type D toxin
Yellow‐legged gull1 (410, 66, May 2008)
Duck viral enteritis Mute swan (1, 68, August 2008, lesions (pathological?) diagnosis)
FCO Red deer (2, 51, December 2007, presence unrelated to death)
Avian histomoniasis Mute swan (1, 26, February 2006), coot (1, 39, February 2006)
H5N1 HP1 Common buzzard (1, 01, 2006), mute swan (54, 01, 2006), common pochard (6, 01, 2006), grey heron (1, 01, 2006), grey lag goose (1, 01, 2006)
Leptospirosis Eurasian beaver (2, 39, October and November 2008)
Mycoplasma agalactiae Alpine ibex (9, 73, 2007‐2008, isolated in the lungs)
Pseudotuberculosis Red squirrel (2, 33, February 2006), Eurasian beaver2 (1, 68, May 2006), coypu (1, 26, May 2007)
Salmonellosis Salmonella mbandaka
Stock dove (4, 35, January 2007)
Haemorrhagic syndrome Hawfinch (6/1, 11/39, 2006, unidentified aetiology)
Tetrameres infestation13 Wood pigeon (1, 36, January 2008) * For the scientific names of these species, refer to Appendix 1. 1 from Hars et al., 2006 2 Identified in European beaver in 1998 and in coypu in 2002 in Indre‐et‐Loire
Among these diseases, type D botulism had not been documented so far in wildlife in France, contrary to types C and E. Duck viral enteritis or duck plague is an acute, contagious disease, sometimes chronic, due to a herpesvirus affecting ducks, geese and swans. Even though outbreaks are uncommon, it is a permanent threat for poultry flocks and ornamental birds and for the avifauna. The status of wild anatids is difficult to know but wild ducks in the Anas genus seem less prone to the clinical expression than domestic palmipedes. They could play a role in the contamination of poultry farms14. IV.B Diseases with an impact on wildlife species’ populations observed between 2006 and 2008 IV.B.1 Species whose hunting is authorized, key events
IV.B.1.1 Wood pigeon
The year 2006 was marked by a significant Newcastle disease episode in Pas‐de‐Calais, as well as a higher number of fowl pox cases. During the 2007‐2008 winter, a high wood pigeon mortality was observed and reported in many departements (Aveyron, Charente, Charente‐Maritime, Côtes d’Armor, Dordogne, Finistère, Gard, Gers, Haute‐Loire, Ille et Vilaine, Isère, Loire‐Atlantique, Marne, Mayenne, Nièvre, Orne, Savoie, Vendée, Yonne and departements of the Centre and Ile de France regions). Every winter, pigeons are found dead as a result of lesions caused by the parasite, but the phenomenon occurred on a larger scale during the 2007‐2008 winter. For example, mortality was estimated at 1 000 individuals between December 2007 and February 2008 in Vendée and at 400 (wood pigeons and doves both taken into account) in Ille et Vilaine with a mortality peak in February. Further details on the distribution of cases are described in SAGIR letters n° 161 and n° 162 (http://www.oncfs.gouv.fr/Reseau‐SAGIR‐Surveillance‐Sanitaire‐de‐la‐Faune‐Sauvage‐ru105/Consulter‐les‐lettres‐SAGIR‐ar297). IV.B.1.2 Stock dove
The month of July 2008 was marked by a significant trichomonosis episode in chicks recorded in Mayenne.
13 Tetrameres infestation is a parasitic affection due to small nematodes localized in the proventriculitis and causing emaciation (wasting, loss of
weight) and regurgitation. 14 Fot further information, you can consult http://www.avicampus.fr/PDF/PDFpathologie/Herpesvirosecanard.pdf
18
IV.B.1.3 Collared dove
Trichomonosis also affected the collared dove Streptopelia decaocto during these three years of monitoring. Cases have been reported in Aude, Dordogne, Gers, Gironde, Indre, Loiret, Nièvre and Pas‐de‐Calais. Aspergillosis marked the year 2006, with the mortality of about a hundred individuals. IV.B.1.4 European rabbit
Myxomatosis, which is endemic in France, is not often reported within the framework of the SAGIR network, despite its impact on rabbit populations. Over 3 years, 29 cases have been notified in 17 departements. The clinical features of this viral disease vary according to the virus strain and virulence. There are several forms of the disease : the first is nodular, the other is called amyxomatous. For the nodular form, the clinical picture is easy to recognize and sick or dead rabbits are often not submitted to the LDAV for analysis ; cases are not or rarely notified. As regards the attenuated nodular form and the amyxomatous form, symptoms are not as characteristic and the auto‐examination made by the observer leads to an underestimation the disease. A confirmation diagnosis performed by the LDAV is required. Between 2006 and 2008, 62 viral haemorrhagic disease (VHD) cases were observed and reported in 30 departements. Between 2006 and 2008, 52 hepatic and digestive coccidiosis, associated with diarrhoea, inflammation and intestine congestion, were observed and reported in young individuals. Lastly, in 15 % of cases, the aetiology of death could not be de determined. In 2006 in particular, the LDAV reported in the majority of cases an absence of lesions at the autopsy on analysed rabbits. IV.B.1.5 Roe deer
Cases of listeriosis, encephalitis, massive Oestrus ovis infestations and polyparasitism were recorded each year. Reported pasteurellosis cases were more numerous in 2006. The LDAV observed quite frequently tumors of the digestive and respiratory systems, concerning adults as well as young animals. IV.B.1.6 Chamois
Cases of abscess disease were observed in the chamois Rupicapra rupicapra in 2006 in Drôme and Isère, and in 2008 in Drôme and Savoie. A higher number of pasteurellosis cases was observed in 2006, as well as other respiratory diseases. IV.B.1.7 Red fox
Many cases of mange were reported in the red fox, confirming that this disease is mortal in this species. IV.B.1.8 European brown hare IV.B.1.8.1 Dominant pathological features
EBHS (European brown hare syndrom) or viral hepatitis of hares was the dominant pathology in 2006 and 2007, overtaken in 200815 by tularemia (Figure 9). For all the reasons evoked in Chapter I. Methods, the percentages mentioned here are not representative of the diseases’ prevalence in hare populations. On the other hand, they allow the identification of a trend in the occurrence of diseases in hare populations or of the interest shown in them.
15 This trend for EBHS in 2008 has to be confirmed by further data analyses.
19
0
5
10
15
20
25
30
2005 2006 2007 2008
t raumat isme
t ularémie
EBHS
pseudot uberculose
inf ect ion respirat oire
past eurellose
coccidiose
sept icémie
colibacillose
Figure 9 : Dominant pathological features in the European brown hare – Relative evolution between 2005 and 2008*. The % were calculated by dividing the number of individuals screened positive for a disease by the number of hares collected in the year. * 2008 results have to be further analysed to confirm these trends. Injuries represent a major and constant cause of European brown hare mortality. In some cases, they can be facilitated by exposure to chemical substances that modify behaviour (cf. Chapter V). Pasteurellosis occupies an important place among brown hare diseases recorded by the SAGIR network. The spatial distribution of outbreaks is shown in Figure 10.
Figure 10 : Cumulated presence and distribution per departement of pasteurellosis in the European brown hare from 2005 to 2008. Further details on pseudotuberculosis and tularemia are presented in the chapter on zoonoses (see infra). Information on EBHS is detailed below. Reproductive disorders (abortion, dystocia, genital infection) have been described for 18 cases in 2006, 11 in 2007 and 5 in 2008, without the aetiological agent being identified.
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
% of hares affected
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
1 year
2 years
3 years
4 years
20
Cases of verminous pneumonia were observed in brown hares killed by hunters in 2008. At the time of evisceration, many brown‐beige colored nodules, localized in the lungs, were observed by hunters and analysed at the LDAV. These observations are recurrent, particularly in some territories of the Tarn. The histological examination of lesions revealed the presence of nematode parasites in the bronchi and alveoli and led to the diagnosis of suppurative bronchopneumonia of verminous origin. Field observations mention animals in good condition, with no abnormal behaviour and showing no sign of impairment. At the date of edition of the present report, new information on this parasitic pathology has led to the definition of a specific study programme in several departements16. IV.B.1.8.2 Zoom on European brown hare syndrome (EBHS)
EBHS is a disease of relevance for managers and makes it worth developing the knowledge obtained by the SAGIR network. The data on macroscopic findings observed by the LDAV have been analysed in the present report. The approach used is an example of what can be carried out for the brown hare and other species and for other pathologies. Nevetheless, it was not possible in this report to develop all these analyses. We chose to develop the example of EBHS. IV.B.1.8.2.1 EBHS macroscopic findings
The analysis of macroscopic data presents a double interest : i) monitoring of the macroscopic expression of the disease as a tool for the detection of an evolution of the virus pathogenicity , ii) inventory of evocative lesions to optimize the triggering of the analysis. In a first stage, lesions were considered independently from organs to rank them according to observation frequency for EBHS cases (Figure 11). The operation enabled the isolation of lesions of low occurrence. The same approach was used with the organs (Figure 12).
0
20
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60
80
100
120
140
160
180
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HEM
ORRHAG
ECO
NGESTION
HYPERTROPH
YINFLAM
MATION
NO LESIONS
ABNORM
AL CO
LOR
NECRO
SIS
ROASTING PICTURE
TRANSUDATE/EXSUDATE
PURU
LENT SECRETION
PETECH
IAE
DEGEN
ERATION
OTH
ERS
Frequency
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40
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80
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%
Figure 11 : Frequency of lesions associated with EBHS in the European brown hare between 2006 and 2008 (Pareto diagram). The category « other» includes lesions whose observation frequency is below 1 %.
16 For further information, consult the SAGIR letters n° 165 and n° 167 (http://www.oncfs.gouv.fr/Reseau‐SAGIR‐Surveillance‐Sanitaire‐de‐la‐Faune‐Sauvage‐ru105/Consulter‐les‐lettres‐SAGIR‐ar297).
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
21
0
20
40
60
80
100
trachea
liver
lung
spleen
intestine
others organs
nose
kidney
thorax
abdomen
bronchus
stom
ach
sinus
others
Frequency
0
20
40
60
80
100
%
Figure 12 : Frequency of affected organs in EBHS cases in the European brown hare between 2006 and 2008 (Pareto diagram). The category « other» includes organs whose observation frequency is below 1 %.
In a second stage, the principal associations between the modalities « lesion » and « organ » were determined by a factorial correspondence analysis (Figure 13).
ASPECT CUIT
COLORATION ANORMALECONGESTION DEGENERESCENCE
HEMORRAGIE
HYPERTROPHIE
INFLAMMATION
NECROSE
PETECHIES
SECRETION MUCOPURULENTE
TRANSUDAT/ EXSUDAT
abdomen
bouche
broncheestomac
foie
intest in
nez
poumon
rate
rein
sinus
thorax
trachee
-1
0
1
2
3
4
-2 -1 0 1 2
- - axe F 1 ( 3 7.9 5 %) - - >
Figure 13 : Representation of the principal lesion/organ associations in EBHS cases in the European brown hare from 2006 to 2008.
Based on this analysis, the modalities having the most significant contributions in EBHS cases are the following lesion/organ associations :
- hypertrophy/spleen ; - transudate‐exsudate/abdomen ;
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
F2 axis (23,77 %)
F1 axis (37,95 %)
22
- abnormal coloration/liver ; - haemorrhage/trachea.
In other words, these associations have likely been determining to set the diagnoses. The second factorial plane retained (not represented here) showed an opposition of the association hypertrophy/spleen and necrosis‐ cooked aspect ‐ abnormal coloration/liver. This means that the spleen hypertrophy is rarely observed when the liver has a cooked aspect, an abnormal coloration or necrotic lesions. Lastly, the macroscopic findings most frequently described were revealed by a statistical classification represented in the dendrogram in Figure 14.
Figure 14 : Classification of lesion associations most frequently described in EBHS cases in the European brown hare between 2006 and 2008. The lesion/organ modalities most frequently associated in EBHS cases are haemorrhage/trachea and hypertrophy/spleen. The pair congestion/lung is aggregated to this group. The main symptoms recorded for EBHS cases were haemorrhages, mostly nasal, diarrhoea, depilation and foam at the nostrils. The other described symptoms were behaviour problems, staggers, apathy, myoclonia and jaundice. However, this information was not systematically present in SAGIR forms, it was thus not possible to analyse these symptoms using the same approach as previously. These analyses establish that no evolution of the macroscopic or symptomatological findings of EBHS in the European brown hare was detected from 2006 to 2008. IV.B.1.8.2.2 Distribution of cases per departement from 2005 to 2008
The cumulated years of EBHS presence from 2005 to 2008 enables one to identify the departements where the virus seems to be endemic (Figure 15). The departements of the south of France are particularly concerned. However, the notification of outbreaks from one year to another is not systematic. It depends on the probability of detecting the outbreak (lethal episode or not, presence of observers in the field, …) and the probability that this oubreak, once detected, is reported to the network by the observer (disease recurrence, knowledge of the disease, interest in the disease, brown hare’s demographic situation in the departement, …). Thus, the absence of EBHS case in a departement or the apparent disappearance of the disease in a departement does not necessarily mean that it is not or no longer present. All the data should thus be interpreted with caution.
Dissimilarity
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
23
Figure 15 : Cumulated presence and distripution per departement of EBHS in the European brown hare from 2005 to 2008. Spread of the EBHS virus in brown hare populations – Retrospective analysis. by Jean‐Sébastien GUITTON, ONCFS, Direction of studies and research
During the last quarter of the year 2004, the SAGIR network observed a higher number of EBHS cases than in previous years in several departements of the south‐east of France. The spatio‐temporal description of this epizootic enabled the ONCFS to put forward and test several hypotheses concerning various epidemiological aspects of this still little‐known disease. The hypothesis that the increase in the number of cases in 2004 could be related to the emergence of a new virus genotype was first tested. The sequencing performed by the AFSSA supported this hypothesis and showed a replacement of ancient viral genotypes by the novel ones over the 10 previous years. A modelling work was then initiated to investigate whether it is necessary to assume that new genotypes have a selective
advantage (in the form of only partial cross‐immunity with the ancient genotypes) to explain the observed dynamics. The first results do not favour this hypothesis : the low exposure of brown hare populations to EBHS in 2003 could have played a more determining role. Some groups of municipalities appeared to have been little or not affected by the disease in 2004. A serological study carried out in 2005 aimed, but unsuccessfully, at showing that the EBHS virus might have little circulated in these populations, for example due to a relative spatial isolation. Lastly, the spatial spread of the epizootics of 2004 described using the SAGIR network data at the scale of several departements was irregular. A work under way aims at showing that this variation is related to a landscape structure (rivers, forests, relief) which influences contacts between brown hares and hence the spread of the virus. These works are in progress or nearing publication.
IV.B.2 Protected species, key events
IV.B.2.1 Alpine ibex
During the 2007‐2008 winter, about ten dead Alpine ibex were transported to the departemental veterinary laboratory of Savoie (LDAV73). This number seemed large compared to previous years, particularly as they were adults, and led to the assumption that the mortality was likely to be abnormal (see SAGIR Letter17 n° 161). Meanwhile, the Vanoise National Park reported an unusually high mortality in some populations cores, in particular in the Champagny en Vanoise and Villarodin le Bourget territories. The
17 SAGIR Letters available at http://www.oncfs.gouv.fr/Reseau‐SAGIR‐Surveillance‐Sanitaire‐de‐la‐Faune‐Sauvage‐ru105/Consulter‐les‐lettres‐
SAGIR‐ar297.
1 year
2 years
3 years
4 years
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
24
performed analyses enabled the identification of the two main diseases found in the species, i.e., keratoconjonctivitis and pneumonia. No new cause of death was thus identified. Within the framework of the detailed analyses performed by the LDAV73, along with the ANSES laboratory in Lyon, the bacteriology revealed for the first time the presence of the Mycoplasma agalactiae bacteria in the lungs of some ibex suffering from pneumonia. This observation raises questions concerning the bacteria’s role in the development of pneumonia in Alpine ibex and its potential impact on population dynamics. A pluridisciplinary collaborative study is currently underway to contribute to answering these questions.
IV.B.2.2 Brent goose
Aspergillosis cases were observed in the brent goose Branta bernicla in the Manche in 2006. IV.B.2.3 Red squirrel
The causes of death of red squirrel specimens collected by the SAGIR network have an infectious origin, with the observation of pseudotuberculosis and respiratory infection, the aetiological agent of which was unidentified. IV.B.2.4 Gulls
In early March 2008, the Norman Ornithological Group reported to the SAGIR network a grouped gull mortality on Tatihou Island in the Manche (see SAGIR Letter11 n° 161). Slightly over 60 individuals, mostly herring gulls Larus argentatus, but also lesser black‐backed gulls Larus fuscus and great black‐backed gulls Larus marinus, were found dead or dying on this small territory. In a first stage, 19 post‐mortem examinations were performed by the Manche departemental veterinary laboratory. Based on the macroscopic findings and the sudden occurrence of the phenomenon, the first hypotheses turned towards toxicology, in particular an intoxication by anticoagulants. The toxicology laboratory of the veterinary VetAgro Sup Campus of Lyon analysed all the submitted samples and searched for most of the molecules on the market. The analyses did not enable the detection of the anticoagulants searched for and thus invalidated our initial hypothesis. Meanwhile, gulls were still found dead or dying, only on the island territory, the number of victims reaching about a hundred. In order to target the further investigations, 2 dying gulls and 3 new dead ones were analysed again and tissue samples were submitted to the histology laboratory Vet Diagnostics (www.vetdiagnostics.fr). Any infectious hypothesis was hence discarded and another toxic hypothesis was put forward in relation with the observed behaviour of the sick animals. Chloralose was identified on one sample. In May 2008, 300 yellow‐legged gulls were found dead or dying on La Corrège island in the middle of the Salses‐Leucate pond in Pyrénées‐Orientales. The analyses performed within the framework of the network confirmed type D botulism. The opportunistic and necrophagous feeding behaviour of this species contributed to maintain the phenomenon. State services, in particular the prefecture, veterinary services and health affairs, could use this information to reassure the populations, although the initial terms used in their communication (« risk for humans », « transmissible germ », « precaution principle », …) had at first needlessly alerted them. For this reason, the basic language used during botulism episodes needs to be precise (see SAGIR Letter11 n° 162). IV.B.2.5 Black‐headed gull
Salmonella typhimurium was identified in several cases of black‐headed gull Chroicocephalus ridibundus mortality in 2006 in the Somme and in 2008 in Indre‐et‐Loire. Visceral gout was diagnosed in 21 gulls in Pas‐de‐Calais (see SAGIR Letter11 n° 158). IV.B.2.6 Siskin
Salmonella typhimurium and group B Salmonella were identified in several siskin Carduelis spinus specimens found dead in 2006 and 2008 in several departements (Alpes de Haute‐Provence, Creuse, Drôme, Isère, Loire, Savoie, Tarn).
25
IV.B.2.7 Greenfinch
Salmonella typhimurium and group B Salmonella were identified in several greenfinch Carduelis chloris specimens found dead in 2006 and 2008 in several departements (Cantal, Corrèze, Côte d’Armor, Creuse, Drôme, Gers, Jura, Tarn). A mortality episode due to trichomonosis was recorded in greenfinch during the 2007‐2008 winter. IV.C Zoonotic pathogens identified between 2006 and 2008 IV.C.1 Tularemia
Compared to the 2005 situation, the number of departements where a least one tularemia case in the European brown hare was detected by SAGIR was higher in 2008 (Figure 16). However, given the SAGIR protocol, it is impossible to specify whether it was due to a true progression of the disease, an increase in the observation pressure, an improvement in the disease detection techniques or a more systematic search for the disease even on animals that did not show any evocative sign.
Figure 16 : Cumulated presence and distribution per departement of tularemia in the European brown hare from 2005 to 2008. The 2007‐2008 winter was marked by an important increase, during a limited period of time, of tularemia cases in the European brown hare and in humans. The increase in human cases was not accompanied by an increase of contact with the brown hare, suggesting one or several common sources of contamination for these 2 species (Mailles et al., 2010). IV.C.2 Swine erysipelas
Swine erysipelas was detected in the wild boar in April 2007 in the Loire, in the roe deer in June 2007 in the Alpes de Haute‐Provence and the Jura and in the European brown hare in November 2008 in Ardèche. IV.C.3 Leptospirosis
Leptospirosis was diagnosed in the Eurasian beaver in autumn 2008 in the Jura. IV.C.4 Pseudotuberculosis
Compared to the 2005 situation, the number of departements where at least one case of pseudotuberculosis in the European brown hare was detected by SAGIR was lower in 2008 (Figure 17).
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
1 year
2 years
3 years
4 years
26
However, one should bear in mind that the same caution as described above for tularemia is required in the interpretation.
Figure 17 : Cumulated presence and distribution per departement of pseudotuberculosis in the European brown hare from 2005 to 2008. IV.D Pathogens shared with domestic animals identified between 2006 and 2008 The SAGIR network analyses identified several pathogens or diseases shared with domestic animals. Between 2006 and 2008, waterfowl botulism, trichomonosis, Mycobacterium avium tuberculosis, fowl cholera and pox, Newcastle disease, classical swine fever in wild boar, bluetongue in the red deer, Brucella suis biovar 2 brucellosis in the European brown hare and the wild boar, salmonellosis and pasteurellosis in various wild bird and mammal species, babesiasis in the Pyrenean chamois, listeriosis in the roe deer , were identified.
V INTOXICATIONS IDENTIFIED BY SAGIR FROM 2006 TO 2008
V.A Identified causative agents of intoxications Between 2006 and 2008, the number of cases for which the cause of death was an intoxication reached 359 individuals. These intoxications were due to one or several molecules, listed in Table III. In this table, an individual is mentioned as many times as toxic agents have been identified in its tissues, which explains the total number 411. Intoxications concerned a similar proportion of birds as mammals. Birds were predominantly intoxicated by chloralose, cholinesterase inhibitors and imidaclopride. Mammals were mostly intoxicated by anticoagulants and cholinesterase inhibitors.
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
1 year
2 years
3 years
4 years
27
Table III : Toxicants quantified per species* and per year from 2006 to 2008. * for species’ scientific names, refer to Appendix 1.
Name of the agent Name of the species 2006 2007 2008 Total
ALDICARBE Red deer 1 1 Rook 1 1 Beech marten 1 1 Europe brown hare 1 1 Wild boar 2 2
ALDRINE Peregrine falcon 4 4 Red fox 1 1
Common buzzard 2 2 Roe deer 2 2 Storck sp. 2 2 Rook 4 4 European rabbit 2 2 European brown hare 11 1 12 Red fox 3 3 6
ANTICOAGULANTS (unidentified molecules)
Wild boar 3 4 7
BROMADIOLONE Common buzzard 2 2 Roe deer 1 2 3 Barn owl 1 1 Comon kestrel 1 1 European rabbit 2 2 European brown hare 4 5 9 Red kite 1 1 Red‐legged partridge 1 1 Red fox 3 9 5 17 Wild boar 4 12 16 32 Collared dove 1 1
CARBOFURAN Common buzzard 7 3 10 Roe deer 1 1 2 Raccoon‐dog 1 1 Mallard 1 1 Starling 2 2 Beech marten 1 1 European hedgehog 2 2 European rabbit 1 1 Red kite 1 1 Black‐headed gull 1 1 Roose sp. 1 1 Red‐legged partridge 1 1 Red fox 5 3 1 9 European robin 1 1 Wild boar 2 2
CHLORALOSE Golden eagle 1 1 Common buzzard 1 1 2 Duck sp. 1 1 Roe deer 2 2 Mallard 7 9 9 25 Crow sp. 1 1 Mute swan 1 1 Pheasant sp. 1 1 2 Coot 1 1 Gull sp. 4 4 Eurasian eagle‐owl 1 1 Grey heron 1 1 Red kite 1 1 House sparrow 3 2 5 Black‐headed gull 1 1 Grey partridge 1 2 1 4 Common wood pigeon 1 2 1 4 Pigeon sp. 4 4 9 17
28
coypu 1 1 Red fox 1 1 Wild boar 3 6 9 Turtle dove 1 1 Collared dove 7 2 9
CHLORMEPHOS Common wood pigeon 1 1
CHLOROPHACINONE Red deer 1 1 Roe deer 2 1 3 Common crane 2 2 Grey heron 1 1 European rabbit 2 2 European brown hare 5 7 2 14 Rock pigeon 2 2 Wild boar 1 1 2
SODIUM CHLORIDE Chamois 1 1
COPPER Mute swan 1 1 Griffon vulture 1 1 2
DICHLORODIPHENYLDICHLOROETHANE Wild boar 1 1
DICHLORVOS European brown hare 1 1 Wild boar 4 4
DIFENACOUM European rabbit 1 1 Red fox 1 1 Wild boar 2 1 3
FIPRONIL Pheasant sp. 1 1
FLOCOUMAFENE Eurasian beaver 1 1
FLUORENE Wild boar 1 1
HEPTACHLOR Common buzzard 1 1 Peregrine falcon 1 1 Grey partridge 1 1 Red fox 1 1
IMIDACLOPRIDE Grey partridge 4 4 Partridge sp. 6 6 Stock dove 4 4 Pigeon sp. 1 4 2 7
CHOLINESTERASE INHIBITORS Golden eagle 1 1 (unidentified molecules) Common buzzard 2 2 Roe deer 1 1 2 Mallard 1 7 8 Crow sp. 1 1 Common genet 1 1 Eurasian eagle‐owl 1 1 European brown hare 2 1 1 4 Black kite 5 5 Red‐legged partridge 3 3 Pigeon sp. 1 1 Coypu 1 1 Red fox 3 1 4 Wild boar 4 4 Turtle dove 1 1
LINDANE Eurasian badger 1 1 Common buzzard 2 2 Peregrine falcon 5 5 European rabbit 1 1 European brown hare 1 1 Red fox 4 1 5 Wild boar 1 1 Griffon vulture 1 1
METALDEHYDE Mallard 11 11 Red fox 1 1 Wild boar 1 1
METHIDATION European brown hare 1 1
MEVINPHOS Wild boar 1 1
NAPHTALENE Wild boar 1 1
ORGANOCHLORINES Golden eagle 1 1 Wild boar 1 1
29
PARATHION Rook 1 1
PCB Peregrine falcon 5 2 7
LEAD Mallard 1 1 Mute swan 2 2 Grey lag goose 1 1 Griffon vulture 1 1
PYRENE Wild boar 1 1
STRYCHNINE Red fox 1 1
TERBUPHOS Wild boar 1 1
TRIAZOPHOS Roe deer 1 1
Total : 122 146 143 411
V.A.1 Intoxications by anticoagulants from 2006 to 2008
Intoxications by anticoagulants recorded from 2006 to 2008 were due to bromadiolone, which is the molecule most often identified, to chlorofacinone, difenacoum and flocoumafene. This type of intoxication was identified in 18 species and more often in the wild boar, the red fox, the European brown hare and the roe deer (Table IV). The wild boar’s exposure was predominantly caused by malevolent actions, with a particularly lethal episode in the Meuse in 2008 (Figure 18). The use of rodenticides in agriculture was the cause of intoxication cases in the European brown hare. As regards raptors and other predators, secondary intoxication by the consumption of contaminated prey appears to be the main route of exposure, either related to a malevolent action or following the use of rodenticides in agriculture, particularly in Franche‐Comté (Figure 18). Rodenticide anticoagulants were a significant cause of wild bird and mammal mortality (Berny et al., 1997 ; Berny et Gaillet, 2008 ; Guitart et al., 2010). Table IV : Number of anticoagulant intoxication cases per species from 2006 to 2008.
Common buzzard 6
Eurasian beaver 1
Red deer 1
Roe deer 10
Barn owl 1
storck sp. 4
Rook 8
Common kestrel 1
Common crane 2
Grey heron 1
European rabbit 9
European brown hare 47
Red kite 1
Red‐legged partridge 1
Rock pigeon 2
Red fox 30
Wild boar 51
Collared dove 1
30
0
2
4
6
8
10
12
f locoumafene
difenacoum
chlorophacinone
bromadiolone
ant icoagulant indéterminé
Figure 18 : Departements concerned by anticoagulant intoxications from 2006 to 2008. V.A.2 Intoxications by cholinesterase inhibitors from 2006 to 2008
Cholinesterase inhibitor intoxications recorded from 2006 to 2008 were due to aldicarbe, carbofuran, dichlorvos, mevinphos, parathion and terbuphos. This type of intoxication has been identified in 27 species, and more often in the wild boar, the red fox, the common buzzard and the mallard (Table V). Table V : Number of cholinesterase inhibitor intoxication cases per species from 2006 to 2008.
Golden eagle 1
Common buzzard 12
Red deer 1
Roe deer 4
Raccoon‐dog 1
Mallard 9
Rook 2
Carrion crow 1
Starling 2
Beech marten 2
Common genet 1
Eurasian eagle‐owl 1
European hedgehog 2
European rabbit 1
European brown hare 6
Black kite 5
Red kite 1
Black‐headed gull 1
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Number of cases
2006 2007 2008
Doubs
Eure
Haute‐Loire
Indre‐et‐Loire
Jura
Loire‐Atlantique
Lot
Manche
Marne
Meu
se
Oise
Somme
Tarn
Aveyron
Deu
x‐Sèvres
Doubs
Eure
Gard
Haute‐Loire
Hérault
Isère
Jura Lot
Meu
se
Oise
Sarthe
Savoie
Somme
Vienne
Yonne
Alpes de Haute‐Provence
Aube
Doubs
Haute‐Loire
Haute‐Saône
Jura
Marne
Meu
se
Seine‐Maritim
e
Vienne
31
Goose sp. 1
Grey partridge 1
Red‐legged partridge 3
pigeon sp. 1
Coypu 1
Red fox 13
European robin 1
Wild boar 14
Turtle dove 1 V.A.3 Intoxications by organochlorines from 2006 to 2008
Organochlorine intoxications recorded from 2006 to 2008 were due to aldrine, PCB and lindane. This type of intoxication has been identified in 8 species, including the peregrine falcon (Table VI). Following ornithologists’ observations relating to a problem of hatchability of peregrine falcon eggs in the Jura in April 2006 and 2008, toxicological analyses were performed. They revealed a contamination of eggs by PCB (Monneret, 2008). Table VI : Number of organochlorine intoxication cases per species from 2006 to 2008.
Golden eagle 1
Eurasian badger 1
Common buzzard 2
Peregrine falcon 16
European rabbit 1
European brown hare 1
Red fox 6
Wild boar 2
Griffon vulture 1
V.A.4 Intoxications by chloralose from 2006 to 2008
Chloralose intoxication was identified in 15 species in 2006 (Table VII). The intoxication was identified in a single mammal species, the roe deer. In case of unexplained nervous disorders in a roe deer, intoxication by chloralose is one of the diagnostic hypotheses. To confirm this hypothesis, the toxicological analysis is performed on the rumen contents. Table VII : Number of individuals per species, intoxicated by chloralose in 2006.
Comon buzzard 1
Roe deer 2
Mallard 23
Rook 3
Crow sp. 4
Mute swan 1
pheasant sp. 1
Eurasian eagle‐owl 1
Grey heron 1
House sparrow 8
Black‐headed gull 9
Grey partridge 1
Common wood pigeon 1
pigeon sp. 10
Collared dove 10
32
In 2006, the proportion of chloralose intoxications in wild birds appears to have increased in relation to other causes of intoxication (Figure 19).
0%
20%
40%
60%
80%
100%
autres toxiques
chloralose
Figure 19 : Proportion of chloralose intoxications among confirmed intoxication cases in wild birds (from Berny, 2007).
The weekly distributions of chloralose intoxication cases and highly pathogenic avian influenza cases in Europe follow the same trends. There is a statistically significant co‐movement18 of the two series, with a time‐lag of two weeks between chloralose cases in France and avian influenza cases in Europe (Figure 20). This time‐lag may correspond to the time elapsed until intoxication and discovery of animals following a malevolent use of chloralose. This positive association is probably the consequence of the fear generated by the avian influenza health crisis, resulting in the poisoning of birds, considered as a health hazard.
18 Co‐movement test : test of the synchronous variation between two variables monitored at the same dates.
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
2006 20052004200320022001 2000
33
0
1
2
3
4
5
6
7
8
9
10
s45/2005
s46/2005
s47/2005
s48/2005
s49/2005
s50/2005
s51/2005
s52/2005
s01/2006
s02/2006
s03/2006
s04/2006
s05/2006
s06/2006
s07/2006
s08/2006
s09/2006
s10/2006
s11/2006
s12/2006
s13/2006
s14/2006
s15/2006
s16/2006
s17/2006
s18/2006
s19/2006
s20/2006
s21/2006
chloralose
IAHP
Figure 20 : Weekly distribution of chloralose intoxication cases in wild birds in France and highly pathogenic avian influenza cases in Europe in 2006 (from Berny, 2007). V.A.5 Intoxications by toxicant associations from 2006 to 2008
Several toxic compounds have sometimes been identified in the same specimen (Table VIII). The majority of such intoxications are due to malevolent actions but they can also be the result of an agricultural practice. Table VIII : Toxicant associations and species concerned.
Toxicant associations Species (number of cases)
chloralose and cholinesterase inhibitor Turtle dove (1), black‐headed gull (1) , Eurasian eagle‐owl (1), mallard (7), coypu (1), common buzzard (1), pigeon sp. (1), golden eagle (1)
anticoagulants and cholinesterase inhibitor Red fox (1), European brown hare (1), roe deer (1), wild boar (1)
DDD and Lindane Wild boar (1)
heptachlor and lindane Red fox (1), common buzzard (1)
heptachlor, lindane, PCB and Aldrine Peregrine falcon (5)
benfuracarbe and dichlorvos Wild boar (2)
methidathion and anticoagulant European brown hare (1)
lindane and metaldehyde Red fox (1)
chlormephos and chloralose Common wood pigeon (1)
heptachlor and chlorase Grey partridge (1)
cadmium and lead Mute swan (1)
cadmium, copper and lead Griffon vulture (1), mute swan (1)
cadmium, copper and lindane Griffon vulture (1)
dichlorvos and bromadiolone Wild boar (1)
aldrine and chloralose Red fox (1)
naphtalene, fluorene and pyrene Wild boar (1)
carbofuran and aldicarbe pigeon sp. (1), beech marten (1)
chloralose and difenacoum Wild boar (1)
Organochlorine and cholinesterase inhibitor Wild boar (1)
Number of cases
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
34
V.B Distribution per departement of intoxication cases from 2006 to 2008 A very large number of departements have reported intoxication cases during these three years (Figure 21). The Doubs recorded a vast majority of intoxication cases due to the use of anticoagulants in agriculture and their non‐intentional effects on wild birds and mammals, the Jura and Eure to a lesser extent. In Pas‐de‐Calais, the majority of intoxications were caused by chloralose, with an imidaclopride intoxication episode in stock doves in 2007, as well as in grey partridges in the Eure the same year. Chloralose intoxication cases were also very common in the Territoire de Belfort and the Lot. The Sarthe observed a grouped mortality episode in mallards due to metaldehyde in 2008. In the Gard, an unidentified cholinesterase inhibitor caused the grouped mortality of red‐legged partridges in 2007. Intentional intoxications targeting the wild boar contributed to the cases recorded in Haute‐Loire, Meuse and Savoie.
0
5
10
15
20
25
30
35
40
2008
2007
2006
Figure 21 : Number of intoxication cases per departement from 2006 to 2008 identified by SAGIR. V.C Intentional intoxication In a number of cases, the case histories19, recorded in the SAGIR form (Appendix 2) and accompanying the collected specimen, are sufficiently detailed to allow the analysis of intoxication circumstances. Besides the major interest of case histories for the diagnosis and identification and for the analysis of substances that are likely to have been the cause of death, they enable one to discriminate, in wild bird and mammal intoxications, the portion of intentional actions, of the misuse of commercial preparations, and agricultural practices in accordance with approved use. Between 2006 and 2008, 107 poisoning intentions were recorded, including 53 established intoxications. Intentional intoxication cases concerned 16 species (Table IX). There were as many intoxicated mammals as birds and a third of affected animals were carnivores. The main species affected among the analysed dead
19 The case histories refer to all the information collected by the observer and specifying circumstances of the discovery, the animal’s environment,
the animal, the context of the discovery, …
Number of cases
Source : Données SA
GIR. R
éseau
ONCFS/FNC/FDC
Loire‐Atlantique
Manche
Tarn
Aveyron
Eure
Gard
Hérault
Isère
Lot
Oise
Sarthe
Savoie
Somme
Yonne
Alpes de Haute‐Provence
Doubs
Haute‐Saône
Jura
Marne
Meu
se
Seine‐Maritim
e
Vienne
Aisne
Alpes‐M
aritim
esArdèche
Aube
Bouches‐du‐Rhône
Calvados
Cantal
Charen
teCôte d’Or
Dordogne
Finistère
Gers
Gironde
Ille‐et‐Vilaine
Indre
Indre‐et‐Loire
Landes
Loire
Haute‐Loire
Lot‐et‐Garonne
Maine‐et‐Loire
Haute‐M
arne
Meu
rthe‐et‐M
oselle
Morbihan
Nord
Orne
Pas‐de‐Calais
Pyrén
ées‐Atlantiques
Pyrén
ées‐Orien
tales
Bas‐Rhin
Haut‐Rhin
Rhône
Saône‐et‐Loire
Haute‐Savoie
Seine‐et‐M
arne
Deu
x‐Sèvres
Vaucluse
Ven
dée
Vosges
Territoire de Belfort
Essonne
35
bodies were the mallard and the red fox, followed by the common buzzard and the wild boar. For some of them, a bait found in the vicinity accompanied the dead body. Among the collected baits, 39 were targeted at carnivores (carcasses stuffed with toxic substances, croquettes, eggs, viscera, meat filled with toxic substances), 25 at granivores (maize, wheat, sunflower filled with toxic substances), 6 at herbivores (cabbage, beetroot, carrots, apples filled with toxic substances) and 2 at several feeding categories (sardines and maize). Table IX : Number of individuals per species intoxicated intentionally from 2006 to 2008.
Common buzzard 8
Red deer 2
Mallard 13
Rook 3
Starling 2
Beech martin 3
Eurasian hedgehog 1
European rabbit 5
European brown hare 3
Red kite 2
Goose sp. 1
Chaffinch 3
Coypu 2
Red fox 12
Wild boar 6
Turtle dove 2
The main toxicants used were cholinesterase inhibitors, in particular carbofuran, chloralose and anticoagulants. The low representation of toxicants such as strychnine and metaldehyde compared to actions of the same type concerning domestic carnivores has been noted (Berny, pers. com.).
VI EXAMPLES OF COMPLEMENTARY SAGIR EPIDEMIOLOGICAL MONITORING PROGRAMMES
SAGIR is a health watch network. It provides a general surveillance over the long term since over fourty years 20. It is an effective system for the detection of health events. But it does not have the capacity to monitor a disease in space and time, given its protocol. SAGIR is thus articulated with other surveillance systems to carry out an effective monitoring. The examples of the monitoring of avian influenza, West‐Nile virus, bovine tuberculosis, classical swine fever of the wild boar and avian schistosoma are presented here to illustrate this complementarity. VI.A Monitoring of influenza viruses in the wild avifauna by Jean HARS, ONCFS, department of studies and research
Wild waterfowl (mainly the orders Anseriformes and Charadriiformes) are considered as the main reservoirs (asymptomatic carriers) of LP (low pathogenicity) AI (avian influenza) viruses. Since 2003, following the occurrence of two very severe avian influenza epizootics among poultry in Europe (in Italy and then in the Netherlands), and a growing awareness of the risk that a wild reservoir could pose for domestic birds, a national programme for the active surveillance of influenza viruses in the wild avifauna was entrusted to the ONCFS by the Ministry of Agriculture. The latter is conducted every year on cloacal swabs from a sample of 1000 to 2000 water birds either captured or killed by hunters (dabbling ducks, diving ducks, gulls, waders…) on several reference sites (Loire Estuary, Dombes, Camargue, Lake Der, shores of Nord Pas de Calais….), as well as from invasive species that are subjected to 20 its name was created by Claude MALLET in 1986 but the health surveillance carried out by hunting federations and the ONCFS exists since 1968
for the surveillance of the effects of phytopharmaceutical products on the mortality of small game and since 1972 for the survey on small game mortality.
36
management plans (African sacred ibis Threskiornis aethiopicus, ruddy duck Oxyura jamaicensis, Canada goose Branta canadensis). This programme is under the scientific responsibility of the national reference laboratory of ANSES at Ploufragan. The monitoring of influenza viruses covers all the subtypes known to date, although it is targeted in priority on the virus subtypes containing hemagglutinin H5 and H7, which are subjected to international regulations owing to their propensity to evolve into highly pathogenic viruses (HP) in poultry, responsible for very severe epizootics such as those mentioned above. Between 2003 and 2008, on 5736 birds that were tested in active surveillance, more than 200 LP viral strains were detected, including 18 H5 strains and 2 H7 strains, mainly on dabbling ducks (mallard, garganey Anas querquedula, teal Anas crecca, shoveler Anas clypeata). On the other hand, no highly pathogenic strain has ever been isolated in France on birds that were in apparent good health. Since September 2005, date at which there began to be fears of an introduction into Europe of the Asian lineage H5N1 HP virus (known to cause mortalities in wild birds) by migratory birds, the monitoring has been strengthened in France with a virus search on dead birds found in the field. This monitoring relied in rural areas on the SAGIR network. The H5N1HP virus was detected for the first time on 13 February 2006 on 3 dead common pochards collected on a pond of the Dombes (Ain). A single turkey farm in the vicinity was contaminated a few days later. In 2006, among 3426 dead birds analysed in France, including 734 in the Ain departement, only 65 birds were tested positive (Baroux et al., 2007), including 64 in the Ain. 82 % of infected birds were mute swans. The epidemiological analysis of this epizootic suggests that the virus was introduced into the Dombes by common pochards or other migratory ducks following a cold spell in Eastern Europe, and that the swan subsequently served as an excellent sentinel species for (signaling?) the infection, since it is very sensitive to the infection and very visible on the ponds. Wild bird mortalities remained in the end very moderate and the epizootics was on the whole restricted to the Dombes (Hars et al., 2007a ; Hars et al., 2008a). A very similar scenario was observed during the summer 2007 when seven cases of H5N1HP virus infections (5 mute swans and 2 mallards) were detected on the ponds of Moselle (Lindre Estate), some time after common pochards had assembled there for moulting. Mortality thus remained very low and this outbreak did not spread outside of the primary infection zone. These observations suggest that the Asian lineage H5N1HP virus is not very lethal and/or not very contagious in wild birds and that prevention and control measures implemented in poultry farms have been effective. Since August 2007, no highly pathogenic virus has been isolated in wild birds in France. VI.B Monitoring of the West‐Nile virus in the wild avifauna by Jean HARS, ONCFS, department of studies and research In relation with the 76 equine cases observed in 2000, the ONCFS has conducted an epidemiological survey which enabled the assessment of the West‐Nile (WN) virus circulation intensity among wild birds. The aim of this surveillance in the avifauna was to allow the early detection of the presence of the WN virus to enable the implementation of risk control measures for horses and humans. This surveillance was based on two operations :
- the detection, by the SAGIR network, of wild bird mortality ;
- the monthly serological monitoring, during the summer, of sentinel birds distributed in about thirty sites along the Mediterranean coast.
Between 2000 and 2007, no abnormal mortality due to the WN virus has ever been observed in the French avifauna by the SAGIR network. The virus was isolated only twice in 2004 in Camargue, on a house sparrow and a magpie. As regards the serological monitoring results, between 2000 and 2007, except for rare cases of serological conversion observed in 2001 and 2002 in sentinel birds, showing a low‐level viral circulation, several serological conversions were observed in Camargue in 2004 shortly before the occurrence of about thirty equine cases. This showed the interest of using sentinel birds as an early warning system. Since 2008, the WN virus surveillance in wild birds is based on the surveillance of mortality and the search for the virus on dead birds in Mediterranean departements.
37
VI.C SAGIR, an essential link for the monitoring of classical swine fever by Sophie Rossi, ONCFS, department of studies and research
When the classical swine fever (CSF) virus emerges in a naïve wild boar population, it causes a high mortality, predominantly among young animals, and this infection can be detected in the field by the discovery of dead bodies. This was notably the case in France in January 1992 (former outbeak of Vosges du Nord), in April 2002 (Eifel‐Luxembourg‐Thionville outbreak) and April 2003 (new epizootic wave in Vosges du Nord). Still more recently, in the beginning of 2009, the discovery of dead wild boars that were infected by CSF has revealed the re‐emergence of the infection in Palatinate (Rhineland‐Palatinate, Germany) and the spread of the Eifel outbreak to the right bank of the Rhine (North Rhine‐Westphalia, Germany). More generally, the recent report by the EFSA (2008) shows the interest of mortality surveillance, such as that conducted by SAGIR, with respect to the detection of CSF in the wild boar in most of the wild outbreaks recorded in Europe. It is particularly interesting to note that, during the epizootic phase, the discovery of infected dead bodies is almost concomitant with the discovery of CSF cases by active surveillance, although the latter uses a hunting sample which is much larger than the sample of dead animals. The monitoring carried out in 2005 in the infected zone of Vosges du Nord thus used a sample of 7 256 wild boars shot by hunters, of which 23 were virology positive, and 63 wild boars found dead or shot sick, among which 5 were CSF positive. In other words, the mortality surveillance can be considered as an excellent mode of detection of CSF in the epizootic phase, both technically and economically speaking. Whereas the relevance of mortality surveillance is crucial in the first stages of a wild CSF outbreak, it becomes less obvious after the peak of infection. The experience gained in France is interesting to illustrate this established fact since the CSF diagnosis on dead bodies has been systematized since 2002 in infected zones and those under surveillance, at the joint instigation of the ONCFS department of studies and research, the veterinary services and the Ministry of Agriculture, local and national actors of the SAGIR network and the national reference laboratory of ANSES for CSF (Chenoufi et al., 2006). This systematized monitoring has shown that whereas CSF cases are detected during the epizootic phase, no CSF infected dead body is on the other hand detected one year after the emergence of the outbreak (Hars et al., 2007). This result is explained by the fact that the CSF virus is able to persist at very low incidence levels. The lower number of deaths caused by CSF during these so‐called enzootic phases makes the detection of the infection by mortality surveillance unlikely, at least until a potential re‐emergence of the oubreak in a more visible form (new epizootic peak and hence peak in amount of dead bodies). For this reason, the CSF surveillance in infected zones uses essentially an active disease surveillance carried out on hunter‐killed animals. As an example, the monitoring conducted in the infected zone of Vosges du nord in 2007 used a sample of 9 910 hunter‐killed wild boars, a single one of which was virology positive, and 91 wild boars found dead or shot sick, all CSF negative. It can be noted that, contrary to what was supposed in the 1990s (Crucières et al., 1998), the non‐detection of dead bodies is not related to a reduced virulence of the virus. The studies conducted by the ONCFS on wild boars monitored using capture‐mark‐recapture (2005‐2007) have shown that CSF results in a high mortality among infected individuals aged less than 6 months, including after the infection peak (Hars et al., 2007b ; Rossi et al., in prep.). But this mortality is hard to detect in the field, probably owing to the difficulty of detecting small sized carcasses concealed by the vegetation cover and quickly consumed by scavengers in the summer. By way of example, the dead body detection probability was estimated at less than 2 % in the Petite Pierre national hunting and wildlife reserve, despite the continuous monitoring carried out by agents of the ONCFS and the National Forest Agency (Rossi et al., in prep.). This undetected mortality is often translated into a decrease in the hunting bag, particularly for the young wild boars, in the autumn (Rossi et al., 2005), often mistakenly interpreted as a reproduction problem by hunting managers (Rossi et al., in prep.).
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VI.D Monitoring of tuberculosis in wild animals in France by Jean HARS, ONCFS, department of studies and research
Bovine tuberculosis is an infectious and contagious disease, widespread in the animal kingdom, due to Mycobacterium bovis. Owing to the damage that it caused in livestock farms and its zoonotic properties, an eradication programme for this disease, which is listed as a regulated disease under the rural code, has been successfully implemented in French cattle stocks since 1965. In 2000, France was officially recognized as being free from bovine tuberculosis and, until this date, M. bovis had never been isolated in a free‐ranging wild animal. In 2001, the disease was discovered for the first time in France, within the SAGIR framework, on red deer killed by hunters in the Brotonne forest in Seine‐Maritime. M. bovis was subsequently isolated on wild ungulates in Côte d’Or and Haute‐Corse as from 2003, and in Pyrénées‐Atlantiques in 2005 and 2006. The evolution of the situation in these various departements is described below.
In the Brotonne forest (Seine‐Maritime and Eure) During the 2001‐2002 hunting season, the epidemiological survey conducted in the Brotonne forest revealed very high apparent infection prevalences, 14 % in the red deer and 28 % in the wild boar (Hars et al., 2004). Despite the implementation by veterinary services of a control plan (reduction of wild ungulate densities, destruction of the viscera of hunter‐killed animals, ban on supplemental feeding at fixed points, …), the phenomenon worsened. Indeed, in 2005‐2006, the apparent prevalence reached 24 % in the red deer and over 30 % in the wild boar (Zanella et al., 2008), with an aggravation of the macroscopic fundings. The same bacterial strain, SB 0134, was isolated in wild ungulates and in the ten infected cattle herds observed in the vicinity of this forest since 1986, suggesting that there is a real epidemiological link between wild and domestic animals. Faced with this situation and taking into account the very particular environmental context, the decision was taken in 2006 to remove totally the red deer population from the Brotonne forest, counting on this species being the reservoir or maintenance host of the disease, and to drastically reduce the wild boar population, hoping that it is only a spill‐over host (hypotheses retained, based on the difference in the macroscopic fundings observed in red deer and wild boar, the foreign bibliography and the modelling works of the ANSES (Zanella et al., 2008)). During the 2007‐2008 hunting season, among the 65 culled red deer, 22 % were still tuberculous, while in the wild boar, the apparent infection prevalence had decreased to 19 % (n= 382). At the end of 2008, it was considered that less than 50 red deer remained in the forest, some of which could still be tuberculous, and that wild boar numbers had significantly decreased. During the 2008‐2009 hunting season, among 19 red deer that were shot and examined, a single animal was tuberculous, while the infection prevalence had decreased to 11 % in the wild boar (Hars et al., 2008b ; Hars et al., 2009). Although it is too soon for us to draw conclusions, we hope that these encouraging results reveal the effectiveness of the control plan. It should be noted that since 2001, among several dozens of tested animals for each species, a single badger, a single roe deer and a single fox were found to be infected by M. bovis in the Brotonne forest.
In Cote d’Or Following several bovine tuberculosis oubreaks in the Pouilly en Auxois canton in 2002, an epidemiological survey of wildlife in the « infected zone» (massif and valley of Ouche) revealed the presence of a hind suffering from a generalized tuberculosis, involving the same bacillus (SB0134) as that isolated in cattle. The surveys conducted between the 2003‐2004 and 2006‐2007 hunting seasons did not reveal the presence of any other tuberculous red deer (n = 284) or badger (n = 63), and only two wild boars with stabilised ganglionic cephalic lesions (n = 160). This apparently favourable situation showed that wildlife was obviously not at the origin of the bovine epizootic. However, on account of the fact that the bovine infection, far from dying out, was also revealed in a second zone (Vénarey‐Vitteaux region), with another M. bovis strain involved (spoligotype SB0120), the wildlife surveillance was maintained, wisely, since it enabled the discovery of 7 infected wild boars (n = 99) in 2007‐2008, including a young animal suffering from an evolutive tuberculosis, and 23 infected wild boars (n = 150), including six young animals with evolutive lesions in 2008‐2009. The apparent infection prevalence seemed to be much higher in the Ouche zone (16,5 %), where the wild boar density was much higher than in the Vénarey‐Vitteaux zone (Hars and Rossi, 2009). While more than 60 cattle herds have been slaughtered on account of tuberculosis since
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2002, there has been an emergence of tuberculosis oubreaks among wild boars in the infected zones since 2007, and reinfection risks for cattle are not well under control. Elsewhere in France, tuberculosis cases have been discovered in wild boars in Corsica (Richomme et al., under press) since 2003 (nine cases including four in 2007) and in Pyrénées‐Atlantiques since 2005 (four cases, n = 227, including 3 in 2006‐2007), some of which exhibited evolutive pulmonary lesions. The bacterial strains affecting wild boar, to date, have always been identical to those isolated in cattle in the considered region. These cases, more sporadic than in the Brotonne forest and in Côte d’Or, enable us to say that the wild boar is a good epidemiological sentinel for bovine infections, but it is unclear whether it poses a real risk of re‐contamination of cattle herds that have meanwhile been rendered free from disease. It should be noted that in Dordogne, where, as in Côte d’Or, a spectacular upsurge of tuberculosis occurred in cattle herds since 2004, M. bovis has never been isolated on almost 500 red deer, roe deer and wild boars that were analysed in areas « at risk ». The discovery of a wild reservoir of bovine tuberculosis is the example of an emerging problem, or pseudo‐emerging problem (since ancient but recently revealed) in wildlife, concerning a disease that is regulated under the rural code, undergoing eradication in the French cattle population and resulting in a long term risk of re‐contamination of domestic animals and/or of transmission to humans. VI.E Avian schistosoma : biodiversity, host – parasite relationships, implications in cercarial dermatitis by Damien Jouet and Hubert Ferté, JE2533 ‐ USC Vecpar Afssa – UFR of Pharmacy, Reims
The increase in aquatic bird populations (migratory and sedentary) on various lakes and the increase in human activities, in particular touristic, on the same sites have favoured the emergence or re‐mergence in France of a parasitosis caused by avian schistosoma : cercarial dermatitis. At the adult stage, these trematodes parasitize aquatic birds. The cycle involves freshwater molluscs which release cercariae belonging to the furcocercariae group, which is the infective stage for the final host. These cercariae can accidentally enter in humans, with ensuing more or less important cutaneous signs. In partnership with managers of lakes with a recreational calling (Der‐Chantecoq lake, Annecy lake), epidemiosurveillance missions have been set up to isolate and identify the various causative agents among the different species involved in the cycle (aquatic birds and molluscs). We were thus able to establish the presence of the various types of carcariae shed by molluscs and to specify the prevalence of those of avian schistosoma, causing cercarial dermatitis. We identified Trichobilharzia szidati, T. franki and T. regenti, for which the complete parasitic cycle is achieved in France. Thanks to the help of the technicians of the ONCFS station on Der‐Chantecoq lake and of the LDAV of Aube and Haute‐Savoie, we could instigate a fauna inventory on several aquatic birds (26 studied species), which enabled us to characterize from a morphological and /or molecular point of view the avian schistosoma in the Bilharziella, Dendrithobilharzia or Trichobilharzia genuses, the latter including the major known species acknowledged as potential causative agents of cercarial dermatitis in Europe. According to the nasal or visceral localization of these parasites, the observed prevalences among aquatic birds are detailed in Table X.
Table IX : Observed prevalences of avian schistosoma in 16 bird species according to the visceral or nasal localization of parasites
Visceral species Nasal species Host species
Examined Infested Examined Infested
Anas platyrhynchos 32 27 196 108
Anas clypeata 5 2 5 2
Anas crecca 15 9 22 0
Anas acuta 2 1 3 0
Anas strepera 2 0 3 0
Aythya fuligula 1 1 6 3
Aythya ferina 2 0 11 1
Cygnus olor 13 6 59 17
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Anser anser 10 6 9 0
Mergus merganser 0 0 1 1
Grus grus 5 1 3 0
Fulica atra 1 0 3 0
Gallinula chloropus 3 1 3 0
Phalacrocorax carbo 3 0 9 0
Podiceps cristatus 1 0 2 0
Ardea cinerea 2 1 2 0
Total 97 55 337 132
In addition to the standard morphological study of adult worms, a molecular approach was applied on several domains of the ribosomial (D2, ITS) and mitochondrial (COX1) DNA (markers considered as species‐ or population‐ specific, commonly used in Trematodes and Nematodes). This molecular approach enabled us to establish the existence of several haplotypes corresponding to the T. franki, T. regenti, T. szidati, Bilharziella polonica and Dendritobilharzia pulverulenta species, but also several new haplotypes non‐attributable to a given species. The continuation of our works should allow us to confirm or not their status of new species or species formerly characterized on other continents (Africa, North America).
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CONCLUSIONS
The SAGIR network has recorded 11 634 cases from 1rst Janurary 2006 to 31 December 2008 inclusive. These cases concerned 175 species of wild birds and mammals, either found dead or captured sick in the field. The species whose hunting is authorized in France were predominant in the sample of these three years. The seven most represented species are, in decreasing order of the number of cases, the European brown hare, the roe deer, the mallard, pigeon sp., the wild boar, the European rabbit and the red fox. The sample also includes a significant portion of specimens belonging to species that are protected in France, with 3 % of raptors and 2 % of larid species. The common buzzard for example ranks in the 9th position among the most analysed species.
The SAGIR network surveillance is conducted throughout the year. Cases have been recorded in all the months of each year, with monthly variations related to health events and to the presence in the field of the network’s observers, hunters, naturalists, technicians of the Departemental hunting federations and agents of the National hunting and wildlife agency (ONCFS). The surveillance has a nationwide coverage. Cases have been recorded in almost all departements, with, since 2007, cases in Martinique, the first overseas departement to have joined the network.
Aetiological diagnoses, when they could be set by veterinary analyses, ranged from infectious and parasitic diseases to intoxications by chemical substances. The dominant pathological features of the main flagship species of the SAGIR network identified during these three years were the same as in previous years, except for slight differences. New health events have extended the range of pathogens identified in wild animals since the network’s creation. Either the pathogen was determining in the observed mortality, this is the case of type D botulism identified in the yellow‐legged gull, or of the highly pathogenic avian influenza virus H5N1 in various anatid species. Or the pathogen was simply isolated thanks to the various analyses, without there being an apparent relation of cause and effect with the animal’s death, this is the case of the bluetongue virus identified in red deer. Or the pathogen was isolated and its role in the pathology is unknown, a relationship is possible between its presence and the death or disease of individuals, this is the case of Mycoplasma agalactiae isolated in the lungs of Alpine ibex, or parasites in the Protostrongylus genus identified in the lungs of European brown hares.
In 2006, as in 2007 and 2008, the SAGIR network has once more demonstrated its capacity to detect, report observed events and, according to the pathogens involved, strengthen the surveillance and participate in health crisis management. The purpose of SAGIR is to carry out surveillance in order to act (surveiller pour agir). This motto makes sense when SAGIR, aware of the limits of its methodological scope, hands the work over to other surveillance systems or other research teams, or works jointly with them, to enhance the understanding of a pathological phenomenon. Indeed, the network’s useful results have also shown their limitations for the characterization of a disease in space and time, in particular regarding the dominant pathological features regularly monitored by the network since its creation. The case of tularemia raises the question of the perceived but not quantified progression of the disease, while the case of the European brown hare syndrom raises questions on the mechanisms underlying epizootics periodically observed in populations. In both cases, the SAGIR network contributes to inform research teams in epidemiology and population dynamics, to improve knowledge and, in the long run, often after several years of works, to determine risk management measures.
Although the SAGIR network is effective for the epidemiovigilance of some wild bird and mammal diseases, it can still aim to progress, following its long history and its commitments to its objectives. In this field, the results of these three years have emphasized once more the essential importance of case histories collected by the observer at the time of the discovery. This information is helpful for the diagnosis – no good diagnosis without a case history ! – and can be used in epidemiological analyses. Pulmonary strongylosis of the European brown hare is a perfect illustration since case histories have been determining to put forward hypotheses on the disease epidemiology and to set up the research protocol. In the field of the surveillance of non intentional effects of the use of phytopharmaceutical products in agriculture, these case histories have a major importance for distinguishing the effects due to the use of products in accordance with the conditions of their authorized marketing, from the other effects, due to their misuse (failure to respect authorization regulations or approved agricultural practices), and those due to an
42
intentional action aiming at destroying wild birds and mammals. In the first case, surveillance in the field provides knowledge that allows a better correspondance between the a priori risk assessment, which has methodological limitations, and the real risks in the field. In this regard, SAGIR, in addition to the regulatory assessment of risks, can serve as a decision support tool for risk managers. In this way, the study of intoxications by rodenticide anticoagulants among wild birds and mammals has enabled the identification of two risk situations and the characterization of overall management solutions for reducing the risk (Lasseur et al., under press). One can thus hope that the still very high number of intoxication cases due to these molecules recorded from 2006 to 2008 will decrease thanks to the implementation of these management measures by farmers, under the instigation of manufacturers and the authorities.
Still in the field of phytopharmaceutical products, a very high number of intoxication cases due to molecules inhibiting cholinesterase – in practice, most insecticides – confirm the impact of these substances on exposed wild birds and mammals. Thanks to the case histories, a portion of cases have been detected on animals that were captured in the field, exhibiting a particular behaviour, or on animals for which the aetiology of death was attributed to predation or to a shock, but found to be contaminated by these substances. These data, already extensive, are worth consolidating since they contribute to the knowlege of sublethal effects of chemical substances on the environment, a wide area still largely undocumented.
SAGIR is thus obviously a reference network for the biological surveillance of the territory. Its effectiveness for wildlife health monitoring and for the surveillance of some diseases and some effects of anthropic activities relies on a collaboration system at the center of which hunters, staff of the Hunting federations, agents of the National hunting and wildlife agency (ONCFS), specialists of the departemental veterinary laboratories, play essential roles. Always on the move – this has been SAGIR’s line of conduct since over forty years – directions for improvement to strengthen epidemiovigilance results have bee identified, as well as for the epidemiosurveillance of some diseases of relevance for the network. SAGIR relentlessly carries on the monitoring by always endeavouring to strengthen its capacities to further the objective of excellence, while not exceeding its scope of intervention.
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Appendix 1
LIST OF BIRD AND MAMMAL SPECIES REPRESENTED IN THE SAGIR DATABASE (by alphabetical order of the vernacular name)
Threskiornis aethiopicus African sacred ibis Falco subbuteo Hobby
Capra ibex Alpine ibex Delichon urbicum House martin
Marmota marmota Alpine marmot Mus musculus House mouse
Recurvirostra avosetta Avocet Rattus rattus House rat
Anser indicus Bar‐headed goose Passer domesticus House sparrow
Tyto alba Barn owl Lymnocryptes minimus Jack snipe
Branta leucopsis Barnacle goose Coloeus monedula Jackdaw
Anser fabalis Bean goose Garrulus glandarius Jay
Gypaetus barbatus Bearded vulture Alcedo atthis Kingfisher
Martes foina Beech marten Regulus sp. Kinglet sp.
Botaurus stellaris Bittern Rissa tridactyla Kittiwake
Lyrurus tetrix Black grouse Vanellus vanellus Lapwing
Milvus migrans Black kite Vanellus sp. Lapwing sp.
Phoenicurus ochruros Black redstrart Mustela nivalis Least weasel
Ciconia nigra Black storck Larus fuscus Lesser black‐backed gull
Cygnus atratus Black swan Carduelis cannabina Linnet
Turdus merula Blackbird Ixobrychus minutus Little bittern
Sylvia atricapilla Blackcap Egretta garzetta Little egret
Chroicocephalus ridibundus Black‐headed gull Tachybaptus ruficollis Little grebe
Himantopus himantopus Black‐winged stilt Charadrius dubius Little ringed plover
Cyanistes caeruleus Blue tit Sternula albifrons Little tern
Aquila fasciata Bonelli’s eagle Asio otus Long‐eared owl
Fringilla montifringilla Brambling Pica pica Magpie
Branta bernicla Brent goose Anas platyrhynchos Mallard
Ursus arctos Brown bear Aix galericulata Mandarin
Anous stolidus Brown noddy Circus aeruginosus Marsh harrier
Rattus norvegicus Brown rat Meadow vole sp.
Budgerigar sp. Ichthyaetus melanocephalus Mediterranean gull
Branta canadensis Canada goose Falco columbarius Merlin
Tetrao urogallus Capercaillie Turdus viscivorus Mistle thrush
Corvus corone Carrion crow Circus pygargus Montagu’s harrier
Bubulcus ibis Cattle egret Gallinula chloropus Moorhen
Fringilla coelebs Chaffinch Ovis gmelini musimon Mouflon
Rupicapra rupicapra Chamois Lepus timidus Mountain hare
Emberiza cirlus Cirl bunting Ondatra zibethicus Muskrat
Serinus serinus Citril finch Cygnus olor Mute swan
Periparus ater Coal tit Procyon lotor Northern raccoon
colibri sp. Nucifraga caryocatactes Nutcracker
Streptopelia decaocto Collared dove Sitta europaea Nuthatch
Buteo buteo Common buzzard Pandion haliaetus Osprey
Genetta genetta Common genet Haematopus ostralegus Oystercatcher
Larus canus Common gull Falco peregrinus Peregrine
Cricetus cricetus Common hamster Phasianus colchicus Pheasant
Falco tinnunculus Common kestrel Anas acuta Pintail
Aythya ferina Common pochard Pipistrellus sp. Pipistrelle sp.
Actitis hypoleucos Common sandpiper Lagopus muta Ptarmigan
Melanitta nigra Common scoter Rupicapra pyrenaica Pyrenean chamois
Trachemys scripta Common slider Coturnix coturnix Quail
Fulica atra Coot Nyctereutes procyonoides Raccoon‐dog
Phalacrocorax carbo Cormorant Corvus corax Raven
Myocastor coypus Coypu Alca torda Razorbill
Grus grus Crane Amandava amandava Red adavat
Numenius sp. Curlew sp. Cervus elaphus Red deer
Prunella modularis Dunnock Vulpes vulpes Red fox
Neophron percnopterus Egyptian vulture Milvus milvus Red kite
Somateria mollissima Eider Sciurus vulgaris Red squirrel
Mustela erminea Ermine Netta rufina Red‐crested pochard
Meles meles Eurasian badger Alectoris rufa Red‐legged partridge
Castor fiber Eurasian beaver Podiceps grisegena Red‐necked grebe
Bubo bubo Eurasian eagle‐owl Tringa totanus Redshank
Erinaceus europaeus Eurasian hedgehog Turdus iliacus Redwing
Felis lynx Eurasian lynx Syrmaticus reevesii Reeve’s pheasant
Lepus europaeus European brown hare Erithacus rubecula Robin
Lutra lutra European otter Columba livia Rock pigeon
Martes martes European pine marten Capreolus capreolus Roe deer
Mustela putorius European polecat Corvus frugilegus Rook
Oryctolagus cuniculus European rabbit Philomachus pugnax Ruff
Dama dama Fallow deer Sandpiper sp.
Mustela furo Ferret Tadorna tadorna Shelduck
Turdus pilaris Fieldfare Circaetus gallicus Short‐toed eagle
Phoenicopterus roseus Flamingo Certhia brachydactyla Short‐toed tree creeper
Flycatcher sp. Anas clypeata Shoveler
Fulmarus glacialis Fulmar Cervus nippon Sika deer
Anas strepera Gadwall Carduelis spinus Siskin
Morus bassanus Gannet Alauda arvensis Skylark
Eliomys quercinus Garden dormouse Gallinago gallinago Snipe
Anas querquedula Garganey Turdus philomelos Song thrush
Aquila chrysaetos Golden eagle Accipiter nisus Sparrow hawk
Bucephala clangula Goldeneye Platalea leucorodia Spoonbill
Carduelis carduelis Goldfinch Porzana porzana Spotted crake
Mergus merganser Goosander Aquila clanga Spotted eagle
Accipiter gentilis Goshawk Sturnus vulgaris Starling
Podiceps cristatus Great crested grebe Columba oenas Stock dove
Dendrocopos major Great spotted woodpecker Ciconia sp. Storck sp.
Parus major Great tit Striped skunks sp.
Ardea alba Great white egret Hirundo rustica Swallow
Rhinolophus ferrumequinum Greater horseshoe bat Cygnus sp. Swan sp.
Myotis myotis Greater mouse‐eared bat Strix aluco Tawny owl
Tringa ochropus Green sandpiper Anas crecca Teal
Picus viridis Green woodpecker Aythya fuligula Tufted duck
Carduelis chloris Greenfinch Streptopelia turtur Turtle dove
Tringa nebularia Greenshank Rallus aquaticus Water rail
Ardea cinerea Grey heron Motacilla alba White wagtail
Perdix perdix Grey partridge Anser albifrons White‐fronted goose
Anser anser Grey‐lag goose Anas penelope Wigeon
Gyps fulvus Griffon vulture Sus scrofa Wild boar
Uria aalge Guillemot Felis silvestris Wild cat
Gelochelidon nilotica Gull‐billed tern Canis lupus Wolf
Phoca vitulina Harbour seal Aix sponsa Wood duck
Lepus sp. Hare sp. Columba palumbus Wood pigeon
Coccothraustes coccothraustes Hawfinch Scolopax rusticola Woodcock
Tetrastes bonasia Hazel grouse Troglodytes troglodytes Wren
Circus cyaneus Hen harrier Emberiza citrinella Yellowhammer
Larus argentatus Herring gull Larus michahellis Yellow‐legged gull
3 - MORTALITÉ GROUPÉE Oui NonEspèce(s) et nombre observé : .........................................
Nombre collecté : .........................................................Date(s) de découverte : ..................................................N° de fiche SAGIR des animaux portés au laboratoire : ............................................................................................
SURVEILLANCE SANITAIRE NATIONALE DE LA FAUNE SAUVAGE
SAGIRNom du laboratoire : ...............................Numéro du laboratoire : ...........................Date de dépôt : .....................................Prélèvement(s) à conserver Photo(s)
DÉCOUVREURNom et prénom .............................................................
Organisme ...................................................................
Téléphone
Email .........................................................................
OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL
COMMENTAIRES :
Cause de la mort suspectée :............................................ à cause des symptômes ou parce que la maladie circule dans la région
COLLECTEURNom et prénom ..............................................................
Organisme ....................................................................
Téléphone
Email .........................................................................
1 - DÉCOUVERTEPrécisez à quelle date : ....................................................
Commune : ..................................................................
Lieu-dit : .....................................................................
Coordonnées GPS (X et Y) : ...............................................
Système de projection : ...................................................
Précisez si lieu remarquable ( ) : .................................
La facture est à adresser à : FDC ONCFS
Autre (précisez) ..........................
Il s’agit d’une opération spéciale : oui non
Précisez : ........................................................
Feuillet n° 1 : à conserver par le Laboratoire départemental
2 - DESCRIPTION DU PRÉLÈVEMENTEspèce (nom complet, ex : Pigeon ramier) : .........................................
Animal trouvé vivant, si achevé, précisez comment :
................................................................................
Animal trouvé mort, vous avez collecté : Le cadavre entier Des organes (précisez lesquels) : ................................... Autres (précisez) : ..................................................
Comment avez-vous conservé le cadavre ?
A température ambiante Au réfrigérateur ou avec des pains de glace A quelle date l’avez-vous réfrigéré : ............................... Au congélateur A quelle date l’avez-vous congelé : ................................
Quel est l’état physiologique de l’animal ? Bon Mauvais Indéterminé
Quel est le sexe de l’animal ? Mâle Femelle Indéterminé
L’âge de l’animal est déterminé à partir Des cornes Des dents Des plumes Des os / cartilage (précisez) : .............................................
Quel est l’âge de l’animal ? Nouveau-né Immature Adulte Indéterminé
4 - COMMÉMORATIFSA - ENVIRONNEMENT DU CADAVREY-a-t-il des infrastructures à moins de 150 m ? Ligne électrique, câble (précisez) : ...................................... Route, chemin (précisez, ex. RN10, ...) : ...................................... Autres (précisez, ex. barbelés, éoliennes, ...) : .....................................Quelles sont les cultures et leurs stades végétatifs dans un rayon de 500 m : ............................................................................................................................................Y-a-t-il eu des traitements pesticides récemment ? Ne sais pas Non Oui, il y a combien de temps ? ...............................Avez-vous remarqué des tas ou des semences non enfouies ? Non Oui
B - EXAMEN EXTERNE DU CADAVREAvez-vous remarqué une position particulière de l’animal ? RAS Particulière (précisez) : ...........................................La rigidité cadavérique s’est-elle installée ? Oui Non IndéterminéAvez-vous remarqué la présence d’indices biologiques ? Non Oui, précisez : Du sang (précisez la localisation) : ............................................ De l’urine, (précisez la couleur) : ............................................ Des écoulements, (précisez la nature et la localisation) : .................... De la diarrhée Autres (précisez) : ..........................................................Y-a-t-il des traces de morsures ? Non Par les chiens à la découverte Avant la découverteY-a-t-il des traces de désordre autour de l’animal indiquant Qu’il y a eu lutte Qu’il y a eu pédalageAvez-vous trouvé des insectes morts autour du cadavre ? Oui
C - SYMPTÔMES SI L’ANIMAL EST TROUVÉ VIVANTTroubles Boiterielocomoteurs Autre (précisez) : ....................................Troubles visuels Aveugle Autre (précisez) : ....................Troubles digestifs Salivation Autre (précisez) : ...................Troubles pulmonaires Toux Écoulementnasal Essoufflement Autre (précisez) : .......................................... .................Troubles nerveux L’animal a conservé sa vigilance Oui Non L’animal tourne sur lui-même L’animal se démange furieusement L’animal ne s’enfuit pas L’animal est paralysé Autres :....................................................................
grotte, cours d’eau, sommet, ...
N° de fiche SAGIR
3 - MORTALITÉ GROUPÉE Oui NonEspèce(s) et nombre observé : .........................................
Nombre collecté : .........................................................Date(s) de découverte : ..................................................N° de fiche SAGIR des animaux portés au laboratoire : ............................................................................................
SURVEILLANCE SANITAIRE NATIONALE DE LA FAUNE SAUVAGE
SAGIRNom du laboratoire : ...............................Numéro du laboratoire : ...........................Date de dépôt : .....................................Prélèvement(s) à conserver Photo(s)
DÉCOUVREURNom et prénom .............................................................
Organisme ...................................................................
Téléphone
Email .........................................................................
OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL DE LA CHASSE ET DE LA FAUNE SAUVAGE OFFICE NATIONAL
COMMENTAIRES :
Cause de la mort suspectée :............................................ à cause des symptômes ou parce que la maladie circule dans la région
COLLECTEURNom et prénom ..............................................................
Organisme ....................................................................
Téléphone
Email .........................................................................
1 - DÉCOUVERTEPrécisez à quelle date : ....................................................
Commune : ..................................................................
Lieu-dit : .....................................................................
Coordonnées GPS (X et Y) : ...............................................
Système de projection : ...................................................
Précisez si lieu remarquable ( ) : .................................
La facture est à adresser à : FDC ONCFS
Autre (précisez) ..........................
Il s’agit d’une opération spéciale : oui non
Précisez : ........................................................
Feuillet n° 1 : à conserver par le Laboratoire départemental
2 - DESCRIPTION DU PRÉLÈVEMENTEspèce (nom complet, ex : Pigeon ramier) : .........................................
Animal trouvé vivant, si achevé, précisez comment :
................................................................................
Animal trouvé mort, vous avez collecté : Le cadavre entier Des organes (précisez lesquels) : ................................... Autres (précisez) : ..................................................
Comment avez-vous conservé le cadavre ?
A température ambiante Au réfrigérateur ou avec des pains de glace A quelle date l’avez-vous réfrigéré : ............................... Au congélateur A quelle date l’avez-vous congelé : ................................
Quel est l’état physiologique de l’animal ? Bon Mauvais Indéterminé
Quel est le sexe de l’animal ? Mâle Femelle Indéterminé
L’âge de l’animal est déterminé à partir Des cornes Des dents Des plumes Des os / cartilage (précisez) : .............................................
Quel est l’âge de l’animal ? Nouveau-né Immature Adulte Indéterminé
4 - COMMÉMORATIFSA - ENVIRONNEMENT DU CADAVREY-a-t-il des infrastructures à moins de 150 m ? Ligne électrique, câble (précisez) : ...................................... Route, chemin (précisez, ex. RN10, ...) : ...................................... Autres (précisez, ex. barbelés, éoliennes, ...) : .....................................Quelles sont les cultures et leurs stades végétatifs dans un rayon de 500 m : ............................................................................................................................................Y-a-t-il eu des traitements pesticides récemment ? Ne sais pas Non Oui, il y a combien de temps ? ...............................Avez-vous remarqué des tas ou des semences non enfouies ? Non Oui
B - EXAMEN EXTERNE DU CADAVREAvez-vous remarqué une position particulière de l’animal ? RAS Particulière (précisez) : ...........................................La rigidité cadavérique s’est-elle installée ? Oui Non IndéterminéAvez-vous remarqué la présence d’indices biologiques ? Non Oui, précisez : Du sang (précisez la localisation) : ............................................ De l’urine, (précisez la couleur) : ............................................ Des écoulements, (précisez la nature et la localisation) : .................... De la diarrhée Autres (précisez) : ..........................................................Y-a-t-il des traces de morsures ? Non Par les chiens à la découverte Avant la découverteY-a-t-il des traces de désordre autour de l’animal indiquant Qu’il y a eu lutte Qu’il y a eu pédalageAvez-vous trouvé des insectes morts autour du cadavre ? Oui
C - SYMPTÔMES SI L’ANIMAL EST TROUVÉ VIVANTTroubles Boiterielocomoteurs Autre (précisez) : ....................................Troubles visuels Aveugle Autre (précisez) : ....................Troubles digestifs Salivation Autre (précisez) : ...................Troubles pulmonaires Toux Écoulementnasal Essoufflement Autre (précisez) : .......................................... .................Troubles nerveux L’animal a conservé sa vigilance Oui Non L’animal tourne sur lui-même L’animal se démange furieusement L’animal ne s’enfuit pas L’animal est paralysé Autres :....................................................................
grotte, cours d’eau, sommet, ...
N° de fiche SAGIR
ABSTRACT
From 2006 to 2008, the SAGIR network has analysed 11 634 specimens belonging to 175 wild bird and mammal species in almost all departements in France. Species whose hunting is authorized in France are predominant in the sample, with the European brown hare, the roe deer, the mallard, pigeon sp., the wild boar, the European rabbit and the red fox at the top of the list. The sample also includes a significant portion of protected species specimens. For example, the common buzzard ranks in the 9th position among the most analysed species.
Aetiological diagnoses range from infectious and parasitic diseases to intoxications by chemical substances. The dominant pathological features of the network’s flagship species identified during these three years were the same as in previous years, except for slight differences.
New health events have extended the range of pathogens identified in wild animals since the network’s creation. Among the ten new pathogens and diseases detected by SAGIR between 2006 and 2008 :
- identification of type D botulic toxin in the yellow‐legged gull ;
- isolation of Mycoplasma agalactiae in the lungs of Alpine ibex ;
- detection of the avian influenza virus H5N1 HP in 65 wild birds among the 3426 analysed in 2006 ;
- detection of the bluetongue virus in 2 red deer in 2007 ;
- observation of the first cases of duck viral enteritis ;
- emergence of pulmonary strongylosis of the European brow hare.
Meanwhile, the network recorded particularly lethal trichomonosis episodes in columbids, during the wintering period, but also at the time of reproduction, in particular in the stock dove. In the field of the surveillance of the network’s dominant pathological features, tularemia cases in the European brown hare were particularly important during the 2007‐2008 winter.
Lastly, 411 cases of intoxication were confirmed by analyses. The use of phytopharmaceutical products in agriculture and intentional actions were the source of these intoxications. During these three years, the high number of cases due to chloralose, to cholinesterase inhibiting molecules and anticoagulant rodenticides, have confirmed the impact of these substances on exposed wild birds and mammals. These results as a whole confirm that the SAGIR network is an effective epidemiosurveillance system. In the field of the epidemiosurveillance of some wildlife diseases, including those that are shared with domestic animals, the SAGIR network is articulated with other surveillance systems to enable the understanding of diseases’ functioning. The SAGIR network participates in this way to the determination of management measures for wildlife, the protection of hunters, and more generally, public health.