An innovative strategy for deworming dogs in Mediterranean areas highly endemic for cystic echinococcosis.

Canids Control programs Echinococcus granulosus GPS dataloggers Geospatial data Home range

Journal

Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774

Informations de publication

Date de publication:
23 Feb 2024
Historique:
received: 12 12 2023
accepted: 07 02 2024
medline: 24 2 2024
pubmed: 24 2 2024
entrez: 23 2 2024
Statut: epublish

Résumé

Cystic echinococcosis (CE), caused by the larval stage of Echinococcus granulosus sensu lato, is a zoonotic parasitic disease of economic and public health importance worldwide, especially in the Mediterranean area. Canids are the main definitive hosts of the adult cestode contaminating the environment with parasite eggs released with feces. In rural and peri-urban areas, the risk of transmission to livestock as well as humans is high because of the free-roaming behavior of owned/not owned dogs. Collecting data on animal movements and behavior using GPS dataloggers could be a milestone to contain the spread of this parasitosis. Thus, this study aims to develop a comprehensive control strategy, focused on deworming a dog population in a pilot area of southern Italy (Campania region) highly endemic for CE. Accordingly, five sheep farms, tested to be positive for CE, were selected. In each sheep farm, all shepherd dogs present were treated every 2 months with praziquantel. Furthermore, 15 GPS dataloggers were applied to sheep and dogs, and their movements were tracked for 1 month; the distances that they traveled and their respective home ranges were determined using minimum convex polygon (MCP) analysis with a convex hull geometry as output. The results showed that the mean daily walking distances traveled by sheep and dogs did not significantly differ. Over 90% of the point locations collected by GPS fell within 1500 mt of the farm, and the longest distances were traveled between 10:00 and 17:00. In all the sheep farms monitored, the area traversed by the animals during their daily activities showed an extension of < 250 hectares. Based on the home range of the animals, the area with the highest risk of access from canids (minimum safe convex polygon) was estimated around the centroid of each farm, and a potential scheme for the delivery of praziquantel-laced baits for the treatment of not owned dogs gravitating around the grazing area was designed. This study documents the usefulness of geospatial technology in supporting parasite control strategies to reduce disease transmission.

Sections du résumé

BACKGROUND BACKGROUND
Cystic echinococcosis (CE), caused by the larval stage of Echinococcus granulosus sensu lato, is a zoonotic parasitic disease of economic and public health importance worldwide, especially in the Mediterranean area. Canids are the main definitive hosts of the adult cestode contaminating the environment with parasite eggs released with feces. In rural and peri-urban areas, the risk of transmission to livestock as well as humans is high because of the free-roaming behavior of owned/not owned dogs. Collecting data on animal movements and behavior using GPS dataloggers could be a milestone to contain the spread of this parasitosis. Thus, this study aims to develop a comprehensive control strategy, focused on deworming a dog population in a pilot area of southern Italy (Campania region) highly endemic for CE.
METHODS METHODS
Accordingly, five sheep farms, tested to be positive for CE, were selected. In each sheep farm, all shepherd dogs present were treated every 2 months with praziquantel. Furthermore, 15 GPS dataloggers were applied to sheep and dogs, and their movements were tracked for 1 month; the distances that they traveled and their respective home ranges were determined using minimum convex polygon (MCP) analysis with a convex hull geometry as output.
RESULTS RESULTS
The results showed that the mean daily walking distances traveled by sheep and dogs did not significantly differ. Over 90% of the point locations collected by GPS fell within 1500 mt of the farm, and the longest distances were traveled between 10:00 and 17:00. In all the sheep farms monitored, the area traversed by the animals during their daily activities showed an extension of < 250 hectares. Based on the home range of the animals, the area with the highest risk of access from canids (minimum safe convex polygon) was estimated around the centroid of each farm, and a potential scheme for the delivery of praziquantel-laced baits for the treatment of not owned dogs gravitating around the grazing area was designed.
CONCLUSIONS CONCLUSIONS
This study documents the usefulness of geospatial technology in supporting parasite control strategies to reduce disease transmission.

Identifiants

pubmed: 38395867
doi: 10.1186/s13071-024-06184-x
pii: 10.1186/s13071-024-06184-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

86

Subventions

Organisme : Partnership for Research and Innovation in the Mediterranean Area (PRIMA)
ID : ECHINO-SAFE-MED project

Informations de copyright

© 2024. The Author(s).

Références

Neglected tropical diseases.World Health Organization (WHO); 2023. https://www.who.int/health-topics/neglected-tropical-diseases#tab=tab_1 . Accessed 1 Nov 2023.
Casulli A, Abela-Ridder B, Petrone D, Fabiani M, Bobić B, Carmena D, et al. Unveiling the incidences and trends of the neglected zoonosis cystic echinococcosis in Europe: a systematic review from the MEmE project. Lancet Infect Dis. 2022;23:e95–107.
pubmed: 36427513 doi: 10.1016/S1473-3099(22)00638-7
Casulli A, Massolo A, Saarma U, Umhang G, Santolamazza F, Santoro A. Species and genotypes belonging to Echinococcus granulosus sensu lato complex causing human cystic echinococcosis in Europe (2000–2021): a systematic review. Parasit Vectors. 2022;15:109.
pubmed: 35346335 pmcid: 8962544 doi: 10.1186/s13071-022-05197-8
Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, et al. Ecology and Life Cycle Patterns of Echinococcus Species. Adv Parasitol. 2017;95:213–314.
pubmed: 28131364 doi: 10.1016/bs.apar.2016.11.002
Tamarozzi F, Legnardi M, Fittipaldo A, Drigo M, Cassini R. Epidemiological distribution of Echinococcus granulosus s.l. infection in human and domestic animal hosts in European Mediterranean and Balkan countries: a systematic review. PLoS Negl Trop Dis. 2020;14:e0008519.
pubmed: 32776936 pmcid: 7440662 doi: 10.1371/journal.pntd.0008519
Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol. 2017;95:315–493.
pubmed: 28131365 doi: 10.1016/bs.apar.2016.11.001
Shams M, Khazaei S, Naserifar R, Shariatzadeh SA, Anvari D, Montazeri F, et al. Global distribution of Echinococcus granulosus genotypes in domestic and wild canids: a systematic review and meta-analysis. Parasitol. 2022;149:1147–59.
doi: 10.1017/S0031182022000658
Cringoli G, Rinaldi L, Musella V, Veneziano V, Maurelli MP, Di Pietro F, et al. Geo-referencing livestock farms as tool for studying cystic echinococcosis epidemiology in cattle and water buffaloes from southern Italy. Geospat Health. 2007;2:105–11.
pubmed: 18686260 doi: 10.4081/gh.2007.259
Rong X, Fan M, Sun X, Wang Y, Zhu H. Impact of disposing stray dogs on risk assessment and control of Echinococcosis in inner Mongolia. Math Biosci. 2018;299:85–96.
pubmed: 29526551 doi: 10.1016/j.mbs.2018.03.008
Rong X, Fan M, Zhu H, Zheng Y. Dynamic modeling and optimal control of cystic echinococcosis. Infect Dis Poverty. 2021;10:38.
pubmed: 33762009 pmcid: 7992812 doi: 10.1186/s40249-021-00807-6
Karshima SN, Ahmed MI, Adamu NB, Magaji AA, Zakariah M, Mohammed K. Africa-wide meta-analysis on the prevalence and distribution of human cystic echinococcosis and canine Echinococcus granulosus infections. Parasit Vectors. 2022;15:357.
pubmed: 36199100 pmcid: 9535855 doi: 10.1186/s13071-022-05474-6
Bentounsi B, Meradi S, Ayachi A, Cabaret J. Cestodes of untreated large stray dog populations in Algeria: a reservoir for herbivore and human parasitic diseases. Open Vet J. 2009;3:64–7.
doi: 10.2174/1874318809003010064
Lahmar S, Arfa I, Ben Othmen S, Jguirim W, Saïd Y, Dhibi A, et al. Intestinal helminths of stray dogs from Tunisia with special reference to zoonotic infections. Parasitol. 2017;3:e18.
Liberato C, Berrilli F, Odorizi L, Scarcella R, Barni M, Amoruso C, et al. Parasites in stray dogs from Italy: prevalence, risk factors and management concerns. Acta Parasitol. 2018;63:27–32.
pubmed: 29351076 doi: 10.1515/ap-2018-0003
Kachani M, Heath D. Dog population management for the control of human echinococcosis. Acta Trop. 2014;139:99–108.
pubmed: 25046696 doi: 10.1016/j.actatropica.2014.05.011
Humane Dog Population Management Guidance. International Companion Animal Management Coalition; 2019. https://www.icam-coalition.org/wp-content/uploads/2019/09/2019-ICAM-DPM-guidance-Interactive-updated-15-Oct-2019.pdf . Accessed 1 Nov 2023.
Lightowlers MW, Gasser RB, Hemphill A, Romig T, Tamarozzi F, Deplazes P, et al. Advances in the treatment, diagnosis, control and scientific understanding of taeniid cestode parasite infections over the past 50 years. Int J Parasitol. 2021;51:1167–92.
pubmed: 34757089 doi: 10.1016/j.ijpara.2021.10.003
Cringoli G, Pepe P, Bosco A, Maurelli MP, Baldi L, Ciaramella P, et al. An integrated approach to control Cystic Echinococcosis in southern Italy. Vet Parasitol. 2021;290:109347.
pubmed: 33444910 doi: 10.1016/j.vetpar.2021.109347
Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q. Echinococcosis: control and prevention. Adv Parasitol. 2017;96:55–158.
pubmed: 28212791 doi: 10.1016/bs.apar.2016.09.002
Larrieu E, Gavidia CM, Lightowlers MW. Control of cystic echinococcosis: background and prospects. Zoonoses Public Health. 2019;66:889–99.
pubmed: 31529690 doi: 10.1111/zph.12649
Yang YR, McManus DP, Huang Y, Heath DD. Echinococcus granulosus infection and options for control of cystic echinococcosis in Tibetan communities of Western Sichuan Province, China. PLoS Negl Trop Dis. 2009;3:e426.
pubmed: 19399162 pmcid: 2668793 doi: 10.1371/journal.pntd.0000426
Irabedra P, Ferreira C, Sayes J, Elola S, Rodríguez M, Morel N, et al. Control programme for cystic echinococcosis in Uruguay. Mem Inst Oswaldo Cruz. 2016;111:372–7.
pubmed: 27223652 pmcid: 4909035 doi: 10.1590/0074-02760160070
Amarir F, Rhalem A, Sadak A, Raes M, Oukessou M, Saadi A, et al. Control of cystic echinococcosis in the Middle Atlas, Morocco: field evaluation of the EG95 vaccine in sheep and cesticide treatment in dogs. PLoS Negl Trop Dis. 2021;15:e0009253.
pubmed: 33684115 pmcid: 7971873 doi: 10.1371/journal.pntd.0009253
Gädicke P, Heath D, Medina-Brunet A, Siva-de la Fuente MC, Espinoza-Rojas H, Villaguala-Pacheco C, et al. Assessment of the vaccination program against Cystic Echinococcosis in sheep in the pehuenche community of central Chile. Animal. 2022;12:679.
Vaniscotte A, Raoul F, Poulle ML, Romig T, Dinkel A, Takahashi K, et al. Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities. Parasitol. 2011;138:1316–29.
doi: 10.1017/S0031182011000874
Harriott L, Gentle M, Traub R, Cobbold R, Soares MR. Geographical distribution and risk factors for Echinococcus granulosus infection in peri-urban wild dog populations. Int J Parasitol Parasites Wildl. 2019;10:149–55.
pubmed: 31528538 pmcid: 6737342 doi: 10.1016/j.ijppaw.2019.08.005
Borriello G, Guccione J, Di Loria A, Bosco A, Pepe P, Prisco F, et al. Fast focus ultrasound liver technique for the assessment of cystic echinococcosis in sheep. Animal. 2021;11:452.
Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, et al. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat Protoc. 2017;12:1723–32.
pubmed: 28771238 doi: 10.1038/nprot.2017.067
Eckert J, Gemmell MA, Meslin F, Pawłowski ZS, WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. World Organisation for Animal Health; 2001. https://www.who.int/publications/i/item/929044522X . Accessed 1 Nov 2023.
Maurelli MP, Bosco A, Pepe P, Ianniello D, Amadesi A, Cringoli G, et al. Innovative tools for the diagnosis of Echinococcus granulosus in definitive hosts. Parasitol Res. 2018;117:2607–12.
pubmed: 29858944 doi: 10.1007/s00436-018-5952-1
Maksimov P, Bergmann H, Wassermann M, Romig T, Gottstein B, Casulli A, et al. Species detection within the Echinococcus granulosus sensu lato complex by novel probe-based real-time PCRs. Pathog. 2020;9:791.
doi: 10.3390/pathogens9100791
Trachsel D, Deplazes P, Mathis A. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitol. 2007;134:911–20.
doi: 10.1017/S0031182007002235
Sparkes J, Körtner G, Ballard G, Fleming PJ. Spatial and temporal activity patterns of owned, free-roaming dogs in coastal eastern Australia. Prev Vet Med. 2022;204:105641.
pubmed: 35461143 doi: 10.1016/j.prevetmed.2022.105641
Ciccone E, Lattero N, Bosco A, Nocerino M, Pepe P, Ciuca L, et al. Baiting stray dogs in extraurban area: Innovative tools for an integrated control of echinococcosis. In: 29th International conference of the world association for advancement of veterinary parasitology; 2023.
Umhang G, Possenti A, Colamesta V, d’Aguanno S, La Torre G, Boué F, et al. A systematic review and meta-analysis on anthelmintic control programs for Echinococcus multilocularis in wild and domestic carnivores. Food Waterborne Parasitol. 2019;15:e00042.
pubmed: 32095614 pmcid: 7034083 doi: 10.1016/j.fawpar.2019.e00042
Multi-Distance Spatial Cluster Analysis (Ripley’s K Function) (Spatial Statistic). ArcGIS Pro. https://pro.arcgis.com/en/pro-app/3.0/tool-reference/spatial-statistics/multi-distance-spatial-cluster-analysis.htm . Accessed 18 Oct 2023.
Serra E, Masu G, Chisu V, Cappai S, Masala G, Loi F, et al. Environmental contamination by Echinococcus spp. eggs as a risk for human health in educational farms of Sardinia, Italy. Vet Sci. 2022;9:143.
pubmed: 35324871 pmcid: 8953574 doi: 10.3390/vetsci9030143
Zhang W, Wang S, McManus DP. Echinococcus granulosus genomics: a new dawn for improved diagnosis, treatment, and control of echinococcosis. Parasite. 2014;21:66.
pubmed: 25514592 pmcid: 4267413 doi: 10.1051/parasite/2014066
Getz WM, Fortmann-Roe S, Cross PC, Lyons AJ, Ryan SJ, Wilmers CC. LoCoH: nonparameteric kernel methods for constructing home ranges and utilization distributions. PLoS ONE. 2007;2:e207.
pubmed: 17299587 pmcid: 1797616 doi: 10.1371/journal.pone.0000207
He P, Klarevas-Irby JA, Papageorgiou D, Christensen C, Strauss ED, Farine DR. A guide to sampling design for GPS-based studies of animal societies. Methods Ecol Evol. 2023;14:1887–905.
doi: 10.1111/2041-210X.13999
Muinde P, Bettridge JM, Sousa FM, Dürr S, Dohoo IR, Berezowski J. Who let the dogs out? Exploring the spatial ecology of free-roaming domestic dogs in western Kenya. Ecol Evol. 2021;11:4218–31.
pubmed: 33976805 pmcid: 8093722 doi: 10.1002/ece3.7317
Mutwiri T, Muigai AW, Magambo J, Mulinge E, Gitau L, Muinde P, et al. The potential role of roaming dogs in establishing a geographically novel life cycle of taeniids (Echinococcus spp. and Taenia spp.) in a non-endemic area. Vet Parasitol. 2023;38:100829.
Sparkes J, Ballard G, Fleming PJS, van de Ven R, Körtner G. Contact rates of wild-living and domestic dog populations in Australia: a new approach. Oecologia. 2016;182:1007–18.
pubmed: 27660202 doi: 10.1007/s00442-016-3720-4
Kennedy B, Brown WY, Vernes K, Körtner G, Butler JR. Dog and cat interactions in a remote Aboriginal community. Animal. 2018;8:65.
Maher EK, Ward MP, Brookes VJ. Investigation of the temporal roaming behaviour of free-roaming domestic dogs in Indigenous communities in northern Australia to inform rabies incursion preparedness. Sci Rep. 2019;9:14893.
pubmed: 31624301 pmcid: 6797733 doi: 10.1038/s41598-019-51447-8
Sparkes J, Körtner G, Ballard G, Fleming PJ, Brown WY. Effects of sex and reproductive state on interactions between free-roaming domestic dogs. PLoS ONE. 2014;9:e116053.
pubmed: 25541983 pmcid: 4277450 doi: 10.1371/journal.pone.0116053
Van Kesteren F, Mastin A, Mytynova B, Ziadinov I, Boufana B, Torgerson PR, et al. Dog ownership, dog behaviour and transmission of Echinococcus spp. in the Alay Valley, southern Kyrgyzstan. Parasitology. 2013;140:1674–84.
pubmed: 23985326 doi: 10.1017/S0031182013001182
Yu Q, Xiao N, Yang SJ, Han S. Deworming of stray dogs and wild canines with praziquantel-laced baits delivered by an unmanned aerial vehicle in areas highly endemic for echinococcosis in China. Infect Dis Poverty. 2017;6:117.
pubmed: 28655333 pmcid: 5488432 doi: 10.1186/s40249-017-0329-8
Pepin KM, Snow NP, Vercauteren KC. Optimal bait density for delivery of acute toxicants to vertebrate pests. J Pest Sci. 2020;93:723–35.
doi: 10.1007/s10340-020-01196-9
Laurimäe T, Kinkar L, Varcasia A, Dessì G, Sgroi G, D’Alessio N, et al. First detection of zoonotic tapeworm Echinococcus granulosus sensu lato genotype G7 in continental Italy. Parasitol Res. 2019;118:2193–201.
pubmed: 31134335 doi: 10.1007/s00436-019-06346-2
Sgroi G, Varcasia A, Dessì G, D’Alessio N, Pacifico L, Buono F, et al. Massive Taenia hydatigena Cysticercosis in a Wild Boar (Sus scrofa) from Italy. Acta Parasitol. 2019;64:938–41.
pubmed: 31444647 doi: 10.2478/s11686-019-00110-3
Sgroi G, Varcasia A, Dessi G, D’Alessio N, Tamponi C, Saarma U, et al. Cystic echinococcosis in wild boars (Sus scrofa) from southern Italy: epidemiological survey and molecular characterization. Int J Parasitol Parasites Wildl. 2019;9:305–11.
pubmed: 31338291 pmcid: 6626981 doi: 10.1016/j.ijppaw.2019.04.013
Sgroi G, Varcasia A, D’Alessio N, Varuzza P, Buono F, Amoroso MG, et al. Taenia hydatigena cysticercosis in wild boar (Sus scrofa) from southern Italy: an epidemiological and molecular survey. Parasitology. 2020;147:1636–42.
pubmed: 32829716 pmcid: 7708990 doi: 10.1017/S0031182020001559
Hegglin D, Deplazes P. Control strategy for Echinococcus multilocularis. Emerg Infect Dis. 2008;14:1626–8.
pubmed: 18826831 pmcid: 2609876 doi: 10.3201/eid1410.080522
König A, Romig T, Janko C, Hildenbrand R, Holzhofer E, Kotulski Y, et al. Integrated-baiting concept against Echinococcus multilocularis in foxes is successful in southern Bavaria, Germany. Eur J Wildl Res. 2008;54:439–47.
doi: 10.1007/s10344-007-0168-1
Comte S, Raton V, Raoul F, Hegglin D, Giraudoux P, Deplazes P, et al. Fox baiting against Echinococcus multilocularis: contrasted achievements among two medium size cities. Prev Vet Med. 2013;111:147–55.
pubmed: 23642656 doi: 10.1016/j.prevetmed.2013.03.016
Hegglin D, Deplazes P. Control of Echinococcus multilocularis: strategies, feasibility and cost-benefit analyses. Int J Parasitol. 2013;43:327–37.
pubmed: 23384814 doi: 10.1016/j.ijpara.2012.11.013
Craig PS, Larrieu E. Control of cystic echinococcosis/hydatidosis: 1863–2002. Adv Parasitol. 2006;61:443–508.
pubmed: 16735171 doi: 10.1016/S0065-308X(05)61011-1
Hegglin D, Bontadina F, Gloor S, Romer J, Müller U, Breitenmoser U, et al. Baiting red foxes in an urban area: a camera trap study. J Wildl Manage. 2004;68:1010–7.
doi: 10.2193/0022-541X(2004)068[1010:BRFIAU]2.0.CO;2
Caputo E, de Alteriis G, Conte C, Nocerino M, Pepe P, Elia S, et al. Development of an embedded system-based dropper payload for drones. In: IEEE 9th international workshop on metrology for AeroSpace (MetroAeroSpace); 2022. p. 639–643.
Da Silva AM, Bastien M, Umhang G, Boué F, Bastid V, Boucher JM, et al. Soil contamination by Echinococcus multilocularis in rural and urban vegetable gardens in relation to fox, cat and dog faecal deposits. Parasite. 2021;28:74.
pubmed: 34723788 pmcid: 8559720 doi: 10.1051/parasite/2021073

Auteurs

Martina Nocerino (M)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.

Paola Pepe (P)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy. paola.pepe@unina.it.

Antonio Bosco (A)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.
Regional Reference Centre for Animal Health (CRESAN), Naples, Campania Region, Italy.

Elena Ciccone (E)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.
Regional Reference Centre for Animal Health (CRESAN), Naples, Campania Region, Italy.

Maria Paola Maurelli (MP)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.
Regional Reference Centre for Animal Health (CRESAN), Naples, Campania Region, Italy.

Franck Boué (F)

ANSES, Nancy Laboratory for Rabies and Wildlife Diseases, Technopôle Agricole et Vétérinaire, BP 40009, 54220, Malzéville, France.

Gérald Umhang (G)

ANSES, Nancy Laboratory for Rabies and Wildlife Diseases, Technopôle Agricole et Vétérinaire, BP 40009, 54220, Malzéville, France.

Justine Pellegrini (J)

ANSES, Nancy Laboratory for Rabies and Wildlife Diseases, Technopôle Agricole et Vétérinaire, BP 40009, 54220, Malzéville, France.

Samia Lahmar (S)

Laboratoire de Parasitologie, École Nationale de Médecine Vétérinaire, 2020 Sidi Thabet, Univ., Manouba, Tunisie.

Yousra Said (Y)

Laboratoire de Parasitologie, École Nationale de Médecine Vétérinaire, 2020 Sidi Thabet, Univ., Manouba, Tunisie.

Smaragda Sotiraki (S)

Veterinary Research Institute, Hellenic Agricultural Organisation-Demeter, 57001, Thessaloniki, Greece.

Panagiota Ligda (P)

Veterinary Research Institute, Hellenic Agricultural Organisation-Demeter, 57001, Thessaloniki, Greece.

AbdElkarim Laatamna (A)

Laboratory of Exploration and Valorization of Steppic Ecosystems, Faculty of Nature and Life Sciences, University of Djelfa, Moudjbara Road, BP 3117, Djelfa, Algeria.

Giorgio Saralli (G)

Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, Rome, Italy.

Orlando Paciello (O)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.

Maria Chiara Alterisio (MC)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.

Laura Rinaldi (L)

Department of Veterinary Medicine and Animal Production, University of Naples Federico II, CREMOPAR, 80137, Naples, Italy.
Regional Reference Centre for Animal Health (CRESAN), Naples, Campania Region, Italy.

Classifications MeSH