Interaction between canine and human visceral leishmaniases in a holoendemic focus of Central Tunisia

Acta Tropica

Volumn 139, Issue , 2014, Pages 32-38

  Zoghlami, Z ^a   Chouihi, E ^a   Barhoumi, W ^a   Dachraoui, K ^a   Massoudi, N ^a   Helel, K Ben ^b   Habboul, Z ^b   Hadhri, M H ^c   Limam, S ^d   Mhadhbi, M ^d   Gharbi, M ^d   Zhioua, E ^a  

^a PASTEUR INSTITUTE OF TUNIS   (Tunisia)

^b Pediatric Department University Hospital of Kairouan   (Tunisia)

^c Regional Department of Health Governorate of Kairouan   (Tunisia)

^d Ecole Nationale de Medecine Veterinaire   (Tunisia)

Author keywords

Canine visceral leishmaniasis; Dogs; Human visceral leishmaniasis; Humans; Phlebotomine; Sand fly vectors

Indexed keywords

ABUNDANCE; ANTIBODY; CANID; DISEASE PREVALENCE; DISEASE TRANSMISSION; DNA; ENDEMIC SPECIES; FAUNA; FLY; RISK FACTOR; CHILD HEALTH; DISEASE;

AGE DISTRIBUTION; ARTICLE; CANINE VISCERAL LEISHMANIASIS; CHILD; CONTROLLED STUDY; DIPTERA; DISEASE ASSOCIATION; DISEASE TRANSMISSION; ENDEMIC DISEASE; FAUNA; FEMALE; GEOGRAPHIC DISTRIBUTION; HUMAN; HUMAN VISCERAL LEISHMANIASIS; IMMUNOFLUORESCENCE TEST; INCIDENCE; INFECTION RATE; INFECTION RISK; LEISHMANIA INFANTUM; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PHLEBOTOMUS LANGERONI; PHLEBOTOMUS LONGICUSPIS; PHLEBOTOMUS PAPATASI; PHLEBOTOMUS PERNICIOSUS; PHLEBOTOMUS SERGENTI; POPULATION ABUNDANCE; PRESCHOOL CHILD; SAND FLY; SERGENTOMYIA; SERGENTOMYIA MINUTA; SEROPREVALENCE; TUNISIA; VISCERAL LEISHMANIASIS; ZOOLOGY; BLOOD SAMPLING; DISEASE SURVEILLANCE; DOG DISEASE; DOMESTIC ANIMAL; INFANT; PARASITE TRANSMISSION; PHLEBOTOMUS; SEX DIFFERENCE; SPECIES IDENTIFICATION; ANIMAL; BLOOD; DISEASE CARRIER; DOG; DOG DISEASES; LEISHMANIASIS, VISCERAL; PARASITOLOGY; VETERINARY; ZOONOSES;

MEDITERRANEAN SEA; TUNISIA; KAIROUAN;

CANIS FAMILIARIS; PHLEBOTOMINAE;

PROTOZOON ANTIBODY;

ANIMALS; ANTIBODIES, PROTOZOAN; DOG DISEASES; DOGS; FEMALE; HUMANS; INSECT VECTORS; LEISHMANIASIS, VISCERAL; MALE; PHLEBOTOMUS; SEROEPIDEMIOLOGIC STUDIES; TUNISIA; ZOONOSES;

EID: 84904464897     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2014.06.012     Document Type: Article

References (71)

1. Abonnenc E. Les phlébotomes de la région éthiopienne (Diptera, Psychodidae). Mém. ORSTOM 1972, 55:289.
2. Anderson C. Chronique du kala azar. Arch. Inst. Pasteur Tunis 1938, 27:97-104.
3. Aoun K., Diwani M.F., Benikhlef R., Bouratbine A., Ben Haj Ali S., Harrat Z., Benlkaïd M., Kilani M., Ben Ismail R. Leishmania infantum MON-1: seul zymodème isolé chez les chiens leishmaniens en Tunisie. Bull. Soc. Pathol. Exot. 2003, 96:77-79.
4. Aoun K., Amri F., Chouihi E., Houas N., Bedoui K., Benikhelf R., Ghrab J., Baba H., Chahed M.K., Harrat Z., Bouratbine A. Epidémiologie de Leishmania (L.) infantum, L. majoret L. killicki en Tunisie: résultats et analyse de l'identification de 226 isolats humains et canins et revue de la littérature. Bull. Soc. Pathol. Exot. 2008, 101:323-328.
5. Aransay A.M., Scoulica E., Tselentis Y. Detection and identification of Leishmania DNA with naturally infected sand flies by seminested PCR on minicircle kinetoplastic DNA. Appl. Environ. Microbiol. 2000, 66:1933-1938.
6. Athansiou L.V., Kontos V.I., Saridomichelakis M.N., Rallis T.S., Diakou A. A cross-sectional sero-epidemiological study of canine leishmaniasis in Greek mainland. Acta Trop. 2012, 122:291-295.
7. Ayadi A., Ben Ismail R., Ben Rachid M.S. Extension de l'aire de transmission du Kala Azar à Leishmania infantum (Nicolle 1908) vers le centre et le sud de la Tunisie. Arch. Inst. Pasteur Tunis 1991, 68:269-273.
8. Baneth G., Dank G., Keren-Kornblatt E., Sekeles E., Adini I., Eisenberger C.L., Schnur L.F., King R., Jaffe C.L. Emergence of visceral leishmaniasis in central Israel. Am. J. Trop. Med. Hyg. 1998, 59:722-725.
9. Barhoumi W., Chelbi I., Zhioua E. Effet du développement des systèmes d'irrigation dans les zones arides sur l'établissement de Phlebotomus (Larroussius) perfiliewi Parrot, 1939. Bull. Soc. Pathol. Exot. 2012, 105:403-405.
10. Beier J.C., El Sawaf B.M., Merdan A.I., El Said S., Doha S. Sand flies (Dipetra: Psychodidae) associated with visceral leishmaniasis in El Agamy, Alexandria governorate, Egypt. J. Med. Entomol. 1986, 23:600-608.
11. Belhadj S., Partlong F., Toumi N.H., Kallel K., Mahjoub H., Baba H., Azaiez R., Dedei J.P., Chaker E. Visceral leishmaniasis in Tunisia: result of the isoenzymatic characterization of 65 Leishmania infantum strains. Trans. R. Soc. Trop. Med. Hyg. 2002, 96:627-630.
12. Ben Ammar R., Ben Ismail R., Helal H., Bach-Hamba D., Chaouch A., Bouden L., Hanachi A., Zemzari A., Ben Rachid M.S. Un nouveau foyer de leishmaniose cutanée de type rural dans la région de Sidi Saad, Tunisie. Bull. Soc. Fr. Parasitol. 1984, 2:9-12.
13. Ben Ismail R. Incrimination de Phlebotomus perniciosus comme vecteur de Leishmania infantum. Arch. Inst. Pasteur Tunis 1993, 70:91-110.
14. Ben Ismail R., Gramiccia M., Gradoni L., Helal H., Ben Rachid M.S. Isolation of Leishmania major from Phlebotomus papatasi in Tunisia. Trans. R. Soc. Trop. Med. Hyg. 1987, 81:749.
15. Ben Ismail R., Gramiccia M., Gardoni L., Ben Said M., Ben Rachid M.S. Identificazione biochemical di isolati Leishmania dell Tunisia. Paras 1987, Parassitologia 28:186-187.
16. Ben Rachid M.S., Hamza B., Tabbane C., Gharbi R., Jedidi H., Ben Said M. Etat actuel des leishmanioses en Tunisie. Ann. Soc. Belg. Méd. Trop. 1983, 63:29-40.
17. Ben Said M., Jaiem A., Smoorenburg M., Semiao-Santos S.J., Ben Rachid M.S., El Harith A. La leishmaniose canine dans la région d'Enfidha (Tunisie Centrale). Bull. Soc. Pathol. Exot. 1992, 85:159-163.
18. Ben Salah A., Ben Ismail R., Amri F., Chlif S., Ben Rzig F., Kharrat H., Hadhri H., Hassouna M., Dellagi K. Investigation of the spread of human visceral leishmaniasis in Central Tunisia. Trans. R. Soc. Trop. Med. Hyg. 2000, 94:382-386.
19. Ben Salah A., Kamarianakis Y., Chlif S., Ben Alya N., Prastacos P. Zoonotic cutaneous leishmaniasis in central Tunisia: spatio-temporal dynamics. Int. J. Epidemiol. 2007, 36:991-1000.
20. Ben Salah A., Smaoui H., Mbarki L., Anderson R.M., Ben Ismail R. Développement d'un modèle mathématique de la dynamique de transmission de la leishmaniose canine. Arch. Inst. Pasteur Tunis 1994, 71:431-438.
21. Berdjane-Brouk Z., Charrel R., Hamrioui B., Izri A. First detection of Leishmania infantum DNA in Phlebotomus longicuspis Nitulescu, 1930 from visceral leishmaniasis endemic focus in Algeria. Parasitol. Res. 2012, 111:419-422.
22. Besbes A., Pousse H., Ben Said M., Kharrat H., Chenimi L. Leishmanioses viscérales infantiles du centre tunisien, (221 cas). Méd. Mal. Infect. 1994, 24:628-634.
23. Bouratbine A., Aoun K., Gharbi M., Houas N., Zaroui J., Harrat Z., Baba H., Darghouth M.A. Données épidémiologiques, cliniques et parasitologiques sur la leishmaniose générale canine en Tunisie. Bull. Soc. Pathol. Exot. 2005, 98:359-362.
24. Bouratbine A., Aoun K., Chahed M.K., Ben Ismail R. Données épidémiologiques sur la leishmaniose viscerale infantile en Tunisie en 1993. Méd. Mal. Infect. 1998, 28:446-447.
25. Cardoso L., Mendäo C., de Carvalho L.M. Prevalence of Dirofilaria immitis, Ehrlichia canis, Borrelia burgdorferi sensu lato, Anaplasma spp., and Leishmania infantum in apparently healthy and CVBD-suspect dogs in Portugal-a national serological survey. Parasite Vectors 2013, 52:62.
26. Chadli A., Ben Rachid M.S., Fhaïel A. Chronique des leishmanioses en Tunisie. Arch. Inst. Pasteur Tunis 1968, 45:1-14.
27. Chaniotis B., Tselentis Y. Water wells as habitat of sand fly (Diptera: Psychodidae) vectors of visceral leishmaniasis in Greece. J. Med. Entomol. 1996, 33:269-270.
28. Chargui N., Houas N., Gordii M., Akrout Messaidi F., Zribi M., Baba H. Increase of canine leishmaniasis in a previously low-endemicity area in Tunisia. Parasite 2007, 14:247-251.
29. Chargui N., Houas N., Slama D., Gorcii M., Jaouadi K., Essabah-Aguir N., Mezhoud H., Baba H. Transmission of visceral leishmaniasis in a previously non-endemic region of Tunisia: detection of Leishmmania DNA in Phlebotomus perniciosus. J. Vector Ecol. 2012, 38:1-5.
30. Chelbi I., Derbali M., A.L-Ahmadi Z., Zaafouri B., El Fahem A., Zhioua E. Phenology of Phlebotomus papatasi (Diptera: Psychodidae) relative to the seasonal prevalence of zoonotic cutaneous leishmaniasis in Central Tunisia. J. Med. Entomol. 2007, 44:385-388.
31. da Costa-Val A.P., Cavalcanti R.R., de Figueiredo Gontijo N., Michalick M.S., Alexander B., Williams P., Melo M.N. Canine visceral leishmaniasis: relationship between clinical status, humoral immune response, haematology and Lutzomyia (Lutzomyia) longipalpis infectivity. Vet. J. 2007, 174:636-643.
32. Croset H., Rioux J.A., Master M., Bayar N. Les phlébotomes de la Tunisie (Diptera, Phlebotominae). Mise au point systématique, chorologique et éthologique. Ann. Parasitol. Hum. Comp. 1978, 53:711-749.
33. Cruz I., Acosta L., Gutiérrez M.N., Nieto J., Canavate C., Deschutter J., Bornay-Llinares F.J. A canine leishmaniasis pilot survey in an emerging focus of visceral leishmaniasis: Posadas (Misiones, Argentina). BMC Infect. Dis. 2010, 10:342.
34. Cruz I., et al. A nested polymerase chain reaction (LnPCR) for diagnosing and monitoring Leishmania infantum infection in patients co-infected with human immunodeficiency virus. Trans. R. Soc. Trop. Med. Hyg. 2002, 96(S1):185-189.
35. Dedet J.P., Ben Osman F., Chadli A., Croset H., Rioux J.A. La leishmaniose canine en Tunisie; fréquences actuelles de l'enzootie d'après une enquête séro-immunologique. Ann. Parasitol. Hum. Comp. 1973, 48:653-660.
36. Diwani F., Ben Alay Bouafif N., Bettaib J., Louzir H., Jedidi S., Ftaiti A., Zaatour A., Jomma I., Dellagi K., Ben Ismail R., Ben Salah A. Dogs Leishmania infantum infection from endemic region of the North of Tunisia: a prospective study. Arch. Inst. Pasteur Tunis 2008, 85:55-61.
37. Doha S., Shehata M.G. Leishmania infantum MON-98 isolated from naturally infected Phlebotomus langeroni (Diptera: Psychodidae) in El Agamy, Egypt. J. Med. Entomol. 1992, 29:891-893.
38. Dogan N., Ozbel Y., Toz S.O., Dinleyici E.C., Bor O. Sero-epidemiological survey on canine visceral leishmaniasis and the distribution of sandfly vectors in Northwestern Turkey: prevention strategies for childhood visceral leishmaniasis. J. Trop. Pediatr. 2006, 52:212-217.
39. DSSB, 2011. Direction Nationale de Soin de Santé de Base. Ministry of Health of Tunisia. Bull. Epidémiol., 2011.
40. DSSB, 2012. Direction Nationale de Soin de Santé de Base. Ministry of Health of Tunisia. Bull. Epidémiol, 2012.
41. Dye C. The logic of visceral leishmaniasis control. Am. J. Trop. Med. Hyg. 1996, 55:125-130.
42. Ghrab J., Rhaim A., Bach Hamba D., Chahed M.K., Aoun K., Nouira S., Bouratbine A. Phlebotominae (Diptera: Psychodidae) of human leishmaniosis sites in Tunisia. Parasite 2006, 13:23-33.
43. Guarnaoui S., Pesson B., Boumezzough A., Pichon G. Distribution of phlebotomine sandflies of the subgenus Larroussius, in Morocco. Med. Vet. Entomol. 2005, 19:111-115.
44. Guerbouj S., Chemki J., Kaabi B., Rahali A., Ben Ismail R., Guizani I. Natural infection of Phlebotomus (Larrousius) langeroni (Diptera; Psychodidae) with Leishmania infantum in Tunisia. Trans. R. Soc. Trop. Med. Hyg. 2007, 101:372-377.
45. Haddadzade H.R., Fattahi R., Mohebali M., Akhoundi B., Ebrahimzade E. Seroepidemiological investigation of visceral leishmaniasis in stray and owned dogs in Albroz province, Central Iran using direct agglutination test. Iran J. Parasitol. 2013, 8:152-157.
46. Hamarsheh O., Naserddin A., Damaj S., Sawalha S., Al-Jawabreh H., Azmi K., Amro A., Erqat S., Abdeen Z., Al-Jawabreh A. Serological and molecular survey of Leishmania parasites in apparently healthy dogs in the West Bank, Palestine. Parasite Vectors 2013, 5:183.
47. Hasibeder G., Dye C., Carpenter J. Mathematical modelling and theory for estimating the basic reproduction number of canine leishmaniasis. Parasitology 1992, 105:43-53.
48. Izri M.A., Belazzoug S. Phlebotomus (Larroussius) perfiliewi naturally infected with dermotropic Leishmania infantum at Tenes; Algeria. Trans. R. Soc. Trop. Med. Hyg. 1993, 87:399.
49. Izri M.A., Belazzoug S., Boudjebla Y., Dereure J.P., Pratlong F., Delabre-Belmonte A., Rioux J.A. Leishmania infantum MON1 isolé de Phlebotomus perniciosus en Kabylie (Algérie). Ann. Parasitol. Hum. Comp. 1990, 65:151-152.
50. Jambou D., Marty P., Jambou R., Le Fichoux Y., Haas P., Jourdain N., Bayada M. Preliminary serological study on canine leishmaniasis in the Alpes-Maritimes department, France. Trans. R. Soc. Trop. Med. Hyg. 1986, 80:666-667.
51. Keddous A. Enquête éco-épidémiologique sur le kala azar dans le gouvernorat de Sidi Bouzid. Etude d'un réservoir canin. (M.D. thesis) 1988, Medical School of Tunis, (p. 152).
52. Kovalenko D.A., Razakov S.A., Ponirovsky E.N., Nasyrova R.M., Ponomareva V.I., Fatullaeva A.A., Naserddin A., Klement E., Alam M.Z., Schnur L., Jaffe C.L., Schönian G., Baneth G. Canine leishmaniosis and its relationship to human visceral leishmaniasis in Eastern Uzbekistan. Parasite Vectors 2011, 4:58.
53. Lachaud L., Marcherhui-Hammami S., Chabbert E., Dereure J., Dedet J.P., Bastien P. Comparaison of six PCR methodsusing peripheral blood for detection of canine leishmaniasis. J. Clin. Microbiol. 2002, 40:210-215.
54. Margonari C., Freitas C.R., Ribeiro R.C., Moura A.C.M., Timbo M., Gripp A.H., Pessanha J.P., Dias E.S. Epidemiology of visceral leishmaniasis through spatial analysis, in Belo Horizonte municipality, state of Minas Gerais, Brazil. Mem. Inst. Oswaldo Cruz 2006, 101:31-38.
55. Maroli M., Gramiccia M., Gradoni L. Natural infection of sandfly Phlebotomus perfiliewi with Leishmania infantum in a cutaneous leishmaniasis focus of the Abruzzi region, Italy. Trans. R. Soc. Trop. Med. Hyg. 1987, 8:596-598.
56. Maroli M., Gramiccia M., Gradoni L., Troiani M., Ascione R. Natural infection of Phlebotomus perniciosus with an enzymatic variant of Leishmania infantum in the Campania region of Italy. Acta Trop. 1994, 57:333-335.
57. Michalsky E.M., Rocha M.F., da Rocha Lima A.C., França-Silva J.C., Pires M.Q., Oliveira F.S., Pacheco R.S., dos Santos S.L., Barata R.A., Romanha A.J., Fortes-Dias C.L., Dias E.S. Infectivity of seropostive dogs, showing different clinical forms of leishmaniasis to Lutzomyia longipalpis phlebotomine sand flies. Vet. Parasitol. 2007, 147:67-76.
58. Miro G., Checa R., Montoya A., Hernandez L., Dado D., Galvez R. Current situation of Leishmania infantum infection in shelter dogs in northern Spain 2012. Parasite Vectors 2012, 5:60.
59. Molina R., Amela C., Nieto J., San-Andrés M., Gonzalez F., Castillo J.A., Lucientes J., Alvar J. Infectivity of dogs naturally infected with Leishmania infantum to colonized Phlebotomus perniciosus. Trans. R. Soc. Trop. Med. Hyg. 1994, 88:491-493.
60. Nicolle C., Compte C. Origine canine du kala azar. Arch. Inst. Pasteur Tunis 1908, 3:99-103.
61. Otranto D., Paradies P., de Carariis D., Stanneck D., Testini G., Grimm F., Deplazes P., Capelli G. Toward diagnosing Leishmania infantum infection in asymptomatic dogs in an area where leishmaniasis is endemic. Clin. Vaccine Immunol. 2009, 16:337-343.
62. Rossi E., Bongiorno G., Ciolli E., Muccio T.Di.Scalone A., Gramiccia M., Gradoni L., Maroli M. Seasonal phenology, host-blood feeding preferences and natural infection of Phlebotomus perniciosus (Diptera, Psychodidae) in a high-endemic focus of canine leishmaniasis in Rome province, Italy. Acta Trop. 2008, 105:158-165.
63. da Silva C.B., Vilela J.A.R., Pires M.S., Santos H.A., Falqueto A., Peixoto M.P., Oliveira T.A., Santos F.N., Silva V.L., Sanavria A., Massard C.L. Seroepidemiological aspects of Leishmania spp. in dogs in the Itaguai micro-region, Rio de Janeiro, Brazil. Rev. Bras. Parasitol. Vet. 2013, 22:39-45.
64. Solano-Gallego L., Morell P., Arboix M., Alberola J., Ferrer L. Prevalence of Leishmania infantum infection in dogs living in an area of canine leishmaniasis endemicity using PCR on several tissues and serology. J. Clin. Microbiol. 2001, 39:560-563.
65. Queiroz P.V.S., Monteiro G.R.G., Macedo V.P.S., Rocha M.A.C., Batista L.M.M., Queiroz J.W., Jeronimo S.M.B., Ximenes M.F.F.M. Canine visceral leishmaniasis in urban and rural areas of Northeast Brazil. Res. Vet. Sci. 2009, 86:267-273.
66. van Eys G.J., Schoone G.J., Kroon N.C., Ebeling S.B. Sequence analysis of small subunit ribosomal RNA genes and its use for detection and identification of Leishmania parasites. Mol. Biochem. Parasitol. 1992, 51:133-142.
67. Vermeil C. Chronique des leishmanioses en Tunisie. Arch. Inst. Pasteur Tunis 1956, 33:195-201.
68. Wang J.Y., Ha Y., Gao C.H., Wang Y., Yang Y.T., Chen H.T. The prevalence of canine Leishmania infantum infection in western China detected by PCR serological tests. Parasite Vectors 2011, 4:69.
69. Werneck G.L., Costa C.H.N., Walker A.M., David J.R., Wand M., Maguire J.H. Multilevel modelling of the incidence of visceral leishmaniasis in Teresina, Brazil. Epidemiol. Infect. 2007, 135:195-201.
70. Yavar R., Hadi K., Reza A.M., Mohebali M., Hasan B., Ali O.M., Sina R., Habib B.H., Abodolrahim H., Manuchehr G. First detection of Leishmania infantum DNA in wild caught Phlebotomus papatasi in endemic focus of cutaneous leishmaniasis, south of Iran. Asian Pac. J. Trop. Biomed. 2013, 3:825-829.
71. Zhioua E., Kaabi B., Chelbi I. Entomological investigations following the spread of visceral leishmaniasis in Tunisia. J. Vector Ecol. 2007, 32:371-374.